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4 - Anatomy and physiology of hematopoiesis

from Part II - Cell biology and pathobiology

Published online by Cambridge University Press:  01 July 2010

Connie J. Eaves
Affiliation:
Deputy Director Terry Fox Laboratory, Vancouver, British Columbia, Canada
Allen C. Eaves
Affiliation:
Director Terry Fox Laboratory, Vancouver, British Columbia, Canada
Ching-Hon Pui
Affiliation:
St. Jude Children's Research Hospital, Memphis
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Summary

Introduction

Hematopoiesis refers to all aspects of the process of blood cell production. Understanding this process requires a comprehensive knowledge of both the anatomy and the physiology of the blood-forming system. Here, the anatomy of the hematopoietic system is viewed as the distinguishable stages of differentiation that together make up the complete hierarchy of hematopoietic cells. These stages reflect the changes that initially endow cells in the embryo with hematopoietic differentiation potential (a step referred to as specification), in addition to those that subsequently constitute the processes of lineage restriction and terminal differentiation. The physiology of hematopoiesis refers to the dynamic aspects of these events and covers issues such as the determination of alternate outcomes, at both the cellular and molecular level, as well as their modulation during development and in response to injury or disease.

Leukemias arise from clonal accumulations of mutations that impact the production and differentiation of blood cells. Because of the low probability of such events, a large number of divisions is thought to be required for their successive acquisition. It is therefore not surprising that, in many leukemias, the first leukemogenic mutation appears to take place in a hematopoietic stem cell. Moreover, in spite of the acute picture of many leukemias, there is growing evidence that they may result from relatively subtle perturbations of the mechanisms that regulate normal hematopoiesis. A framework for understanding normal hematopoiesis is therefore essential to obtaining new insights into the nature and better management of these diseases.

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Childhood Leukemias , pp. 69 - 105
Publisher: Cambridge University Press
Print publication year: 2006

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References

Williams, W. J., Beutler, E., Erslev, A. J., & Lichtman, M. A. (eds.). Hematology, 4th edn (New York: McGraw-Hill, 1990).Google Scholar
Killmann, S. A., Cronkite, E. P., Fliedner, T. M., & Bond, V. P.Mitotic indices of human bone marrow cells. I. Number and cytologic distribution of mitoses. Blood, 1962; 19: 743–50.Google ScholarPubMed
Killmann, S. A., Cronkite, E. P., Fliedner, T. M., & Bond, V. P.Mitotic indices of human bone marrow cells. III. Duration of some phases of erythrocytic and granulocytic proliferation computed from mitotic indices. Blood, 1964; 24: 267–80.Google Scholar
Warner, H. R., & Athens, J. W.An analysis of granulocyte kinetics in blood and bone marrow. Ann N Y Acad Sci, 1964; 113: 523–36.CrossRefGoogle ScholarPubMed
Dameshek, W.Some speculations on the myeloproliferative syndromes. Blood, 1951; 6: 372–5.Google ScholarPubMed
Barnes, D. W. H., Ford, C. E., Gray, S. M., & Loutit, J. F. Spontaneous and induced changes in cell populations in heavily irradiated mice. In , J. C. Bugher, , J. Coursaget, & , J. F. Loutit, eds., Progress in Nuclear Energy (Series Ⅵ) (London: Pergamon Press, 1959), pp. 1–10.Google Scholar
Whang, J., Frei, E. III, Tjio, J. H., Carbone, P. P., & Brecher, G.The distribution of the Philadelphia chromosome in patients with chronic myelogenous leukemia. Blood, 1963; 22: 664–73.Google ScholarPubMed
Rastrick, J. M., Fitzgerald, P. H., & Gunz, F. W.Direct evidence for presence of Ph1 chromosome in erythroid cells. Br Med J, 1968; 1: 96–8.CrossRefGoogle Scholar
Turhan, A. G., Humphries, R. K., Phillips, G. L., Eaves, A. C., & Eaves, C. J.Clonal hematopoiesis demonstrated by X-linked DNA polymorphisms after allogeneic bone marrow transplantation. N Engl J Med, 1989; 320: 1655–61.CrossRefGoogle ScholarPubMed
Eaves, C. J. Myelopoiesis. In , E. S. Henderson, , T. A. Lister, & , M. F. Greaves, eds., Leukemia, 7th edn. (Philadelphia, PA: W. B. Saunders, 2002), pp. 19–45.
Palis, J., Robertson, S., Kennedy, M., Wall, C., & Keller, G.Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development, 1999; 126: 5073–84.Google ScholarPubMed
Moore, M. A. S. & Metcalf, D.Ontogeny of the haemopoietic system; yolk sac origin of in vivo and in vitro colony forming cell in the developing mouse embryo. Br J Haematol, 1970; 18: 279–86.CrossRefGoogle ScholarPubMed
Houssaint, E.Differentiation of the mouse hepatic primordium. II. Extrinsic origin of the haemopoietic cell line. Cell Differ, 1981; 10: 243–52.CrossRefGoogle ScholarPubMed
Wong, P. M. C., Chung, S. W., Chui, D. H. K., & Eaves, C. J.Properties of the earliest clonogenic hemopoietic precursors to appear in the developing murine yolk sac. Proc Natl Acad Sci U S A, 1986; 83: 3851–4.CrossRefGoogle ScholarPubMed
Huang, H., Zettergren, L. D., & Auerbach, R.In vitro differentiation of B cells and myeloid cells from the early mouse embryo and its extraembryonic yolk sac. Exp Hematol, 1994; 22: 19–25.Google ScholarPubMed
Dzierzak, E.Hematopoietic stem cells and their precursors: developmental diversity and lineage relationships. Immunol Rev, 2002; 187: 126–38.CrossRefGoogle ScholarPubMed
Peault, B. & Tavian, M.Hematopoietic stem cell emergence in the human embryo and fetus. Ann N Y Acad Sci, 2003; 996: 132–40.CrossRefGoogle ScholarPubMed
Johnson, G. R. & Moore, M. A. S.Role of stem cell migration in initiation of mouse foetal liver haemopoiesis. Nature, 1975; 258: 726–8.CrossRefGoogle ScholarPubMed
Delassus, S. & Cumano, A.Circulation of hematopoietic progenitors in the mouse embryo. Immunity, 1996; 4: 97–106.CrossRefGoogle ScholarPubMed
Eaves, C. J.Manipulating hematopoietic stem cell amplification with Wnt. Nat Immunol, 2003; 4: 511–2.CrossRefGoogle ScholarPubMed
Reya, T., Duncan, A. W., Ailles, L., et al.A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature, 2003; 423: 409–14.CrossRefGoogle ScholarPubMed
Rich, I. N. & Kubanek, B.The ontogeny of erythropoiesis in the mouse detected by the erythroid colony-forming technique. J Embryol Exp Morphol, 1980; 58: 143–55.Google ScholarPubMed
Roodman, G. D. & Zanjani, E.Endogenous erythroid colony-forming cells in fetal and newborn sheep. J Lab Clin Med, 1979; 94: 699–707.Google ScholarPubMed
Nakano, T., Kodama, H., & Honjo, T.In vitro development of primitive and definitive erythrocytes from different precursors. Science, 1996; 272: 722–4.CrossRefGoogle ScholarPubMed
Migliaccio, A. R. & Migliaccio, G.Human embryonic hemopoiesis: control mechanisms underlying progenitor differentiation in vitro. Dev Biol, 1988; 125: 127–34.CrossRefGoogle ScholarPubMed
Kurata, H., Mancini, G. C., Alespeiti, G., Migliaccio, A. R., & Migliaccio, G.Stem cell factor induces proliferation and differentiation of fetal progenitor cells in the mouse. Br J Haematol, 1998; 101: 676–87.CrossRefGoogle ScholarPubMed
Miller, C. L., Rebel, V. I., Lemieux, M. E., et al.Studies of W mutant mice provide evidence for alternate mechanisms capable of activating hematopoietic stem cells. Exp Hematol, 1996; 24: 185–94.Google ScholarPubMed
Miller, C. L., Rebel, V. I., Helgason, C. D., Lansdorp, P. M., & Eaves, C. J.Impaired steel factor responsiveness differentially affects the detection and longterm maintenance of fetal liver hematopoietic stem cells in vivo. Blood, 1997; 89: 1214–23.Google Scholar
Roy, V., Miller, J. S., & Verfaillie, C. M.Phenotypic and functional characterization of committed and primitive myeloid and lymphoid hematopoietic precursors in human fetal liver. Exp Hematol, 1997; 25: 387–94.Google ScholarPubMed
Glimm, H. & Eaves, C. J.Direct evidence for multiple self-renewal divisions of human in vivo repopulating hematopoietic cells in short-term culture. Blood, 1999; 94: 2161–8.Google ScholarPubMed
Barker, J. E.Development of the mouse hematopoietic system. Dev Biol, 1968; 18: 14–29.CrossRefGoogle ScholarPubMed
Kazazian, H. H. Jr. & Woodhead, A. P.Hemoglobin A synthesis in the developing fetus. N Engl J Med, 1973; 289: 58–62.CrossRefGoogle ScholarPubMed
Weissman, I. L.Developmental switches in the immune system. Cell, 1994; 76: 207–18.CrossRefGoogle ScholarPubMed
Sanchez, M.-J., Holmes, A., Miles, C., & Dzierzak, E.Characterization of the first definitive hematopoietic stem cells in the AGM and liver of the mouse embryo. Immunity, 1996; 5: 513–25.CrossRefGoogle ScholarPubMed
Yoder, M. C., Hiatt, K., Dutt, P., et al.Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity, 1997; 7: 335–44.CrossRefGoogle ScholarPubMed
Huang, H. & Auerbach, R.Identification and characterization of hematopoietic stem cells from the yolk sac of the early mouse embryo. Proc Natl Acad Sci U S A, 1993; 90: 10110–4.CrossRefGoogle ScholarPubMed
Morrison, S. J., Hemmati, H. D., Wandycz, A. M., & Weissman, I. L.The purification and characterization of fetal liver hematopoietic stem cells. Proc Natl Acad Sci U S A, 1995; 92: 10302–6.CrossRefGoogle ScholarPubMed
Randall, T. D. & Weissman, I. L.Phenotypic and functional changes induced at the clonal level in hematopoietic stem cells after 5-fluorouracil treatment. Blood, 1997; 89: 3596–606.Google ScholarPubMed
Rebel, V. I., Miller, C. L., Thornbury, G. R., et al.A comparison of long-term repopulating hematopoietic stem cells in fetal liver and adult bone marrow from the mouse. Exp Hematol, 1996; 24: 638–48.Google ScholarPubMed
Bhatia, M., Bonnet, D., Murdoch, B., Gan, O. I., & Dick, J. E.A newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nat Med, 1998; 4: 1038–45.CrossRefGoogle ScholarPubMed
Uchida, N., Dykstra, B., Lyons, K., et al.ABC transporter activities of murine hematopoietic stem cells vary according to their developmental and activation status. Blood, 2004; 103: 4487–95.CrossRefGoogle ScholarPubMed
Rebel, V. I., Miller, C. L., Eaves, C. J., & Lansdorp, P. M.The repopulation potential of fetal liver hematopoietic stem cells in mice exceeds that of their adult bone marrow counterparts. Blood, 1996; 87: 3500–7.Google ScholarPubMed
Pawliuk, R., Eaves, C., & Humphries, R. K.Evidence of both ontogeny and transplant dose-regulated expansion of hematopoietic stem cells in vivo. Blood, 1996; 88: 2852–8.Google ScholarPubMed
Nicolini, F. E., Holyoake, T. L., Cashman, J. D., et al.Unique differentiation programs of human fetal liver stem cells revealed both in vitro and in vivo in NOD/SCID mice. Blood, 1999; 94: 2686–95.Google Scholar
Cumano, A., Paige, C. J., Iscove, N. N., & Brady, G.Bipotential precursors of B cells and macrophages in murine fetal liver. Nature, 1992; 356: 612–15.CrossRefGoogle ScholarPubMed
Mebius, R. E., Miyamoto, T., Christensen, J., et al.The fetal liver counterpart of adult common lymphoid progenitors gives rise to all lymphoid lineages, CD45+CD4+CD3- cells, as well as macrophages. J Immunol, 2001; 166: 6593–601.CrossRefGoogle ScholarPubMed
Sheridan, B. L., Weatherall, D. J., Clegg, J. B., et al.The patterns of fetal haemoglobin production in leukaemia. Br J Haematol, 1976; 32: 487–506.CrossRefGoogle ScholarPubMed
Till, J. E. & McCulloch, E. A.A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res, 1961; 14: 213–22.CrossRefGoogle ScholarPubMed
Szilvassy, S. J., Humphries, R. K., Lansdorp, P. M., Eaves, A. C., & Eaves, C. J.Quantitative assay for totipotent reconstituting hematopoietic stem cells by a competitive repopulation strategy. Proc Natl Acad Sci U S A, 1990; 87: 8736–40.CrossRefGoogle ScholarPubMed
Conneally, E., Cashman, J., Petzer, A., & Eaves, C.Expansion in vitro of transplantable human cord blood stem cells demonstrated using a quantitative assay of their lympho-myeloid repopulating activity in nonobese diabetic-scid/scid mice. Proc Natl Acad Sci U S A, 1997; 94: 9836–41.CrossRefGoogle ScholarPubMed
Fazekas, Groth S. de St.The evaluation of limiting dilution assays. J Immunol Methods, 1982; 49: R11–23.Google Scholar
Fowler, J. H., Wu, A. M., Till, J. E., McCulloch, E. A., & Siminovitch, L.The cellular composition of hemopoietic spleen colonies. J Cell Physiol, 1967; 69: 65–72.CrossRefGoogle Scholar
Metcalf, D.Hemopoietic Colonies: In Vitro Cloning of Normal and Leukemic Cells (Berlin, Heidelberg: Springer, 1977).CrossRefGoogle ScholarPubMed
Sutherland, H. J., Lansdorp, P. M., Henkelman, D. H., Eaves, A. C., & Eaves, C. J.Functional characterization of individual human hematopoietic stem cells cultured at limiting dilution on supportive marrow stromal layers. Proc Natl Acad Sci U S A, 1990; 87: 3584–8.CrossRefGoogle ScholarPubMed
Lemieux, M. E., Rebel, V. I., Lansdorp, P. M., & Eaves, C. J.Characterization and purification of a primitive hematopoietic cell type in adult mouse marrow capable of lympho-myeloid differentiation in long-term marrow “switch” cultures. Blood, 1995; 86: 1339–47.Google Scholar
Trevisan, M. & Iscove, N.Phenotypic analysis of murine long-term hematopoietic reconstituting cells quantitated competitively in vivo and comparison with more advanced colony-forming progeny. J Exp Med, 1995; 181: 93–103.CrossRefGoogle ScholarPubMed
Audet, J., Miller, C. L., Rose-John, S., Piret, J., & Eaves, C. J.Distinct role of gp130 activation in promoting self-renewal divisions by mitogenically stimulated murine hematopoietic stem cells. Proc Natl Acad Sci U S A, 2001; 98: 1757–62.CrossRefGoogle ScholarPubMed
Osawa, M., Hanada, K. I., Hamada, H., & Nakauchi, H.Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science, 1996; 273: 242–5.CrossRefGoogle ScholarPubMed
McCulloch, E. A.Stem cells in normal and leukemic hemopoiesis. Blood, 1983; 62: 1–13.Google ScholarPubMed
Bonnet, D. & Dick, J. E.Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med, 1997; 3: 730–6.CrossRefGoogle ScholarPubMed
Raskind, W. H. & Fialkow, P. J.The use of cell markers in the study of human hematopoietic neoplasia. Adv Cancer Res, 1987; 49: 127–67.CrossRefGoogle Scholar
Fearon, E. R., Burke, P. J., Schiffer, C. A., Zehnbauer, B. A., & Vogelstein, B.Differentiation of leukemia cells to polymorphonuclear leukocytes in patients with acute nonlymphocytic leukemia. N Engl J Med, 1986; 315: 15–24.CrossRefGoogle ScholarPubMed
McCulloch, E. A., Siminovitch, L., & Till, J. E.Spleen colony formation in anemic mice of genotype W/Wv. Science, 1964; 144: 844–6.CrossRefGoogle Scholar
Juraskova, V. & Tkadlecek, L.Character of primary and secondary colonies of haematopoieses in the spleen of irradiated mice. Nature, 1965; 206: 951–2.CrossRefGoogle Scholar
Boggs, S. S., Chervenick, P. A., & Boggs, D. R.The effect of postirradiation bleeding or endotoxin on proliferation and differentiation of hematopoietic stem cells. Blood, 1972; 40: 375–89.Google ScholarPubMed
Gregory, C. J., McCulloch, E. A., & Till, J. E.Transient erythropoietic spleen colonies: effects of erythropoietin in normal and genetically anemic W/Wv mice. J Cell Physiol, 1975; 86: 1–8.CrossRefGoogle ScholarPubMed
Siminovitch, L., McCulloch, E. A., & Till, J. E.The distribution of colony-forming cells among spleen colonies. J Cell Physiol, 1963; 62: 327–36.CrossRefGoogle ScholarPubMed
Magli, M. C., Iscove, N. N., & Odartchenko, N.Transient nature of early haematopoietic spleen colonies. Nature, 1982; 295: 527–9.CrossRefGoogle ScholarPubMed
Gregory, C. J. & Henkelman, R. M. Relationships between early hemopoietic progenitor cells determined by correlation analysis of their numbers in individual spleen colonies. In , S. J. Baum & , G. D. Ledney, eds., Experimental Hematology Today (New York: Springer, 1977), pp. 93–101.Google Scholar
Hodgson, G. S. & Bradley, T. R.Properties of hematopoietic stem cells surviving 5-fluorouracil treatment: evidence for a pre-CFU-S cell ?Nature, 1979; 281: 381–2.CrossRefGoogle ScholarPubMed
Worton, R. G., McCulloch, E. A., & Till, J. E.Physical separation of hemopoietic stem cells differing in their capacity for self-renewal. J Exp Med, 1969; 130: 91.CrossRefGoogle ScholarPubMed
Bertoncello, I., Hodgson, G. S., & Bradley, T. R.Multiparameter analysis of transplantable hemopoietic stem cells. II. Stem cells of long-term bone marrow-reconstituted recipients. Exp Hematol, 1988; 16: 245–9.Google ScholarPubMed
Spangrude, G. J. & Johnson, G. R.Resting and activated subsets of mouse multipotent hematopoietic stem cells. Proc Natl Acad Sci U S A, 1990; 87: 7433–7.CrossRefGoogle ScholarPubMed
Morrison, S. J. & Weissman, I. L.The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity, 1994; 1: 661–73.CrossRefGoogle ScholarPubMed
Hodgson, G. S. & Bradley, T. R.In vivo kinetic states of hematopoietic stem and progenitor cells as inferred from labelling with bromodeoxyuridine. Exp Hematol, 1984; 12: 683–7.Google Scholar
Dumenil, D., Jacquemin-Sablon, H., Neel, H., Frindel, E., & Dautry, F.Mock retroviral infection alters the developmental potential of murine bone marrow stem cells. Mol Cell Biol, 1989; 9: 4541–4.CrossRefGoogle ScholarPubMed
Wolf, N. S., Kone, A., Priestley, G. V., & Bartelmez, S. H.In vivo and in vitro characterization of long-term repopulating primitive hematopoietic cells isolated by sequential Hoechst 33342-rhodamine123 FACS selection. Exp Hematol, 1993; 21: 614–22.Google ScholarPubMed
Ploemacher, R. E. & Brons, R. H. C.Separation of CFU-S from primitive cells responsible for reconstitution of the bone marrow hemopoietic stem cell compartment following irradiation: evidence for a pre-CFU-S cell. Exp Hematol, 1989; 17: 263–6.Google ScholarPubMed
Jones, R. J., Collector, M. I., Barber, J. P., et al.Characterization of mouse lymphohematopoietic stem cells lacking spleen colony-forming activity. Blood, 1996; 88: 487–91.Google ScholarPubMed
Metcalf, D. & Moore, M. A. S. Haematopoietic cells. In , A. Neuberger & , E. L. Tatum, eds., Frontiers of Biology (Amsterdam: North-Holland Publishing, 1971), p. 550.Google Scholar
Lahiri, S. K., Keizer, H. J., & Putten, L. M. Van.The efficiency of the assay for haemopoietic colony forming cells. Cell Tissue Kinet, 1970; 3: 355–62.Google ScholarPubMed
Testa, N. G., Lord, B. I., & Shore, N. A.The in vivo seeding of hemopoietic colony-forming cells in irradiated mice. Blood, 1972; 40: 654–61.Google ScholarPubMed
Lord, B. I. In vivo assays of multipotential and marrow repopulating cells. In , N. G. Testa & , G. Molineux, eds., Haemopoiesis: A Practical Approach (New York: Oxford University Press, 1993), pp. 1–20.Google Scholar
Wu, A. M., Till, J. E., Siminovitch, L., & McCulloch, E. A.Cytological evidence for a relationship between normal hematopoietic colony-forming cells and cells of the lymphoid system. J Exp Med, 1968; 127: 455–64.CrossRefGoogle ScholarPubMed
Dick, J. E., Magli, M. C., Huszar, D., Phillips, R. A., & Bernstein, A.Introduction of a selectable gene into primitive stem cells capable of long-term reconstitution of the hemopoietic system of W/Wv mice. Cell, 1985; 42: 71–9.CrossRefGoogle ScholarPubMed
Keller, G., Paige, C., Gilboa, E., & Wagner, E. F.Expression of a foreign gene in myeloid and lymphoid cells derived from multipotent haematopoietic precursors. Nature, 1985; 318: 149–54.CrossRefGoogle ScholarPubMed
Lemischka, I. R., Raulet, D. H., & Mulligan, R. C.Developmental potential and dynamic behavior of hematopoietic stem cells. Cell, 1986; 45: 917–27.CrossRefGoogle ScholarPubMed
Harrison, D. E.Normal production of erythrocytes by mouse marrow continuous for 73 months. Proc Natl Acad Sci U S A, 1973; 70: 3184–8.CrossRefGoogle ScholarPubMed
Szilvassy, S. J., Nicolini, F. E., Eaves, C. J., & Miller, C. L. Quantitation of murine and human hematopoietic stem cells by limiting-dilution analysis in competitively repopulated hosts. In , C. T. Jordon & , C. A. Klug, eds. Methods in Molecular Medicine: Hematopoietic Stem Cell Protocols (Totowa, NJ: Humana Press, 2002), pp. 167–87.Google Scholar
Jordan, C. T. & Lemischka, I. R.Clonal and systemic analysis of long-term hematopoiesis in the mouse. Genes Dev, 1990; 4: 220–32.CrossRefGoogle ScholarPubMed
Zhong, R.-K., Astle, C. M., & Harrison, D. E.Distinct developmental patterns of short-term and long-term functioning lymphoid and myeloid precursors defined by competitive limiting dilution analysis in vivo. J Immunol, 1996; 157: 138–45.Google ScholarPubMed
Uchida, N., Dykstra, B., Lyons, K. J., Leung, F. Y. K., & Eaves, C. J.Different in vivo repopulating activities of purified hematopoietic stem cells before and after being stimulated to divide in vitro with the same kinetics. Exp Hematol, 2003; 31: 1338–47.CrossRefGoogle ScholarPubMed
Audet, J., Miller, C. L., Eaves, C. J., & Piret, J. M.Common and distinct features of cytokine effects on hematopoietic stem and progenitor cells revealed by dose response surface analysis. Biotechnol Bioeng, 2002; 80: 393–404.CrossRefGoogle ScholarPubMed
Harrison, D. E.Competitive repopulation: a new assay for long-term stem cell functional capacity. Blood, 1980; 55: 77–81.Google ScholarPubMed
Harrison, D. E.Evaluating functional abilities of primitive hematopoietic stem cell populations. Curr Top Microbiol Immunol, 1992; 177: 13–30.Google ScholarPubMed
Benveniste, P., Cantin, C., Hyam, D., & Iscove, N. N.Hematopoietic stem cells engraft in mice with absolute efficiency. Nat Immunol, 2003; 4: 708–13.CrossRefGoogle ScholarPubMed
Matsuzaki, Y., Kinjo, K., Mulligan, R. C., & Okano, H.Unexpectedly efficient homing capacity of purified murine hematopoietic stem cells. Immunity, 2004; 20: 87–93.CrossRefGoogle ScholarPubMed
Szilvassy, S. J., Ragland, P. L., Miller, C. L., & Eaves, C. J.The marrow homing efficiency of murine hematopoietic stem cells remains constant during ontogeny. Exp Hematol, 2003; 31: 331–8.CrossRefGoogle ScholarPubMed
Kawada, H. & Ogawa, M.Bone marrow origin of hematopoietic progenitors and stem cells in murine muscle. Blood, 2001; 98: 2008–13.CrossRefGoogle ScholarPubMed
McKinney-Freeman, S. L., Jackson, K. A., Camargo, F. D., et al.Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc Natl Acad Sci U S A, 2002; 99: 1341–6.CrossRefGoogle ScholarPubMed
Uchida, N., Leung, F. Y. K., & Eaves, C. J.Liver and marrow of adult mdr-1a/1b−/− mice show normal generation, function and multi-tissue trafficking of primitive hematopoietic cells. Exp Hematol, 2002; 30: 862–9.CrossRefGoogle ScholarPubMed
Ramshaw, H. S., Rao, S. S., Crittenden, R. B., et al.Engraftment of bone marrow cells into normal unprepared hosts: effects of 5-fluorouracil and cell cycle status. Blood, 1995; 86: 924–9.Google ScholarPubMed
Habibian, H. K., Peters, S. O., Hsieh, C. C., et al.The fluctuating phenotype of the lympho-hematopoietic stem cell with cell cycle transit. J Exp Med, 1998; 188: 393–8.CrossRefGoogle Scholar
Becker, A. J., McCulloch, E. A., Siminovitch, L., & Till, J. E.The effect of differing demands for blood cell production on DNA synthesis by hemopoietic colony-forming cells of mice. Blood, 1965; 26: 296–308.Google Scholar
Toksoz, D., Dexter, T. M., Lord, B. I., Wright, E. G., & Lajtha, L. G.The regulation of hemopoiesis in long-term bone marrow cultures. II. Stimulation and inhibition of stem cell proliferation. Blood, 1980; 55: 931–6.Google ScholarPubMed
Wang, J. C. Y., Dorrell, C., Ito, C. Y., et al. Normal and leukemic human stem cells assayed in immune-deficient mice. In , L. I. Zon, ed., Hematopoiesis: A Developmental Approach (New York: Oxford University Press, 2001), pp. 99–118.Google Scholar
Kollet, O., Peled, A., Byk, T., et al.β2 microglobulin-deficient (β2mnull) NOD/SCID mice are excellent recipients for studying human stem cell function. Blood, 2000; 95: 3102–5.Google Scholar
Glimm, H., Eisterer, W., Lee, K., et al.Previously undetected human hematopoietic cell populations with short-term repopulating activity selectively engraft NOD/SCID-b2 microglobulin-null mice. J Clin Invest, 2001; 107: 199–206.CrossRefGoogle ScholarPubMed
Hiramatsu, H., Nishikomori, R., Heike, T., et al.Complete reconstitution of human lymphocytes from cord blood CD34+ cells using the NOD/SCID/gammacnull mice model. Blood, 2003; 102: 873–80.CrossRefGoogle ScholarPubMed
Goldman, J. P., Blundell, M. P., Lopes, L., et al.Enhanced human cell engraftment in mice deficient in RAG2 and the common cytokine receptor gamma chain. Br J Haematol, 1998; 103: 335–42.CrossRefGoogle ScholarPubMed
Traggiai, E., Chicha, L., Mazzucchelli, L., et al.Development of a human adaptive immune system in cord blood cell-transplanted mice. Science, 2004; 304: 104–7.CrossRefGoogle ScholarPubMed
Zanjani, E. D., Almeida-Porada, G., & Flake, A. W.The human/sheep xenograft model: a large animal model of human hematopoiesis. Int J Hematol, 1996; 63: 179–92.CrossRefGoogle ScholarPubMed
Bernstein, J., Boyle, D. W., Srour, E. F., et al.Variation in long-term engraftment of a large consecutive series of lambs transplanted in utero with human hematopoietic cells. Biol Blood Marrow Transplant, 1997; 3: 247–54.Google ScholarPubMed
Christianson, S. W., Greiner, D. L., Hesselton, R., et al.Enhanced human CD4+ T cell engraftment in b2-microglobulin-deficient NOD-scid mice. J Immunol, 1997; 158: 3578–86.Google ScholarPubMed
Cashman, J. D. & Eaves, C. J.High marrow seeding efficiency of human lymphomyeloid repopulating cells in irradiated NOD/SCID mice. Blood, 2000; 96: 3979–81.Google ScholarPubMed
Ballen, K. K., Valinski, K., Greiner, D., et al.Variables to predict engraftment of umbilical cord blood into immunodeficient mice: usefulness of the non-obese diabetic-severe combined immunodeficient assay. Br J Haematol, 2001; 114: 211–18.CrossRefGoogle ScholarPubMed
Meyerrose, T., Herrbrich, P. E., Hess, D. A., & Nolta, J. A.Immune-deficient mouse models for analysis of human stem cells. Biotechniques, 2003; 35: 1262–71.Google ScholarPubMed
Srour, E. F., Zanjani, E. D., Cornetta, K., et al.Persistence of human multilineage, self-renewing lymphohematopoietic stem cells in chimeric sheep. Blood, 1993; 82: 3333–42.Google ScholarPubMed
Civin, C. I., Almeida-Porada, G., Lee, M.-J., et al.Sustained, retransplantable, multilineage engraftment of highly purified adult human bone marrow stem cells in vivo. Blood, 1996; 88: 4102–9.Google ScholarPubMed
Zanjani, E. D., Almeida-Porada, G., Livingston, A. G., Flake, A. W., & Ogawa, M.Human bone marrow CD34− cells engraft in vivo and undergo multilineage expression that includes giving rise to CD34+ cells. Exp Hematol, 1998; 26: 353–60.Google ScholarPubMed
Cashman, J. D. & Eaves, C. J.Human growth factor-enhanced regeneration of transplantable human hematopoietic stem cells in nonobese diabetic/severe combined immunodeficient mice. Blood, 1999; 93: 481–7.Google ScholarPubMed
Hogan, C. J., Shpall, E. J., McNulty, O., et al.Engraftment and development of human CD34+-enriched cells from umbilical cord blood in NOD/LtSz-scid/scid mice. Blood, 1997; 90: 85–96.Google ScholarPubMed
Hogan, C. J., Shpall, E. J., & Keller, G.Differential long-term and multilineage engraftment potential from subfractions of human CD34+ cord blood cells transplanted into NOD/SCID mice. Proc Natl Acad Sci U S A, 2002; 99: 413–18.CrossRefGoogle ScholarPubMed
Pflumio, F., Izac, B., Katz, A., et al.Phenotype and function of human hematopoietic cells engrafting immune-deficient CB17-severe combined immunodeficiency mice and nonobese diabetic-severe combined immunodeficiency mice after transplantation of human cord blood mononuclear cells. Blood, 1996; 88: 3731–40.Google Scholar
Cashman, J., Bockhold, K., Hogge, D. E., Eaves, A. C., & Eaves, C. J.Sustained proliferation, multi-lineage differentiation and maintenance of primitive human haematopoietic cells in NOD/SCID mice transplanted with human cord blood. Br J Haematol, 1997; 97: 1026–36.CrossRefGoogle Scholar
Lapidot, T., Pflumio, F., Doedens, M., et al.Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in SCID mice. Science, 1992; 255: 1137–41.CrossRefGoogle ScholarPubMed
Cashman, J. D., Lapidot, T., Wang, J. C. Y., et al.Kinetic evidence of the regeneration of multilineage hematopoiesis from primitive cells in normal human bone marrow transplanted into immunodeficient mice. Blood, 1997; 89: 4307–16.Google ScholarPubMed
Peled, A., Petit, I., Kollet, O., et al.Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science, 1999; 283: 845–8.CrossRefGoogle ScholarPubMed
Holyoake, T. L., Nicolini, F. E., & Eaves, C. J.Functional differences between transplantable human hematopoietic stem cells from fetal liver, cord blood, and adult marrow. Exp Hematol, 1999; 27: 1418–27.CrossRefGoogle ScholarPubMed
Rossi, M. I. D., Medina, K. L., Garrett, K., et al.Relatively normal human lymphopoiesis but rapid turnover of newly formed B cells in transplanted nonobese diabetic/SCID mice. J Immunol, 2001; 167: 3033–42.CrossRefGoogle ScholarPubMed
Nicolini, F. E., Cashman, J. D., Hogge, D. E., Humphries, R. K., & Eaves, C. J.NOD/SCID mice engineered to express human IL-3, GM-CSF, and Steel factor constitutively mobilize engrafted human progenitors and compromise human stem cell regeneration. Leukemia, 2004; 18: 341–7.CrossRefGoogle ScholarPubMed
Kerre, T. C., De Smet, G., De Smedt, M., et al.Both CD34+38+ and CD34+38− cells home specifically to the bone marrow of NOD/LtSZ scid/scid mice but show different kinetics in expansion. J Immunol, 2001; 167: 3692–8.CrossRefGoogle ScholarPubMed
Mazurier, F., Doedens, M., Gan, O. I., & Dick, J. E.Rapid myeloerythroid repopulation after intrafemoral transplantation of NOD-SCID mice reveals a new class of human stem cells. Nat Med, 2003; 9: 959–63.CrossRefGoogle ScholarPubMed
Glimm, H., Oh, I., & Eaves, C.Human hematopoietic stem cells stimulated to proliferate in vitro lose engraftment potential during their S/G2/M transit and do not reenter Go. Blood, 2000; 96: 4185–93.Google Scholar
Wang, J. C. Y., Doedens, M., & Dick, J. E.Primitive human hematopoietic cells are enriched in cord blood compared with adult bone marrow or mobilized peripheral blood as measured by the quantitative in vivo SCID-repopulating cell assay. Blood, 1997; 89: 3919–24.Google ScholarPubMed
Ailles, L. E., Gerhard, B., Kawagoe, H., & Hogge, D. E.Growth characteristics of acute myelogenous leukemia progenitors that initiate malignant hematopoiesis in nonobese diabetic/severe combined immunodeficient mice. Blood, 1999; 94: 1761–72.Google ScholarPubMed
Rombouts, W. J. C., Martens, A. C. M., & Ploemacher, R. E.Identification of variables determining the engraftment potential of human acute myeloid leukemia in the immunodeficient NOD/SCID human chimera model. Leukemia, 2000; 14: 889–97.CrossRefGoogle ScholarPubMed
Feuring-Buske, M., Gerhard, B., Cashman, J., et al.Improved engraftment of human acute myeloid leukemia progenitor cells in beta 2-microglobulin-deficient NOD/SCID mice and in NOD/SCID mice transgenic for human growth factors. Leukemia, 2003; 17: 760–3.CrossRefGoogle ScholarPubMed
Kamel-Reid, S., Letarte, M., Sirard, C., et al.A model of human acute lymphoblastic leukemia in immune-deficient SCID mice. Science, 1989; 246: 1597–600.CrossRefGoogle ScholarPubMed
Nijmeijer, B. A., Mollevanger, P., van Zelderen-Bhola, S. L., et al.Monitoring of engraftment and progression of acute lymphoblastic leukemia in individual NOD/SCID mice. Exp Hematol, 2001; 29: 322–9.CrossRefGoogle ScholarPubMed
Eisterer, W., Jiang, X., Bachelot, T., et al.Unfulfilled promise of endostatin in a gene therapy-xenotransplant model of human acute lymphocytic leukemia. Mol Ther, 2002; 5: 352–9.CrossRefGoogle Scholar
Sawyers, C. L., Gishizky, M. L., Quan, S., Golde, D. W., & Witte, O. N.Propagation of human blastic myeloid leukemias in the SCID mouse. Blood, 1992; 79: 2089–98.Google ScholarPubMed
Sirard, C., Lapidot, T., Vormoor, J., et al.Normal and leukemic SCID-repopulating cells (SRC) co-exist in the bone marrow and peripheral blood from CML patients in chronic phase while leukemic SRC are detected in blast crisis. Blood, 1996; 87: 1539–48.Google Scholar
Pilarski, L. M., Hipperson, G., Seeberger, K., et al.Myeloma progenitors in the blood of patients with aggressive or minimal disease: engraftment and self-renewal of primary human myeloma in the bone marrow of NOD SCID mice. Blood, 2000; 95: 1056–65.Google ScholarPubMed
Matsui, W., Huff, C. A., Wang, Q., et al.Characterization of clonogenic multiple myeloma cells. Blood, 2004; 103: 2332–6.CrossRefGoogle ScholarPubMed
Mitsiades, C. S., Mitsiades, N. S., Bronson, R. T., et al.Fluorescence imaging of multiple myeloma cells in a clinically relevant SCID/NOD in vivo model: biologic and clinical implications. Cancer Res, 2003; 63: 6689–96.Google Scholar
Shimoni, A., Marcus, H., Dekel, B., et al.Autologous T cells control B-chronic lymphocytic leukemia tumor progression in human-mouse radiation chimera. Cancer Res, 1999; 59: 5968–74.Google ScholarPubMed
Dialynas, D. P., Lee, M-J., Gold, D. P., et al.Preconditioning with fetal cord blood facilitates engraftment of primary childhood T-cell acute lymphoblastic leukemia in immunodeficient mice. Neoplasia, 2001; 97: 3218–25.Google ScholarPubMed
Terpstra, W., Ploemacher, R. E., Prins, A., et al.Fluorouracil selectively spares acute myeloid leukemia cells with long-term growth abilities in immunodeficient mice and in culture. Blood, 1996; 88: 1944–50.Google ScholarPubMed
Guan, Y., Gerhard, B., & Hogge, D. E.Detection, isolation, and stimulation of quiescent primitive leukemic progenitor cells from patients with acute myeloid leukemia (AML). Blood, 2003; 101: 3142–9.CrossRefGoogle Scholar
Blair, A., Hogge, D. E., Ailles, L. E., Lansdorp, P. M., & Sutherland, H. J.Lack of expression of Thy-1 (CD90) on acute myeloid leukaemia cells with long-term proliferative ability in vitro and in vivo. Blood, 1997; 89: 3104–12.Google ScholarPubMed
Lapidot, T., Grunberger, T., Vormoor, J., et al.Identification of human juvenile chronic myelogenous leukemia stem cells capable of initiating the disease in primary and secondary SCID mice. Blood, 1996; 88: 2655–64.Google ScholarPubMed
Thanopoulou, E., Cashman, J., Kakagianne, T., et al.Engraftment of NOD/SCID-b2 microglobulin null mice with multilineage neoplastic cells from patients with myelodysplastic syndrome. Blood, 2004; 103: 4285–93.CrossRefGoogle ScholarPubMed
Lewis, I. D., McDiarmid, L. A., Samels, L. M., Bik To, L., & Hughes, T. P.Establishment of a reproducible model of chronic-phase chronic myeloid leukemia in NOD/SCID mice using blood-derived mononuclear or CD34+ cells. Blood, 1998; 91: 630–40.Google ScholarPubMed
Wang, J. C. Y., Lapidot, T., Cashman, J. D., et al.High level engraftment of NOD/SCID mice by primitive normal and leukemic hematopoietic cells from patients with chronic myeloid leukemia in chronic phase. Blood, 1998; 91: 2406–14.Google ScholarPubMed
Sutherland, H. J., Eaves, C. J., Eaves, A. C., Dragowska, W., & Lansdorp, P. M.Characterization and partial purification of human marrow cells capable of initiating long-term hematopoiesis in vitro. Blood, 1989; 74: 1563–70.Google ScholarPubMed
Ploemacher, R. E., Sluijs, J. P., Beurden, C. A. J., Baert, M. R. M., & Chan, P. L.Use of limiting-dilution type long-term marrow cultures in frequency analysis of marrow-repopulating and spleen colony-forming hematopoietic stem cells in the mouse. Blood, 1991; 78: 2527–33.Google ScholarPubMed
Dexter, T. M., Allen, T. D., & Lajtha, L. G.Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol, 1977; 91: 335–44.CrossRefGoogle ScholarPubMed
Greenberger, J. S.Sensitivity of corticosteroid-dependent insulin-resistant lipogenesis in marrow preadipocytes of obese-diabetic (db/db) mice. Nature, 1978; 275: 752–4.CrossRefGoogle ScholarPubMed
Gartner, S. & Kaplan, H. S.Long-term culture of human bone marrow cells. Proc Natl Acad Sci U S A, 1980; 77: 4756–9.CrossRefGoogle ScholarPubMed
Greenberg, H. M., Newburger, P. E., Parker, L. M., Novak, T., & Greenberger, J. S.Human granulocytes generated in continuous bone marrow culture are physiologically normal. Blood, 1981; 58: 724–32.Google ScholarPubMed
Gronthos, S. & Simmons, P. J.The growth factor requirements of STRO-1-positive human bone marrow stromal precursors under serum-deprived conditions in vitro. Blood, 1995; 85: 929–40.Google ScholarPubMed
Roecklein, B. A. & Torok-Storb, B.Functionally distinct human marrow stromal cell lines immortalized by transduction with the human papilloma virus E6/E7 genes. Blood, 1995; 85: 997–1005.Google ScholarPubMed
Li, J., Sensebe, L., Herve, P., & Charbord, P.Nontransformed colony-derived stromal cell lines from normal human marrows. III. The maintenance of hematopoiesis from CD34+ cell populations. Exp Hematol, 1997; 25: 582–91.Google ScholarPubMed
Sutherland, H. J., Eaves, C. J., Lansdorp, P. M., Thacker, J. D., & Hogge, D. E.Differential regulation of primitive human hematopoietic cells in long-term cultures maintained on genetically engineered murine stromal cells. Blood, 1991; 78: 666–72.Google ScholarPubMed
Issaad, C., Croisille, L., Katz, A., Vainchenker, W., & Coulombel, L.A murine stromal cell line allows the proliferation of very primitive human CD34++/CD38− progenitor cells in long-term cultures and semisolid assays. Blood, 1993; 81: 2916–24.Google ScholarPubMed
Baum, C. M., Weissman, I. L., Tsukamoto, A. S., Buckle, A. M., & Péault, B.Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci U S A, 1992; 89: 2804–8.CrossRefGoogle ScholarPubMed
Thiemann, F. T., Moore, K. A., Smogorzewska, E. M., Lemischka, I. R., & Crooks, G. M.The murine stromal cell line AFT024 acts specifically on human CD34+CD38− progenitors to maintain primitive function and immunophenotype in vitro. Exp Hematol, 1998; 26: 612–19.Google ScholarPubMed
Wineman, J., Moore, K., Lemischka, I., & Muller-Sieburg, C.Functional heterogeneity of the hematopoietic microenvironment: rare stromal elements maintain long-term repopulating stem cells. Blood, 1996; 87: 4082–90.Google ScholarPubMed
Friedrich, C., Zausch, E., Sugrue, S. P., & Gutierrez-Ramos, J.-C.Hematopoietic supportive functions of mouse bone marrow and fetal liver microenvironment: dissection of granulocyte, B-lymphocyte, and hematopoietic progenitor support at the stroma cell clone level. Blood, 1996; 87: 4596–606.Google ScholarPubMed
Charbord, P., Oostendorp, R., Pang, W., et al.Comparative study of stromal cell lines derived from embryonic fetal, and postnatal mouse blood-forming tissues. Exp Hematol, 2004; 30: 1202–10.CrossRefGoogle Scholar
Moore, K. A., Pytowski, B., Witte, L., Hicklin, D., & Lemischka, I. R.Hematopoietic activity of a stromal cell transmembrane protein containing epidermal growth factor-like repeat motifs. Proc Natl Acad Sci U S A, 1997; 94: 4011–16.CrossRefGoogle ScholarPubMed
Varnum-Finney, B., Purton, L. E., Yu, M., et al.The Notch ligand, Jagged-1, influences the development of primitive hematopoietic precursor cells. Blood, 1998; 91: 4084–91.Google ScholarPubMed
Karanu, F. N., Murdoch, B., Gallacher, L., et al.The Notch ligand Jagged-1 represents a novel growth factor of human hematopoietic stem cells. J Exp Med, 2000; 192: 1365–72.CrossRefGoogle ScholarPubMed
Ohishi, K., Varnum-Finney, B., & Bernstein, I. D.Delta-1 enhances marrow and thymus repopulating ability of human CD34+CD38− cord blood cells. J Clin Invest, 2002; 110: 1165–74.CrossRefGoogle ScholarPubMed
Gupta, P., McCarthy, J. B., & Verfaillie, C. M.Stromal fibroblast heparan sulfate is required for cytokine-mediated ex vivo maintenance of human long-term culture-initiating cells. Blood, 1996; 87: 3229–36.Google ScholarPubMed
Gupta, P., Oegema, T. R. J., Brazil, J. J., et al.Structurally specific heparan sulfates support primitive human hematopoiesis by formation of a multimolecular stem cell niche. Blood, 1998; 92: 4641–51.Google ScholarPubMed
Hogge, D. E., Lansdorp, P. M., Reid, D., Gerhard, B., & Eaves, C. J.Enhanced detection, maintenance and differentiation of primitive human hematopoietic cells in cultures containing murine fibroblasts engineered to produce human Steel factor, interleukin-3 and granulocyte colony-stimulating factor. Blood, 1996; 88: 3765–73.Google ScholarPubMed
Miller, C. L. & Eaves, C. J. Long-term culture-initiating cell assays for human and murine cells. In , C. A. Klug & , C. T. Jordan, eds., Methods in Molecular Medicine: Hematopoietic Stem Cell Protocols (Totowa, NJ: Humana Press, 2002), pp. 123–41.Google Scholar
Hao, Q. L., Thiemann, F. T., Petersen, D., Smogorzewska, E. M., & Crooks, G. M.Extended long-term culture reveals a highly quiescent and primitive human hematopoietic progenitor population. Blood, 1996; 88: 3306–13.Google ScholarPubMed
Freedman, A. R., Zhu, H., Levine, J. D., Kalams, S., & Scadden, D. T.Generation of human T lymphocytes from bone marrow CD34+ cells in vitro. Nat Med, 1996; 2: 46–51.CrossRefGoogle Scholar
Punzel, M., Wissink, S. D., Miller, J. S., et al.The myeloid-lymphoid initiating cell (ML-IC) assay assesses the fate of multipotent human progenitors in vitro. Blood, 1999; 93: 3750–6.Google ScholarPubMed
Berardi, A. C., Meffre, E., Pflumio, F., et al.Individual CD34+CD38lowCD19−CD10− progenitor cells from human cord blood generate B lymphocytes and granulocytes. Blood, 1997; 89: 3554–64.Google ScholarPubMed
Gan, O. I., Dorrell, C., Pereira, D. S., et al.Characterization and retroviral transduction of an early human lymphomyeloid precursor assayed in nonswitched long-term culture on murine stroma. Exp Hematol, 1999; 27: 1097–106.CrossRefGoogle ScholarPubMed
Harrison, D. E., Lerner, C. P., & Spooncer, E.Erythropoietic repopulating ability of stem cells from long-term marrow culture. Blood, 1987; 69: 1021–5.Google ScholarPubMed
Fraser, C. C., Szilvassy, S. J., Eaves, C. J., & Humphries, R. K.Proliferation of totipotent hematopoietic stem cells in vitro with retention of long-term competitive in vivo reconstituting ability. Proc Natl Acad Sci U S A, 1992; 89: 1968–72.CrossRefGoogle ScholarPubMed
Moore, K. A., Ema, H., & Lemischka, I. R.In vitro maintenance of highly purified, transplantable hematopoietic stem cells. Blood, 1997; 89: 4337–47.Google ScholarPubMed
Lemieux, M. E. & Eaves, C. J.Identification of properties that can distinguish primitive populations of stromal cell-responsive lympho-myeloid cells from cells that are stromal cell-responsive but lymphoid-restricted and cells that have lympho-myeloid potential but are also capable of competitively repopulating myeloablated recipients. Blood, 1996; 88: 1639–48.Google ScholarPubMed
Larochelle, A., Vormoor, J., Hanenberg, H., et al.Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implications for gene therapy. Nat Med, 1996; 2: 1329–37.CrossRefGoogle ScholarPubMed
Hennemann, B., Oh, I.-H., Chuo, J. Y., et al.Efficient retrovirus-mediated gene transfer to transplantable human bone marrow cells in the absence of fibronectin. Blood, 2000; 96: 2432–9.Google ScholarPubMed
Uchida, N., Fujisaki, T., Eaves, A. C., & Eaves, C. J.Transplantable hematopoietic stem cells in human fetal liver have a CD34+ side population (SP) phenotype. J Clin Invest, 2001; 108: 1071–7.CrossRefGoogle ScholarPubMed
Eaves, C. J. & Eaves, A. C. Progenitor cell dynamics. In , A. M. Carella, , G. Q. Daley, , C. J. Eaves, , J. M. Goldman, & , R. Hehlmann, eds., Chronic Myeloid Leukemia: Biology and Treatment (London: Martin Dunitz, 2001), pp. 73–100.Google Scholar
Coulombel, L., Eaves, C., Kalousek, D., Gupta, C., & Eaves, A.Long-term marrow culture of cells from patients with acute myelogenous leukemia. Selection in favor of normal phenotypes in some but not all cases. J Clin Invest, 1985; 75: 961–9.CrossRefGoogle Scholar
Sutherland, H. J., Blair, A., & Zapf, R. W.Characterization of a hierarchy in human acute myeloid leukemia progenitor cells. Blood, 1996; 87: 4754–61.Google ScholarPubMed
Petzer, A. L., Eaves, C. J., Lansdorp, P. M., et al.Characterization of primitive subpopulations of normal and leukemic cells present in the blood of patients with newly diagnosed as well as established chronic myeloid leukemia. Blood, 1996; 88: 2162–71.Google ScholarPubMed
Ailles, L. E., Gerhard, B., & Hogge, D. E.Detection and characterization of primitive malignant and normal progenitors in patients with acute myelogenous leukemia using long-term coculture with supportive feeder layers and cytokines. Blood, 1997; 90: 2555–64.Google ScholarPubMed
Young, D. C., Demetri, G. D., Ernst, T. J., Cannistra, S. A., & Griffin, J. D.In vitro expression of colony-stimulating factor genes by human acute myeloblastic leukemia cells. Exp Hematol, 1988; 16: 378–82.Google ScholarPubMed
Jiang, X., Lopez, A., Holyoake, T., Eaves, A., & Eaves, C.Autocrine production and action of IL-3 and granulocyte colony-stimulating factor in chronic myeloid leukemia. Proc Natl Acad Sci U S A, 1999; 96: 12804–9.CrossRefGoogle ScholarPubMed
Coulombel, L., Kalousek, D. K., Eaves, C. J., Gupta, C. M., & Eaves, A. C.Long-term marrow culture reveals chromosomally normal hematopoietic progenitor cells in patients with Philadelphia chromosome-positive chronic myelogenous leukemia. N Engl J Med, 1983; 308: 1493–8.CrossRefGoogle ScholarPubMed
Guan, Y., Ralph, S., Ling, V., & Hogge, D. E.Polyclonal normal hematopoietic progenitors in patients with acute myeloid leukemia (AML). Exp Hematol, 2002; 30: 721–8.CrossRefGoogle Scholar
Nara, N. & McCulloch, E. A.The proliferation in suspension of the progenitors of the blast cells in acute myeloblastic leukemia. Blood, 1985; 65: 1484–93.Google ScholarPubMed
Trevisan, M., Yan, X.-Q., & Iscove, N. N.Cycle initiation and colony formation in culture by murine marrow cells with long-term reconstituting potential in vivo. Blood, 1996; 88: 4149–58.Google ScholarPubMed
Petzer, A. L., Hogge, D. E., Lansdorp, P. M., Reid, D. S., & Eaves, C. J.Self-renewal of primitive human hematopoietic cells (long-term-culture-initiating cells) in vitro and their expansion in defined medium. Proc Natl Acad Sci U S A, 1996; 93: 1470–4.CrossRefGoogle ScholarPubMed
Maguer-Satta, V., Oostendorp, R., Reid, D., & Eaves, C. J.Evidence that ceramide mediates the ability of tumor necrosis factor to modulate primitive human hematopoietic cell fates. Blood, 2000; 96: 4118–23.Google ScholarPubMed
Bradley, T. R., & Metcalf, D.The growth of mouse bone marrow cells in vitro. Aust J Exp Biol Med Sci, 1966; 44: 287–300.CrossRefGoogle ScholarPubMed
Pluznik, D. H., & Sachs, L.The cloning of normal “mast” cells in tissue culture. J Cell Comp Physiol, 1965; 66: 319–24.CrossRefGoogle ScholarPubMed
Senn, J. S., McCulloch, E. A., & Till, J. E.Comparison of colony-forming ability of normal and leukaemic human marrow in cell culture. Lancet, 1967; 2: 597–8.CrossRefGoogle ScholarPubMed
Worton, R. G., McCulloch, E. A., & Till, J. E.Physical separation of hemopoietic stem cells from cells forming colonies in culture. J Cell Physiol, 1969; 74: 171–82.CrossRefGoogle ScholarPubMed
Metcalf, D.Control of granulocytes and macrophages: molecular, cellular, and clinical aspects. Science, 1991; 254: 529–33.CrossRefGoogle ScholarPubMed
Metcalf, D.The granulocyte-macrophage regulators: reappraisal by gene inactivation. Exp Hematol, 1995; 23: 569–72.Google ScholarPubMed
Campbell, H. D., Tucker, W. Q. J., Hort, Y., et al.Molecular cloning, nucleotide sequence, and expression of the gene encoding human eosinophil differentiation factor (interleukin 5). Proc Natl Acad Sci U S A, 1987; 84: 6629–33.CrossRefGoogle Scholar
Yamaguchi, Y., Suda, T., Suda, J., et al.Purified interleukin 5 supports the terminal differentiation and proliferation of murine eosinophilic precursors. J Exp Med, 1988; 167: 43–56.CrossRefGoogle ScholarPubMed
Lord, B. I., Gurney, H., Chang, J., et al.Haemopoietic cell kinetics in humans treated with rGM-CSF. Int J Cancer, 1992; 50: 26–31.CrossRefGoogle ScholarPubMed
Williams, G. T., Smith, C. A., Spooncer, E., Dexter, T. M., & Taylor, D. R.Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis. Nature, 1990; 343: 76–9.CrossRefGoogle ScholarPubMed
Bol, S. & Williams, N.The maturation state of three types of granulocyte/macrophage progenitor cells from mouse bone marrow. J Cell Physiol, 1980; 102: 233–43.CrossRefGoogle ScholarPubMed
Metcalf, D. & MacDonald, H. R.Heterogeneity of in vitro colony- and cluster-forming cells in the mouse marrow: segregation by velocity sedimentation. J Cell Physiol, 1975; 85: 643–54.CrossRefGoogle ScholarPubMed
Cashman, J., Eaves, A. C., & Eaves, C. J.Regulated proliferation of primitive hematopoietic progenitor cells in long-term human marrow cultures. Blood, 1985; 66: 1002–5.Google ScholarPubMed
Gregory, C. J.Erythropoietin sensitivity as a differentiation marker in the hemopoietic system: studies of three erythropoietic colony responses in culture. J Cell Physiol, 1976; 89: 289–301.CrossRefGoogle ScholarPubMed
Stephenson, J. R., Axelrad, A. A., McLeod, D. L., & Shreeve, M. M.Induction of colonies of hemoglobin-synthesising cells by erythropoietin in vitro. Proc Natl Acad Sci U S A, 1971; 68: 1542–6.CrossRefGoogle ScholarPubMed
Heath, D. S., Axelrad, A. A., McLeod, D. L., & Shreeve, M. M.Separation of the erythropoietin-responsive progenitors BFU-E and CFU-E in mouse bone marrow by unit gravity sedimentation. Blood, 1976; 47: 777–92.Google ScholarPubMed
Clark, B. J. & Housman, D.Characterization of an erythroid precursor cell of high proliferative capacity in normal human peripheral blood. Proc Natl Acad Sci U S A, 1977; 74: 1105–9.CrossRefGoogle Scholar
Eaves, C. J. & Eaves, A. C.Erythropoietin (Ep) dose–response curves for three classes of erythroid progenitors in normal human marrow and in patients with polycythemia vera. Blood, 1978; 52: 1196–210.Google ScholarPubMed
Gregory, C. J. & Eaves, A. C.Three stages of erythropoietic progenitor cell differentiation distinguished by a number of physical and biologic properties. Blood, 1978; 51: 527–37.Google ScholarPubMed
Eaves, C. J., Humphries, R. K., & Eaves, A. C. In vitro characterization of erythroid precursor cells and the erythropoietic differentiation process. In , G. Stamatoyannopoulos & , A. W. Nienhuis, eds., Cellular and Molecular Regulation of Hemoglobin Switching (New York: Grune and Stratton, 1979), pp. 251–73.Google Scholar
Koury, M. J. & Bondurant, M. C.Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor cells. Science, 1990; 248: 378–81.CrossRefGoogle ScholarPubMed
Stopka, T., Zivny, J. H., Stopkova, P., Prchal, J. F., & Prchal, J. T.Human hematopoietic progenitors express erythropoietin. Blood, 1998; 91: 3766–72.Google ScholarPubMed
Prchal, J. F. & Axelrad, A. A.Bone marrow responses in polycythemia vera. N Engl J Med, 1974; 290: 1382.Google ScholarPubMed
Eaves, A. C., Krystal, G., Cashman, J. D., & Eaves, C. J. Polycythemia vera: in vitro analysis of regulatory defects. In , E. D. Zanjani, , M. Tavassoli, & , J. L. Ascensao, eds., Regulation of erythropoiesis (New York: PMA Publishing, 1988), pp. 523–35.Google Scholar
Lemoine, F., Najman, A., Baillou, C., et al.A prospective study of the value of bone marrow erythroid progenitor cultures in polycythemia. Blood, 1986; 68: 996–1002.Google ScholarPubMed
Zwicky, C., Theiler, L., Zbären, K., Ischi, E., & Tobler, A.The predictive value of clonogenic stem cell assays for the diagnosis of polycythaemia vera. Br J Haematol, 2002; 117: 598–604.CrossRefGoogle Scholar
Zanjani, E. D., Weinberg, R. S., Nomdedeu, B., Kaplan, M. E., & Wasserman, L. R. In vitro assessment of similarities between erythroid precursors of fetal sheep and patients with polycythemia vera. In , M. J. Murphy, ed., In Vitro Aspects of Erythropoiesis (Berlin: Springer, 1978), pp. 118–122.Google Scholar
Eaves, A. C. & Eaves, C. J.Abnormalities in the erythroid progenitor compartments in patients with chronic myelogenous leukemia (CML). Exp Hematol, 1979; 7: 65–75.Google Scholar
Issaad, C. & Vainchenker, W.Growth of erythroid colonies in chronic myelogenous leukemia is independent of erythropoietin only in the presence of steel factor. Blood, 1994; 84: 3447–56.Google ScholarPubMed
Turhan, A. G., Cashman, J. D., Eaves, C. J., Humphries, R. K., & Eaves, A. C.Variable expression of features of normal and neoplastic stem cells in patients with thrombocytosis. Br J Haematol, 1992; 82: 50–7.CrossRefGoogle ScholarPubMed
Juvonen, E., Ikkala, E., Oksanen, K., & Ruutu, T.Megakaryocyte and erythroid colony formation in essential thrombocythaemia and reactive thrombocytosis: diagnostic value and correlation to complications. Br J Haematol, 1993; 83: 192–7.CrossRefGoogle ScholarPubMed
Florensa, L., Besses, C., Woessner, S., et al.Endogenous megakaryocyte and erythroid colony formation from blood in essential thrombocythaemia. Leukemia, 1994; 9: 271–3.Google Scholar
Griesshammer, M., Klippel, S., Strunck, E., et al.PRV-1 mRNA expression discriminates two types of essential thrombocythemia. Ann Hematol, 2004; 83: 364–70.CrossRefGoogle ScholarPubMed
Nakeff, A. & Daniels-McQueen, S.In vitro colony assay for a new class of megakaryocyte precursor: colony-forming unit megakaryocyte (CFU-M). Proc Soc Exp Biol Med, 1976; 151: 587–90.CrossRefGoogle Scholar
Ishibashi, T., Miller, S. L., & Burstein, S. A.Type beta transforming growth factor is a potent inhibitor of murine megakaryocytopoiesis in vitro. Blood, 1987; 69: 1737–41.Google ScholarPubMed
Berthier, R., Valiron, O., Scheweitzer, A., & Marguerie, G.Serum-free medium allows the optimal growth of human megakaryocyte progenitors compared with human plasma supplemented cultures: role of TGF-beta. Stem Cells, 1993; 11: 120–9.CrossRefGoogle ScholarPubMed
Hogge, D., Fanning, S., Bockhold, K., et al.Quantitation and characterization of human megakaryocyte colony-forming cells using a standardized serum-free agarose assay. Br J Haematol, 1997; 96: 790–800.CrossRefGoogle ScholarPubMed
Briddell, R. A. & Hoffman, R.Cytokine regulation of the human burst-forming unit-megakaryocyte. Blood, 1990; 76: 516–22.Google ScholarPubMed
Debili, N., Wendling, F., Katz, A., et al.The Mpl-ligand or thrombopoietin or megakaryocyte growth and differentiative factor has both direct proliferative and differentiative activities on human megakaryocyte progenitors. Blood, 1986; 86: 2516–25.Google Scholar
Hoffman, R.Regulation of megakaryocytopoiesis. Blood, 1989; 74: 1196–212.Google ScholarPubMed
Debili, N., Issaad, C., Masse, J.-M., et al.Expression of CD34 and platelet glycoproteins during human megakaryocytic differentiation. Blood, 1992; 80: 3022–35.Google ScholarPubMed
Johnson, G. R. & Metcalf, D.Pure and mixed erythroid colony formation in vitro stimulated by spleen conditioned medium with no detectable erythropoietin. Proc Natl Acad Sci U S A, 1977; 74: 3879–82.CrossRefGoogle ScholarPubMed
Fauser, A. A. & Messner, H. A.Granuloerythropoietic colonies in human bone marrow, peripheral blood, and cord blood. Blood, 1978; 52: 1243–8.Google ScholarPubMed
Humphries, R. K., Jacky, P. B., Dill, F. J., Eaves, A. C., & Eaves, C. J.CFU-S in individual erythroid colonies derived in vitro from adult mouse marrow. Nature, 1979; 279: 718–20.CrossRefGoogle ScholarPubMed
Holyoake, T. L., Freshney, M. G., Konwalinka, G., et al.Mixed colony formation in vitro by the heterogeneous compartment of multipotential progenitors in human bone marrow. Leukemia, 1993; 7: 207–13.Google ScholarPubMed
McNiece, I. K., Stewart, F. M., Deacon, D. M., et al.Detection of a human CFC with a high proliferative potential. Blood, 1989; 74: 609–12.Google ScholarPubMed
Pragnell, I. B., Wright, E. G., Lorimore, S. A., et al.The effect of stem cell proliferation regulators demonstrated with an in vitro assay. Blood, 1988; 72: 196–201.Google ScholarPubMed
Ogawa, M.Differentiation and proliferation of hematopoietic stem cells. Blood, 1993; 81: 2844–53.Google ScholarPubMed
Humphries, R. K., Eaves, A. C., & Eaves, C. J.Characterization of a primitive erythropoietic progenitor found in mouse marrow before and after several weeks in culture. Blood, 1979; 53: 746–63.Google ScholarPubMed
Nakahata, T. & Ogawa, M.Identification in culture of a class of hemopoietic colony-forming units with extensive capability to self-renew and generate multipotential hemopoietic colonies. Proc Natl Acad Sci U S A, 1982; 79: 3843–7.CrossRefGoogle ScholarPubMed
Lim, B., Jamal, N., & Messner, H. A.Flexible association of hemopoietic differentiation programs in multilineage colonies. J Cell Physiol, 1984; 121: 291–7.CrossRefGoogle ScholarPubMed
Suda, T., Suda, J., & Ogawa, M.Proliferative kinetics and differentiation of murine blast cell colonies in culture: evidence for variable Go periods and constant doubling rates of early pluripotent hemopoietic progenitors. J Cell Physiol, 1983; 117: 308–18.CrossRefGoogle Scholar
Leary, A. G., Zeng, H. Q., Clark, S. C., & Ogawa, M.Growth factor requirements for survival in Go and entry into the cell cycle of primitive human hemopoietic progenitors. Proc Natl Acad Sci U S A, 1992; 89: 4013–17.CrossRefGoogle Scholar
Leary, A. G. & Ogawa, M.Blast cell colony assay for umbilical cord blood and adult bone marrow progenitors. Blood, 1987; 69: 953–6.Google ScholarPubMed
Hirayama, F., Shih, J. P., Awgulewitsch, A., et al.Clonal proliferation of murine lymphohemopoietic progenitors in culture. Proc Natl Acad Sci U S A, 1992; 89: 5907–11.CrossRefGoogle ScholarPubMed
Hirayama, F., Aiba, Y., Ikebuchi, K., Sekiguchi, S., & Ogawa, M.Differentiation in culture of murine primitive lymphohematopoietic progenitors toward T-cell lineage. Blood, 1999; 93: 4187–95.Google ScholarPubMed
Yonemura, Y., Ku, H., Hirayama, F., Souza, L. M., & Ogawa, M.Interleukin 3 or interleukin 1 abrogates the reconstituting ability of hematopoietic stem cells. Proc Natl Acad Sci U S A, 1996; 93: 4040–4.CrossRefGoogle ScholarPubMed
Buick, R. N., Till, J. E., & McCulloch, E. A.Colony assay for proliferative blast cells circulating in myeloblastic leukemia. Lancet, 1977; 1: 862–3.CrossRefGoogle Scholar
Moore, M. A. S., Williams, N., & Metcalf, D.In vitro colony formation by normal and leukemic human hematopoietic cells: characterization of the colony-forming cells. J Natl Cancer Inst, 1973; 50: 603–23.CrossRefGoogle ScholarPubMed
Izaguirre, C. A., Minden, M. D., Howatson, A. F., & McCulloch, E. A.Colony formation by normal and malignant human B-lymphocytes. Br J Cancer, 1980; 42: 430–7.CrossRefGoogle ScholarPubMed
Izaguirre, C. A., Curtis, J., Messner, H., & McCulloch, E. A.A colony assay for blast cell progenitors in non-B non-T (common) acute lymphoblastic leukemia. Blood, 1981; 57: 823–9.Google ScholarPubMed
Oster, W., Mertelsmann, R., & Herrmann, F.Role of colony-stimulating factors in the biology of acute myelogenous leukemia. Int J Cell Cloning, 1989; 7: 13–29.CrossRefGoogle ScholarPubMed
Lowenberg, B. & Touw, I. P.Hematopoietic growth factors and their receptors in acute leukemia. Blood, 1993; 81: 281–92.Google ScholarPubMed
Drexler, H. G.Expression of FLT3 receptor and response to FLT3 ligand by leukemic cells. Leukemia, 1996; 10: 588–99.Google ScholarPubMed
Drexler, H. G. & Quentmeier, H.Thrombopoietin: expression of its receptor MPL and proliferative effects on leukemic cells. Leukemia, 1996; 10: 1405–21.Google ScholarPubMed
Fialkow, P. J., Janssen, J. W. G., & Bartram, C. R.Clonal remissions in acute nonlymphocytic leukemia: evidence for a multistep pathogenesis of the malignancy. Blood, 1991; 77: 1415–17.Google ScholarPubMed
Tachibana, N., Raimondi, S. C., Lauer, S. J., Sartain, P., & Dow, L. W.Evidence for a multipotential stem cell disease in some childhood Philadelphia chromosome-positive acute lymphoblastic leukemia. Blood, 1987; 70: 1458–61.Google ScholarPubMed
Secker-Walker, L. M. & Craig, J. M.Prognostic implications of breakpoint and lineage heterogeneity in Philadelphia-positive acute lymphoblastic leukemia: a review. Leukemia, 1993; 7: 147–51.Google ScholarPubMed
Spangrude, G. J., Heimfeld, S., & Weissman, I. L.Purification and characterization of mouse hematopoietic stem cells. Science, 1988; 241: 58–62.CrossRefGoogle ScholarPubMed
Bertoncello, I., Hodgson, G. S., & Bradley, T. R.Multiparameter analysis of transplantable hemopoietic stem cells: I. The separation and enrichment of stem cells homing to marrow and spleen on the basis of Rhodamine-123 fluorescence. Exp Hematol, 1985; 13: 999–1006.Google ScholarPubMed
Chaudhary, P. M. & Roninson, I. B.Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells. Cell, 1991; 66: 85–94.CrossRefGoogle ScholarPubMed
Zhou, S., Scheutz, J. D., Bunting, K. D., et al.The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med, 2001; 7: 1028–34.CrossRefGoogle Scholar
Jones, R. J., Barber, J. P., Vala, M. S., et al.Assessment of aldehyde dehydrogenase in viable cells. Blood, 1995; 85: 2742–6.Google ScholarPubMed
Storms, R. W., Trujillo, A. P., Springer, J. B., et al.Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci U S A, 1999; 96: 9118–23.CrossRefGoogle ScholarPubMed
Lansdorp, P. M., Dragowska, W., & Mayani, H.Ontogeny-related changes in proliferative potential of human hematopoietic cells. J Exp Med, 1993; 178: 787–91.CrossRefGoogle ScholarPubMed
Lyons, A. B. & Parish, C. R.Determination of lymphocyte division by flow cytometry. J Immunol Methods, 1994; 171: 131–7.CrossRefGoogle ScholarPubMed
Nordon, R. E., Ginsberg, S. S., & Eaves, C. J.High resolution cell division tracking demonstrates the Flt3-ligand-dependence of human marrow CD34+CD38− cell production in vitro. Br J Haematol, 1997; 98: 528–39.CrossRefGoogle ScholarPubMed
Akashi, K., Traver, D., Miyamoto, T., & Weissman, I. L.A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature, 2000; 404: 193–7.CrossRefGoogle ScholarPubMed
Nakorn, T. N., Traver, D., Weissman, I. L., & Akashi, K.Myeloerythroid-restricted progenitors are sufficient to confer radioprotection and provide the majority of day 8 CFU-S. J Clin Invest, 2002; 109: 1579–85.CrossRefGoogle Scholar
Manz, M. G., Miyamoto, T., Akashi, K., & Weissman, I. L.Prospective isolation of human clonogenic common myeloid progenitors. Proc Natl Acad Sci U S A, 2002; 99: 11872–7.CrossRefGoogle ScholarPubMed
Sauvageau, G., Lansdorp, P. M., Eaves, C. J., et al.Differential expression of homeobox genes in functionally distinct CD34+ subpopulations of human bone marrow cells. Proc Natl Acad Sci U S A, 1994; 91: 12223–7.CrossRefGoogle ScholarPubMed
Goodell, M. A., Brose, K., Paradis, G., Conner, A. S., & Mulligan, R. C.Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med, 1996; 183: 1797–806.CrossRefGoogle ScholarPubMed
Krause, D. S., Fackler, M. J., Civin, C. I., & May, W. S.CD34: structure, biology, and clinical utility. Blood, 1996; 87: 1–13.Google ScholarPubMed
Krause, D. S., Ito, T., Fackler, M. J., et al.Characterization of murine CD34, a marker for hematopoietic progenitor and stem cells. Blood, 1994; 84: 691–701.Google ScholarPubMed
Morel, F., Szilvassy, J., Travis, M., Chen, B., & Galy, A.Primitive hematopoietic cells in murine bone marrow express the CD34 antigen. Blood, 1996; 88: 3774–84.Google ScholarPubMed
Bhatia, M., Wang, J. C. Y., Kapp, U., Bonnet, D., & Dick, J. E.Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci U S A, 1997; 94: 5320–5.CrossRefGoogle ScholarPubMed
Kawano, Y., Takaue, Y., Watanabe, A., et al.Partially mismatched pediatric transplants with allogeneic CD34(+) blood cells from a related donor. Blood, 1998; 92: 3123–30.Google ScholarPubMed
Michallet, M., Philip, T., Philip, I., et al.Transplantation with selected autologous peripheral blood CD34+Thy1+ hematopoietic stem cells (HSCs) in multiple myeloma: impact of HSC dose on engraftment, safety, and immune reconstitution. Exp Hematol, 2000; 28: 858–70.CrossRefGoogle ScholarPubMed
Negrin, R. S., Atkinson, K., Leemhuis, T., et al.Transplantation of highly purified CD34+Thy-1+ hematopoietic stem cells in patients with metastatic breast cancer. Biol Blood Marrow Transplant, 2000; 6: 262–71.CrossRefGoogle ScholarPubMed
Fujisaki, T., Berger, M. G., Rose-John, S., & Eaves, C. J.Rapid differentiation of a rare subset of adult human lin−CD34−CD38− cells stimulated by multiple growth factors in vitro. Blood, 1999; 94: 1926–32.Google ScholarPubMed
Storms, R. W., Goodell, M. A., Fisher, A., Mulligan, R. C., & Smith, C.Hoechst dye efflux reveals a novel CD7+ CD34− lymphoid progenitor in human umbilical cord blood. Blood, 2000; 96: 2125–33.Google ScholarPubMed
Zanjani, E. D., Almeida-Porada, G., Livingston, A. G., Zeng, H., & Ogawa, M.Reversible expression of CD34 by adult human bone marrow long-term engrafting hematopoietic stem cells. Exp Hematol, 2003; 31: 406–12.CrossRefGoogle ScholarPubMed
Okuno, Y., Iwasaki, H., Huettner, C. S., et al.Differential regulation of the human and murine CD34 genes in hematopoietic stem cells. Proc Natl Acad Sci U S A, 2002; 99: 6246–51.CrossRefGoogle ScholarPubMed
Radomska, H. S., Gonzalez, D. A., Okuno, Y., et al.Transgenic targeting with regulatory elements of the human CD34 gene. Blood, 2002; 100: 4410–19.CrossRefGoogle ScholarPubMed
Deaglio, S., Mehta, K., & Malavasi, F.Human CD38: a (r)evolutionary story of enzymes and receptors. Leuk Res, 2001; 25: 1–12.CrossRefGoogle ScholarPubMed
Tajima, F., Deguchi, T., Laver, J. H., Zeng, H., & Ogawa, M.Reciprocal expression of CD38 and CD34 by adult murine hematopoietic stem cells. Blood, 2001; 97: 2618–24.CrossRefGoogle ScholarPubMed
Higuchi, Y., Zeng, H., & Ogawa, M.CD38 expression by hematopoietic stem cells of newborn and juvenile mice. Leukemia, 2003; 17: 171–4.CrossRefGoogle ScholarPubMed
Terstappen, L. W. M. M., Huang, S., Safford, M., Lansdorp, P. M., & Loken, M. R.Sequential generations of hematopoietic colonies derived from single nonlineage-committed CD34+CD38− progenitor cells. Blood, 1991; 77: 1218–27.Google ScholarPubMed
Hao, Q.-L. H., Shah, A. J., Thiemann, F. T., Smogorzewska, E. M., & Crooks, G. M.A functional comparison of CD34+CD38− cells in cord blood and bone marrow. Blood, 1995; 86: 3745–53.Google ScholarPubMed
Nicolini, F. E., Imren, S., Oh, I.-H., et al.Expression of a human beta-globin transgene in erythroid cells derived from retrovirally transduced transplantable human fetal liver and cord blood cells. Blood, 2002; 100: 1257–64.CrossRefGoogle ScholarPubMed
Dorrell, C., Gan, O. I., Pereira, D. S., Hawley, R. G., & Dick, J. E.Expansion of human cord blood CD34+CD38− cells in ex vivo culture during retroviral transduction without a corresponding increase in SCID repopulating cell (SRC) frequency: dissociation of SRC phenotype and function. Blood, 2000; 95: 102–10.Google ScholarPubMed
Zhou, S., Morris, J. J., Barnes, Y., Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc Natl Acad Sci U S A, 2002; 99: 12339–44.CrossRefGoogle ScholarPubMed
Scharenberg, C. W., Harkey, M. A., & Torok-Storb, B.The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood, 2002; 99: 507–12.CrossRefGoogle ScholarPubMed
Goodell, M. A., Rosenzweig, M., Kim, H., et al.Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat Med, 1997; 3: 1337–45.CrossRefGoogle ScholarPubMed
Feuring-Buske, M. & Hogge, D. E.Hoechst 33342 efflux identifies a subpopulation of cytogenetically normal CD34+CD38− progenitor cells from patients with acute myeloid leukemia. Blood, 2001; 97: 3882–9.CrossRefGoogle ScholarPubMed
Gussoni, E., Soneoka, Y., Strickland, C. D., et al.Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature, 1999; 401: 390–4.CrossRefGoogle ScholarPubMed
Murayama, A., Matsuzaki, Y., Kawaguchi, A., Shimazaki, T., & Okano, H.Flow cytometric analysis of neural stem cells in the developing and adult mouse brain. J Neurosci Res, 2002; 69: 837–47.CrossRefGoogle ScholarPubMed
Bhattacharya, S., Jackson, J. D., Das, A. V., et al.Direct identification and enrichment of retinal stem cells/progenitors by Hoechst dye efflux assay. Invest Ophthalmol Vis Sci, 2003; 44: 2764–73.CrossRefGoogle ScholarPubMed
Hierlihy, A. M., Seale, P., Lobe, C. G., Rudnicki, M. A., & Megeney, L. A.The post-natal heart contains a myocardial stem cell population. FEBS Lett, 2002; 530: 239–43.CrossRefGoogle ScholarPubMed
Asakura, A. & Rudnicki, M. A.Side population cells from diverse adult tissues are capable of in vitro hematopoietic differentiation. Exp Hematol, 2002; 30: 1339–45.CrossRefGoogle ScholarPubMed
Issarachai, S., Priestley, G. V., Nakamoto, B., & Papayannopoulou, T.Cells with hemopoietic potential residing in muscle are itinerant bone marrow-derived cells. Exp Hematol, 2002; 30: 366–73.CrossRefGoogle ScholarPubMed
Morrison, S. J., Wright, D. E., & Weissman, I. L.Cyclophosphamide/granulocyte colony-stimulating factor induces hematopoietic stem cells to proliferate prior to mobilization. Proc Natl Acad Sci U S A, 1997; 94: 1908–13.CrossRefGoogle ScholarPubMed
Jordan, C. T., McKearn, J. P., & Lemischka, I. R.Cellular and developmental properties of fetal hematopoietic stem cells. Cell, 1990; 61: 953–63.CrossRefGoogle ScholarPubMed
Ortiz, M., Wine, J. W., Lohrey, N., et al.Functional characterization of a novel hematopoietic stem cell and its place in the c-kit maturation pathway in bone marrow cell development. Immunity, 1999; 10: 173–82.CrossRefGoogle ScholarPubMed
Christensen, J. L. & Weissman, I. L.Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc Natl Acad Sci U S A, 2001; 98: 14541–6.CrossRefGoogle ScholarPubMed
Adolfsson, J., Borge, O. J., Bryder, D., et al.Upregulation of flt3 expression within the bone marrow Lin−Sca1+c-kit+ stem cell compartment is accompanied by loss of self-renewal capacity. Immunity, 2001; 15: 659–69.CrossRefGoogle ScholarPubMed
Hasumura, M., Imada, C., & Nawa, K.Expression change of Flk-2/Flt-3 on murine hematopoietic stem cells in activating state. Exp Hematol, 2003; 31: 1331–7.CrossRefGoogle ScholarPubMed
Huang, S. & Terstappen, L. W. M. M.Lymphoid and myeloid differentiation of single human CD34+, HLA-DR+, CD38− hematopoietic stem cells. Blood, 1994; 83: 1515–26.Google ScholarPubMed
Miller, J. S., McCullar, V., & Verfaillie, C. M.Ex vivo culture of CD34+/Lin−/DR− cells in stroma-derived soluble factors, interleukin-3, and macrophage inflammatory protein 1-alpha maintains not only myeloid but also lymphoid progenitors in a novel switch culture assay. Blood, 1998; 91: 4516–22.Google ScholarPubMed
Traycoff, C. M., Abboud, M. R., Laver, J., et al.Evaluation of the in vitro behavior of phenotypically defined populations of umbilical cord blood hematopoietic progenitor cells. Exp Hematol, 1994; 22: 215–22.Google ScholarPubMed
Debili, N., Robin, C., Schiavon, V., et al.Different expression of CD41 on human lymphoid and myeloid progenitors from adults and neonates. Blood, 2001; 97: 2023–30.CrossRefGoogle ScholarPubMed
Lander, E. S., Linton, L. M., Birren, B., et al.Initial sequencing and analysis of the human genome. Nature, 2001; 409: 860–921.CrossRefGoogle ScholarPubMed
Venter, J. C., Adams, M. D., Myers, E. W., et al.The sequence of the human genome. Science, 2001; 291: 1304–51.CrossRefGoogle ScholarPubMed
Waterston, R. H., Lindblad-Toh, K., Birney, E., et al.Initial sequencing and comparative analysis of the mouse genome. Nature, 2002; 420: 520–62.Google ScholarPubMed
Brady, G., Billia, F., Knox, J., et al.Analysis of gene expression in a complex differentiation hierarchy by global amplification of cDNA from single cells. Curr Biol, 1995; 5: 909–22.CrossRefGoogle Scholar
Cheng, T., Shen, H., Giokas, D., et al.Temporal mapping of gene expression levels during the differentiation of individual primary hematopoietic cells. Proc Natl Acad Sci U S A, 1996; 93: 13158–63.CrossRefGoogle ScholarPubMed
Zinovyeva, M. V., Mark, J., Zijlmans, J. M., et al.Analysis of gene expression in subpopulations of murine hematopoietic stem and progenitor cells. Exp Hematol, 2000; 28: 318–34.CrossRefGoogle ScholarPubMed
Oh, I.-H., Lau, A., & Eaves, C. J.During ontogeny primitive (CD34+CD38−) hematopoietic cells show altered expression of a subset of genes associated with early cytokine and differentiation responses of their adult counterparts. Blood, 2000; 96: 4160–8.Google ScholarPubMed
Phillips, R. L., Ernst, R. E., Brunk, B., et al.The genetic program of hematopoietic stem cells. Science, 2000; 288: 1635–40.CrossRefGoogle ScholarPubMed
Billia, F., Barbara, M., McEwen, J., Trevisan, M., & Iscove, N. N.Resolution of pluripotential intermediates in murine hematopoietic differentiation by global complementary DNA amplification from single cells: confirmation of assignments by expression profiling of cytokine receptor transcripts. Blood, 2001; 97: 2257–68.CrossRefGoogle ScholarPubMed
Ivanova, N. B., Dimos, J. T., Schaniel, C., et al.A stem cell molecular signature. Science, 2002; 298: 601–4.CrossRefGoogle ScholarPubMed
Akashi, K., He, X., Chen, J., et al.Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood, 2003; 101: 383–90.CrossRefGoogle ScholarPubMed
Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R. C., & Melton, D. A.“Stemness”: transcriptional profiling of embryonic and adult stem cells. Science, 2002; 298: 597–600.CrossRefGoogle ScholarPubMed
Terskikh, A. V., Easterday, M. C., Li, L., et al.From hematopoiesis to neuropoiesis: evidence of overlapping genetic programs. Proc Natl Acad Sci U S A, 2001; 98: 7934–9.CrossRefGoogle ScholarPubMed
Hu, M., Krause, D., Greaves, M., et al.Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev, 1997; 11: 774–85.CrossRefGoogle ScholarPubMed
Delassus, S., Titley, I., & Enver, T.Functional and molecular analysis of hematopoietic progenitors derived from the aorta-gonad-mesonephros region of the mouse embryo. Blood, 1999; 94: 1495–503.Google ScholarPubMed
Bruno, L., Hoffmann, R., McBlane, F., et al.Molecular signatures of self-renewal, differentiation, and lineage choice in multipotential hemopoietic progenitor cells in vitro. Mol Cell Biol, 2004; 24: 741–56.CrossRefGoogle ScholarPubMed
Miyamoto, T., Iwasaki, H., Reizis, B., et al.Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment. Dev Cell, 2002; 3: 137–47.CrossRefGoogle ScholarPubMed
Ye, M., Iwasaki, H., Laiosa, C. V., et al.Hematopoietic stem cells expressing the myeloid lysozyme gene retain long-term, multilineage repopulation potential. Immunity, 2003; 19: 689–99.CrossRefGoogle ScholarPubMed
Eschbach, J. W., Abdulhadi, M. H., Browne, J. K., et al.Recombinant human erythropoietin in anemic patients with end-stage renal disease: results of a Phase III multicenter clinical trial. Ann Intern Med, 1989; 111: 992–1000.CrossRefGoogle ScholarPubMed
Packham, G.Mutation of BCL-2 family proteins in cancer. Apoptosis, 1998; 3: 75–82.CrossRefGoogle Scholar
Stirewalt, D. L. & Radich, J. P.The role of FLT3 in haematopoietic malignancies. Nat Rev Cancer, 2003; 3: 650–65.CrossRefGoogle ScholarPubMed
Lutterbach, B. & Hiebert, S. W.Role of the transcription factor AML-1 in acute leukemia and hematopoietic differentiation. Gene, 2000; 245: 223–35.CrossRefGoogle ScholarPubMed
Robb, L. & Begley, C. G.The SCL/TAL1 gene: roles in normal and malignant haematopoiesis. Bioessays, 1997; 19: 607–13.CrossRefGoogle ScholarPubMed
Goldman, J. M. & Melo, J. V.Chronic myeloid leukemia – advances in biology and new approaches to treatment. N Engl J Med, 2003; 349: 1451–64.CrossRefGoogle Scholar
Williams, G. T. & Smith, C. A.Molecular regulation of apoptosis: genetic controls on cell death. Cell, 1993; 74: 777–9.CrossRefGoogle ScholarPubMed
Wickremasinghe, R. G. & Hoffbrand, A. V.Biochemical and genetic control of apoptosis: relevance to normal hematopoiesis and hematological malignancies. Blood, 1999; 93: 3587–600.Google ScholarPubMed
Barisic, K., Petrik, J., & Rumora, L.Biochemistry of apoptotic cell death. Acta Pharm, 2003; 53: 151–64.Google ScholarPubMed
Peters, R., Leyvraz, S., & Perey, L.Apoptotic regulation in primitive hematopoietic precursors. Blood, 1998; 92: 2041–52.Google ScholarPubMed
Veis, D. J., Sorenson, C. M., Shutter, J. R., & Korsmeyer, S. J.Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell, 1993; 75: 229–40.CrossRefGoogle ScholarPubMed
Nakayama, K. I., Nakayama, K., Negishi, I., et al.Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice. Science, 1993; 261: 1584–8.CrossRefGoogle ScholarPubMed
Bouillet, P., Metcalf, D., Huang, D. C., et al.Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science, 1999; 286: 1735–8.CrossRefGoogle ScholarPubMed
Motoyama, N., Kimura, T., Takahashi, T., Watanabe, T., & Nakano, T.Bcl-× prevents apoptotic cell death of both primitive and definitive erythrocytes at the end of maturation. J Exp Med, 1999; 189: 1691–8.CrossRefGoogle ScholarPubMed
Hamasaki, A., Sendo, F., Nakayama, K., et al.Accelerated neutrophil apoptosis in mice lacking A1-a, a subtype of the bcl-2-related A1 gene. J Exp Med, 1998; 188: 1985–92.CrossRefGoogle ScholarPubMed
Sherr, C. J. & Roberts, J. M.CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev, 1999; 13: 1501–12.CrossRefGoogle ScholarPubMed
Jones, S. M. & Kazlauskas, A.Growth-factor-dependent mitogenesis requires two distinct phases of signalling. Nat Cell Biol, 2001; 3: 165–72.CrossRefGoogle ScholarPubMed
Bartek, J. & Lukas, J.p27 destruction: Cks1 pulls the trigger. Nat Cell Biol, 2001; 3: E95–98.CrossRefGoogle ScholarPubMed
Della, R. F., Borriello, A., Mastropietro, S., et al.Expression of G1-phase cell cycle genes during hematopoietic lineage. Biochem Biophys Res Commun, 1997; 231: 73–6.CrossRefGoogle Scholar
Bassini, A., Pierpaoli, S., Falcieri, E., et al.Selective modulation of the cyclin B/CDK1 and cyclin D/CDK4 complexes during in vitro human megakaryocyte development. Br J Haematol, 1999; 104: 820–8.CrossRefGoogle ScholarPubMed
Yaroslavskiy, B., Watkins, S., Donnenberg, A. D., Patton, T. J., & Steinman, R. A.Subcellular and cell-cycle expression profiles of CDK-inhibitors in normal differentiating myeloid cells. Blood, 1999; 93: 2907–17.Google ScholarPubMed
Taniguchi, T., Endo, H., Chikatsu, N., et al.Expression of p21Cip1/Waf1/Sdi1 and p27Kip1 cyclin-dependent kinase inhibitors during human hematopoiesis. Blood, 1999; 93: 4167–78.Google Scholar
Hsieh, F. F., Barnett, L. A., Green, W. F., et al.Cell cycle exit during terminal erythroid differentiation is associated with accumulation of p27(Kip1) and inactivation of cdk2 kinase. Blood, 2000; 96: 2746–54.Google ScholarPubMed
Cheng, T., Rodrigues, N., Shen, H., et al.Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science, 2000; 287: 1804–8.CrossRefGoogle ScholarPubMed
Cheng, T., Rodrigues, N., Dombkowski, D., Stier, S., & Scadden, D. T.Stem cell repopulation efficiency but not pool size is governed by p27kip1. Nat Med, 2000; 6: 1235–40.CrossRefGoogle ScholarPubMed
Zandstra, P. W., Conneally, E., Petzer, A. L., Piret, J. M., & Eaves, C. J.Cytokine manipulation of primitive human hematopoietic cell self-renewal. Proc Natl Acad Sci U S A, 1997; 94: 4698–703.CrossRefGoogle ScholarPubMed
Matsunaga, T., Kato, T., Miyazaki, H., & Ogawa, M.Thrombopoietin promotes the survival of murine hematopoietic long-term reconstituting cells: comparison with the effects of FLT3/FLK-2 ligand and interleukin-6. Blood, 1998; 92: 452–61.Google ScholarPubMed
Borge, O. J., Ramsfjell, V., Cui, L., & Jacobsen, S. E. W.Ability of early acting cytokines to directly promote survival and suppress apoptosis of human primitive CD34+CD38− bone marrow cells with multilineage potential at the single-cell level: key role of thrombopoietin. Blood, 1997; 90: 2282–92.Google ScholarPubMed
Sitnicka, E., Lin, N., Priestley, G. V., et al.The effect of thrombopoietin on the proliferation and differentiation of murine hematopoietic stem cells. Blood, 1996; 87: 4998–5005.Google ScholarPubMed
Li, C. L. & Johnson, G. R.Stem cell factor enhances the survival but not the self-renewal of murine hematopoietic long-term repopulating cells. Blood, 1994; 84: 408–14.Google Scholar
Takatoku, M., Sellers, S., Agricola, B. A., et al.Avoidance of stimulation improves engraftment of cultured and retrovirally transduced hematopoietic cells in primates. J Clin Invest, 2001; 108: 447–55.CrossRefGoogle ScholarPubMed
Fauser, A. A. & Messner, H. A.Proliferative state of human pluripotent hemopoietic progenitors (CFU-GEMM) in normal individuals and under regenerative conditions after bone marrow transplantation. Blood, 1979; 54: 1197–200.Google ScholarPubMed
Jordan, C. T., Yamasaki, G., & Minamoto, D.High-resolution cell cycle analysis of defined phenotypic subsets within primitive human hematopoietic cell populations. Exp Hematol, 1996; 24: 1347–55.Google ScholarPubMed
Berardi, A. C., Wang, A., Levine, J. D., Lopez, P., & Scadden, D. T.Functional isolation and characterization of human hematopoietic stem cells. Science, 1995; 267: 104–8.CrossRefGoogle ScholarPubMed
Gothot, A., Loo, J. C. M., Clapp, W., & Srour, E. F.Cell cycle-related changes in repopulating capacity of human mobilized peripheral blood CD34+cells in non-obese diabetic/severe combined immune-deficient mice. Blood, 1998; 92: 2641–9.Google ScholarPubMed
Bradford, G. B., Williams, B., Rossi, R., & Bertoncello, I.Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. Exp Hematol, 1997; 25: 445–53.Google ScholarPubMed
Cheshier, S. H., Morrison, S. J., Liao, X., & Weissman, I. L.In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc Natl Acad Sci U S A, 1999; 96: 3120–5.CrossRefGoogle ScholarPubMed
Mahmud, N., Devine, S. M., Weller, K. P., et al.The relative quiescence of hematopoietic stem cells in nonhuman primates. Blood, 2001; 97: 3061–8.CrossRefGoogle ScholarPubMed
Rufer, N., Brummendorf, T. H., Kolvraa, S., et al.Telomere fluorescence measurements in granulocytes and T lymphocyte subsets point to a high turnover of hematopoietic stem cells and memory T cells in early childhood. J Exp Med, 1999; 190: 157–67.CrossRefGoogle Scholar
Gordon, M. Y., Riley, G. P., Watt, S. M., & Greaves, M. F.Compartmentalization of a haematopoietic growth factor (GM-CSF) by glycosaminoglycans in the bone marrow microenvironment. Nature, 1987; 326: 403–5.CrossRefGoogle ScholarPubMed
Roberts, R., Gallagher, J., Spooncer, E., et al.Heparan sulphate bound growth factors: a mechanism for stromal cell mediated haemopoiesis. Nature, 1988; 332: 376–8.CrossRefGoogle ScholarPubMed
Anderson, D. M., Lyman, S. D., Baird, A., et al.Molecular cloning of mast cell growth factor, a hematopoietin that is active in both membrane bound and soluble forms. Cell, 1990; 63: 235–43.CrossRefGoogle ScholarPubMed
Flanagan, J. G., Chan, D. C., & Leder, P.Transmembrane form of the kit ligand growth factor is determined by alternative splicing and is missing in the SId mutant. Cell, 1991; 64: 1025–35.CrossRefGoogle ScholarPubMed
Rettenmier, C. W., Roussel, M. F., Ashmun, R. A., et al.Synthesis of membrane-bound colony-stimulating factor 1 (CSF-1) and downmodulation of CSF-1 receptors in NIH 3T3 cells transformed by cotransfection of the human CSF-1 and c-fms (CSF-1 receptor) genes. Mol Cell Biol, 1987; 7: 2378–87.CrossRefGoogle ScholarPubMed
Stein, J., Borzillo, G. V., & Rettenmier, C. W.Direct stimulation of cells expressing receptors for macrophage colony-stimulating factor (CSF-1) by a plasma membrane-bound precursor of human CSF-1. Blood, 1990; 76: 1308–14.Google ScholarPubMed
Gidali, J. & Lajtha, L. G.Regulation of haemopoietic stem cell turnover in partially irradiated mice. Cell Tissue Kinet, 1972; 5: 147–57.Google ScholarPubMed
McCulloch, E. A., Siminovitch, L., Till, J. E., Russell, E. S., & Bernstein, S. E.The cellular basis of the genetically determined hemopoietic defect in anemic mice of genotype Sl/Sld. Blood, 1965; 26: 399–410.Google Scholar
Graham, G. J., Wright, E. G., Hewick, R., et al.Identification and characterization of an inhibitor of haemopoietic stem cell proliferation. Nature, 1990; 344: 442–4.CrossRefGoogle ScholarPubMed
Broxmeyer, H. E., Sherry, B., Lu, L., et al.Enhancing and suppressing effects of recombinant murine macrophage inflammatory proteins on colony formation in vitro by bone marrow myeloid progenitor cells. Blood, 1990; 76: 1110–16.Google ScholarPubMed
Quesniaux, V. F. J., Graham, G. J., Pragnell, I., et al.Use of 5-fluorouracil to analyze the effect of macrophage inflammatory protein-1a on long-term reconstituting stem cells in vivo. Blood, 1993; 81: 1497–504.Google Scholar
Eaves, C. J., Cashman, J. D., Wolpe, S. D., & Eaves, A. C.Unresponsiveness of primitive chronic myeloid leukemia cells to macrophage inflammatory protein 1 alpha, an inhibitor of primitive normal hematopoietic cells. Proc Natl Acad Sci U S A, 1993; 90: 12015–9.CrossRefGoogle ScholarPubMed
Cashman, J. D., Clark-Lewis, I., Eaves, A. C., & Eaves, C. J.Differentiation stage-specific regulation of primitive human hematopoietic progenitor cycling by exogenous and endogenous inhibitors in an in vivo model. Blood, 1999; 94: 3722–9.Google Scholar
Cashman, J. D., Eaves, C. J., Sarris, A. H., & Eaves, A. C.MCP-1, not MIP-1alpha is the endogenous chemokine that cooperates with TGF-beta to inhibit the cycling of primitive normal but not leukemic (CML) progenitors in long-term human marrow cultures. Blood, 1998; 92: 2338–44.Google Scholar
Cashman, J., Clark-Lewis, I., Eaves, A., & Eaves, C.Stromal-derived factor 1 inhibits the cycling of very primitive human hematopoietic cells in vitro and in NOD/SCID mice. Blood, 2002; 99: 792–9.CrossRefGoogle ScholarPubMed
Cashman, J., Dykstra, B., Clark-Lewis, I., Eaves, A., & Eaves, C.Changes in the proliferative activity of human hematopoietic stem cells in NOD/SCID mice and enhancement of their transplantability after in vivo treatment with cell cycle inhibitors. J Exp Med, 2002; 196: 1141–9.CrossRefGoogle ScholarPubMed
Glimm, H., Tang, P., Clark-Lewis, I., Kalle, C. von, & Eaves, C.Ex vivo treatment of proliferating human cord blood stem cells with stroma-derived factor-1 enhances their ability to engraft NOD/SCID mice. Blood, 2002; 99: 3454–7.CrossRefGoogle ScholarPubMed
Till, J. E., McCulloch, E. A., & Siminovitch, L.A stochastic model of stem cell proliferation, based on the growth of spleen colony-forming cells. Proc Natl Acad Sci U S A, 1964; 51: 29–36.CrossRefGoogle ScholarPubMed
Vogel, H., Niesisch, H., & Matioli, G.The self-renewal probability of haemopoietic stem cells. J Cell Physiol, 1968; 72: 221.CrossRefGoogle Scholar
Till, J. E. & McCulloch, E. A.Hemopoietic stem cell differentiation. Biochim Biophys Acta, 1980; 605: 431–59.Google ScholarPubMed
Humphries, R. K., Eaves, A. C., & Eaves, C. J. Expression of stem cell behaviour during macroscopic burst formation in vitro. In , S. J. Baum, , G. D. Ledney, & , D. W. van Bekkum, eds., Experimental Hematology Today (New York: Karger, 1980), pp. 39–46.Google Scholar
Nakahata, T., Gross, A. J., & Ogawa, M.A stochastic model of self-renewal and commitment to differentiation of the primitive hemopoietic stem cells in culture. J Cell Physiol, 1982; 113: 455–8.CrossRefGoogle ScholarPubMed
Eaves, C., Miller, C., Conneally, E., et al.Introduction to stem cell biology in vitro: threshold to the future. Ann N Y Acad Sci, 1999; 872: 1–8.CrossRefGoogle Scholar
Iscove, N. N. & Nawa, K.Hematopoietic stem cells expand during serial transplantation in vivo without apparent exhaustion. Curr Biol, 1997; 7: 805–8.CrossRefGoogle ScholarPubMed
Thorsteinsdottir, U., Sauvageau, G., & Humphries, R. K.Enhanced in vivo regenerative potential of HOXB4-transduced hematopoietic stem cells with regulation of their pool size. Blood, 1999; 94: 2605–12.Google ScholarPubMed
Pineault, N., Helgason, C. D., Lawrence, H. J., & Humphries, R. K.Differential expression of Hox, Meis1 and Pbx1 genes in primitive cells throughout murine hematopoietic ontogeny. Exp Hematol, 2002; 30: 49–57.CrossRefGoogle ScholarPubMed
Lessard, J., Baban, S., & Sauvageau, G.Stage-specific expression of Polycomb group genes in human bone marrow cells. Blood, 1998; 91: 1216–24.Google ScholarPubMed
Park, I. K., Qian, D., Kiel, M., et al.Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature, 2003; 423: 302–5.CrossRefGoogle ScholarPubMed
Sauvageau, G., Thorsteinsdottir, U., Eaves, C. J., et al.Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes Dev, 1995; 9: 1753–65.CrossRefGoogle ScholarPubMed
Buske, C., Feuring-Buske, M., Abramovich, C., et al.Deregulated expression of HOXB4 enhances the primitive growth activity of human hematopoietic cells. Blood, 2002; 100: 862–8.CrossRefGoogle ScholarPubMed
Antonchuk, J., Sauvageau, G., & Humphries, R. K.HoxB4-induced expansion of adult hematopoietic stem cells ex vivo. Cell, 2002; 109: 39–45.CrossRefGoogle ScholarPubMed
Lessard, J. & Sauvageau, G.Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature, 2003; 423: 255–60.CrossRefGoogle ScholarPubMed
Krosl, J., Austin, P., Beslu, N., et al.In vitro expansion of hematopoietic stem cells by recombinant TAT-HOXB4 protein. Nat Med, 2003; 9: 1428–32.CrossRefGoogle ScholarPubMed
Tsuji, K., Lyman, S. D., Sudo, T., Clark, S. C., & Ogawa, M.Enhancement of murine hematopoiesis by synergistic interactions between Steel factor (ligand for c-kit), Interleukin-11, and other early acting factors in culture. Blood, 1992; 79: 2855–60.Google Scholar
Yonemura, Y., Ku, H., Lyman, S. D., & Ogawa, M.In vitro expansion of hematopoietic progenitors and maintenance of stem cells: comparison between Flt3/Flk-2 ligand and kit ligand. Blood, 1997; 89: 1915–21.Google ScholarPubMed
Ueda, T., Tsuji, K., Yoshino, H., et al.Expansion of human NOD/SCID-repopulating cells by stem cell factor, Flk2/Flt3 ligand, thrombopoietin, IL-6, and soluble IL-6 receptor. J Clin Invest, 2001; 105: 1013–21.CrossRefGoogle Scholar
Ramsfjell, V., Borge, O. J., Veiby, O. P., et al.Thrombopoietin, but not erythropoietin, directly stimulates multilineage growth of primitive murine bone marrow progenitor cells in synergy with early acting cytokines: distinct interactions with the ligands for c-kit and FLT3. Blood, 1996; 88: 4481–92.Google Scholar
Ku, H., Yonemura, Y., Kaushansky, K., & Ogawa, M.Thrombopoietin, the ligand for the Mpl receptor, synergizes with steel factor and other early acting cytokines in supporting proliferation of primitive hematopoietic progenitors of mice. Blood, 1996; 87: 4544–51.Google Scholar
Petzer, A. L., Zandstra, P. W., Piret, J. M., & Eaves, C. J.Differential cytokine effects on primitive (CD34+CD38−) human hematopoietic cells: novel responses to flt3-ligand and thrombopoietin. J Exp Med, 1996; 183: 2551–8.CrossRefGoogle ScholarPubMed
Ebihara, Y., Wada, M., Ueda, T., et al.Reconstitution of human haematopoiesis in non-obese diabetic/severe combined immunodeficient mice by clonal cells expanded from single CD34+CD38− cells expressing Flk2/Flt3. Br J Haematol, 2002; 119: 525–34.CrossRefGoogle ScholarPubMed
Sitnicka, E., Buza-Vidas, N., Larsson, S., et al.Human CD34+ hematopoietic stem cells capable of multilineage engrafting NOD/SCID mice express flt3: distinct flt3 and c-kit expression and response patterns on mouse and candidate human hematopoietic stem cells. Blood, 2003; 102: 881–6.CrossRefGoogle ScholarPubMed
Murdoch, B., Chadwick, K., Martin, M., et al.Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc Natl Acad Sci U S A, 2003; 100: 3422–7.CrossRefGoogle ScholarPubMed
Cobas, M., Wilson, A., Ernst, B., et al.β-catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med, 2004; 199: 221–9.CrossRefGoogle ScholarPubMed
Bryder, D., Ramsfjell, V., Dybedal, I., et al.Self-renewal of multipotent long-term repopulating hematopoietic stem cells is negatively regulated by fas and tumor necrosis factor receptor activation. J Exp Med, 2001; 194: 941–52.CrossRefGoogle ScholarPubMed
Dybedal, I., Bryder, D., Fossum, A., Rusten, L. S., & Jacobsen, S. E.Tumor necrosis factor (TNF)-mediated activation of the p55 TNF receptor negatively regulates maintenance of cycling reconstituting human hematopoietic stem cells. Blood, 2001; 98: 1782–91.CrossRefGoogle ScholarPubMed
Shivdasani, R. A. & Orkin, S. H.The transcriptional control of hematopoiesis. Blood, 1996; 87: 4025–39.Google ScholarPubMed
Tenen, D. G., Hromas, R., Licht, J. D., & Zhang, D.Transcription factors, normal myeloid development and leukemia. Blood, 1997; 90: 489–519.Google ScholarPubMed
Nutt, S. L., Heavey, B., Rolink, A. G., & Busslinger, M.Commitment to the B-lymphoid lineage depends on the transcription factor Pax5. Nature, 1999; 401: 556–62.CrossRefGoogle ScholarPubMed
Westin, E. H., Gallo, R. C., Arya, S. K., et al.Differential expression of the amv gene in human hematopoietic cells. Proc Natl Acad Sci U S A, 1982; 79: 2194–8.CrossRefGoogle ScholarPubMed
Gonda, T. J. & Metcalf, D.Expression of myb, myc and fos proto-oncogenes during the differentiation of a murine myeloid leukaemia. Nature, 1984; 310: 249–51.CrossRefGoogle ScholarPubMed
Sheiness, D. & Gardinier, M.Expression of a proto-oncogene (proto-myb) in hemopoietic tissues of mice. Mol Cell Biol, 1984; 4: 1206–12.CrossRefGoogle Scholar
Buske, C. & Humphries, R. K.Homeobox genes in leukemogenesis. Int J Hematol, 2000; 71: 301–8.Google ScholarPubMed
Lawrence, H. J., Sauvageau, G., Largman, C., & Humphries, R. K. Homeobox gene networks and the regulation of hematopoiesis. In , L. I. Zon, ed., Hematopoiesis: A Developmental Approach (New York: Oxford University Press, 2001), pp. 402–14.Google Scholar
Katzav, S., Martin-Zanca, D., & Barbacid, M.Vav, a novel human oncogene derived from a locus ubiquitously expressed in hematopoetic cells. EMBO J, 1989; 8: 2283–90.Google Scholar
Adams, J. M., Houston, H., Allen, J., Lints, T., & Harvey, R.The hematopoietically expressed vav proto-oncogene shares homology with the dbl GDP-GTP exchange factor, the bcr gene and a yeast gene (CDC24) involved in cytoskeletal organization. Oncogene, 1992; 7: 611–18.Google Scholar
Wagner, J. E., Collins, D., Fuller, S., et al.Isolation of small, primitive human hematopoietic stem cells: distribution of cell surface cytokine receptors and growth in SCID-Hu mice. Blood, 1995; 86: 512–23.Google ScholarPubMed
Testa, U., Fossati, C., Samoggia, P., et al.Expression of growth factor receptors in unilineage differentiation culture of purified hematopoietic progenitors. Blood, 1996; 88: 3391–406.Google ScholarPubMed
McKinstry, W. J., Li, C. L., Rasko, J. E. J., et al.Cytokine receptor expression on hematopoietic stem and progenitor cells. Blood, 1997; 89: 65–71.Google ScholarPubMed
Helgason, C. D., Damen, J. E., Rosten, P., et al.Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev, 1998; 12: 1610–20.CrossRefGoogle Scholar
Voura, E. B., Billia, F., Iscove, N. N., & Hawley, R. G.Expression mapping of adhesion receptor genes during differentiation of individual hematopoietic precursors. Exp Hematol, 1997; 25: 1172–9.Google ScholarPubMed
Mucenski, M. L., McLain, K., Kier, A. B., et al.A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell, 1991; 65: 677–89.CrossRefGoogle ScholarPubMed
Pevny, L., Simon, M. C., Robertson, E., et al.Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature, 1991; 349: 257–60.CrossRefGoogle ScholarPubMed
Georgopoulos, K., Moore, D. D., & Derfler, B.Ikaros, an early lymphoid-specific transcription factor and a putative mediator for T cell commitment. Science, 1992; 258: 808–12.CrossRefGoogle Scholar
Georgopoulos, K., Bigby, M., Wang, J. H., et al.Early arrest in lymphocyte differentiation in Ikaros mutant mice. Cell, 1994; 78: 143–56.CrossRefGoogle Scholar
Scott, E. W., Simon, M. C., Anastasi, J., & Singh, H.Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science, 1994; 265: 1573–7.CrossRefGoogle ScholarPubMed
Urbanek, P., Wang, Z.-Q., Fetka, I., Wagner, E. F., & Busslinger, M.Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell, 1994; 79: 901–12.CrossRefGoogle Scholar
Olson, M. C., Scott, E. W., Hack, A. A., et al.PU.1 is not essential for early myeloid gene expression but is required for terminal myeloid differentiation. Immunity, 1995; 3: 703–14.CrossRefGoogle Scholar
Robb, L., Elwood, N. J., Elefanty, A. G., et al.The scl gene is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J, 1996; 15: 4123–9.Google ScholarPubMed
Porcher, C., Swat, W., Rockwell, K., et al.The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell, 1996; 86: 47–57.CrossRefGoogle Scholar
Okuda, T., Deursen, J., Hiebert, S. W., Grosveld, G., & Downing, J. R.AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell, 1996; 84: 321–30.CrossRefGoogle ScholarPubMed
Sasaki, K., Yagi, H., Bronson, R. T., et al.Absence of fetal liver hematopoiesis in mice deficient in transcriptional coactivator core binding factor beta. Proc Natl Acad Sci U S A, 1996; 93: 12359–63.CrossRefGoogle ScholarPubMed
Wang, Q., Stacy, T., Binder, M., et al.Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci U S A, 1996; 93: 3444–9.CrossRefGoogle ScholarPubMed
Hendriks, R. W., Nawijn, M. C., Engel, J. D., et al.Expression of the transcription factor GATA-3 is required for the development of the earliest T cell progenitors and correlates with stages of cellular proliferation in the thymus. Eur J Immunol, 1999; 29: 1912–18.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
Valtieri, M., Tocci, A., Gabbianelli, M., et al.Enforced TAL-1 expression stimulates primitive, erythroid and megakaryocytic progenitors but blocks the granulopoietic differentiation program. Cancer Res, 1998; 58: 562–9.Google ScholarPubMed
Iwasaki, H., Mizuno, S., Wells, R. A., et al.GATA-1 converts lymphoid and myelomonocytic progenitors into the megakaryocyte/erythrocyte lineages. Immunity, 2003; 19: 451–62.CrossRefGoogle ScholarPubMed
Thorsteinsdottir, U., Sauvageau, G., Hough, M. R., et al.Overexpression of HOXA10 in murine hematopoietic cells perturbs both myeloid and lymphoid differentiation and leads to acute myeloid leukemia. Mol Cell Biol, 1997; 17: 495–505.CrossRefGoogle ScholarPubMed
Sauvageau, G., Thorsteinsdottir, U., Hough, M. R., et al.Overexpression of HOXB3 in hematopoietic cells causes defective lymphoid development and progressive myeloproliferation. Immunity, 1997; 6: 13–22.CrossRefGoogle ScholarPubMed
Kulessa, H., Frampton, J., Graf, T.GATA-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, and erythroblasts. Genes Dev, 1995; 9: 1250–62.CrossRefGoogle ScholarPubMed
Thorsteinsdottir, U., Mamo, A., Kroon, E., et al.Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood, 2002; 99: 121–9.CrossRefGoogle ScholarPubMed
Taghon, T., Stolz, F., De Smedt, M., et al.HOX-A10 regulates hematopoietic lineage commitment: evidence for a monocyte-specific transcription factor. Blood, 2002; 99: 1197–204.CrossRefGoogle ScholarPubMed
Hirasawa, R., Shimizu, R., Takahashi, S., et al.Essential and instructive roles of GATA factors in eosinophil development. J Exp Med, 2002; 195: 1379–86.CrossRefGoogle ScholarPubMed
Cantor, A. B. & Orkin, S. H.Hematopoietic development: a balancing act. Curr Opin Genet Dev, 2001; 11: 513–19.CrossRefGoogle ScholarPubMed
Rolink, A. G., Nutt, S. L., Melchers, F., & Busslinger, M.Long-term in vivo reconstitution of T-cell development by Pax5-deficient B-cell progenitors. Nature, 1999; 401: 603–6.CrossRefGoogle ScholarPubMed
Nerlov, C., Querfurth, E., Kulessa, H., & Graf, T.GATA-1 interacts with the myeloid PU.1 transcription factor and represses PU.1-dependent transcription. Blood, 2000; 95: 2543–51.Google ScholarPubMed
Zhang, P., Behre, G., Pan, J., et al.Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1. Proc Natl Acad Sci U S A, 1999; 96: 8705–10.CrossRefGoogle ScholarPubMed
Rekhtman, N., Radparvar, F., Evans, T., & Skoultchi, A. I.Direct interaction of hematopoietic transcription factors PU.1 and GATA-1: functional antagonism in erythroid cells. Genes Dev, 1999; 13: 1398–411.CrossRefGoogle ScholarPubMed
Querfurth, E., Schuster, M., Kulessa, H., et al.Antagonism between C/EBPbeta and FOG in eosinophil lineage commitment of multipotent hematopoietic progenitors. Genes Dev, 2000; 14: 2515–25.CrossRefGoogle ScholarPubMed
Wu, A. M., Siminovitch, L., Till, J. E., & McCulloch, E. A.Evidence for a relationship between mouse hemopoietic stem cells and cells forming colonies in culture. Proc Natl Acad Sci U S A, 1968; 59: 1209–15.CrossRefGoogle ScholarPubMed
Suda, T., Suda, J., & Ogawa, M.Disparate differentiation in mouse hemopoietic colonies derived from paired progenitors. Proc Natl Acad Sci U S A, 1984; 81: 2520–4.CrossRefGoogle ScholarPubMed
Takano, H., Ema, H., Sudo, K., & Nakauchi, H.Asymmetric division and lineage commitment at the level of hematopoietic stem cells: inference from differentiation in daughter cell and granddaughter cell pairs. J Exp Med, 2004; 199: 295–302.CrossRefGoogle ScholarPubMed
Pharr, P. N., Ogawa, M., Hofbauer, A., & Longmore, G. D.Expression of an activated erythropoietin or a colony-stimulating factor 1 receptor by pluripotent progenitors enhances colony formation but does not induce differentiation. Proc Natl Acad Sci U S A, 1994; 91: 7482–6.CrossRefGoogle Scholar
Goldsmith, M. A., Mikami, A., You, Y., et al.Absence of cytokine receptor-dependent specificity in red blood cell differentiation in vivo. Proc Natl Acad Sci USA, 1998; 95: 7006–11.CrossRefGoogle ScholarPubMed
Stoffel, R., Ziegler, S., Ghilardi, N., et al.Permissive role of thrombopoietin and granulocyte colony-stimulating factor receptors in hematopoietic cell fate decisions in vivo. Proc Natl Acad Sci U S A, 1999; 96: 698–702.CrossRefGoogle ScholarPubMed
Dexter, T. M., Heyworth, C. M., Spooncer, E., & Ponting, I. L. O.The role of growth factors in self-renewal and differentiation of haemopoietic stem cells. Philos Trans R Soc Lond B Biol Sci, 1990; 327: 85–98.CrossRefGoogle ScholarPubMed
Borzillo, G. V., Ashmun, R. A., & Sherr, C. J.Macrophage lineage switching of murine early pre-B lymphoid cells expressing transduced fms genes. Mol Cell Biol, 1990; 10: 2703–14.CrossRefGoogle ScholarPubMed
Martin, M., Strasser, A., Baumgarth, N., et al.A novel cellular model (SPGM 1) of switching between the pre-B cell and myelomonocytic lineages. J Immunol, 1993; 150: 4395–406.Google ScholarPubMed
Klinken, S. P., Alexander, W. S., & Adams, J. M.Hemopoietic lineage switch: v-raf oncogene converts Emu-myc transgenic B cells into macrophages. Cell, 1988; 53: 857–67.CrossRefGoogle ScholarPubMed
Kondo, M., Scherer, D. C., Miyamoto, T., et al.Cell-fate conversion of lymphoid-committed progenitors by instructive actions of cytokines. Nature, 2000; 407: 383–6.CrossRefGoogle ScholarPubMed
Fukunaga, R., Ishizaka-Ikeda, E., & Nagata, S.Growth and differentiation signals mediated by different regions in the cytoplasmic domain of granulocyte colony-stimulating factor receptor. Cell, 1993; 74: 1079–87.CrossRefGoogle ScholarPubMed
Metcalf, D.Clonal analysis of proliferation and differentiation of paired daughter cells: action of granulocyte-macrophage colony-stimulating factor on granulocyte-macrophage precursors. Proc Natl Acad Sci U S A, 1980; 77: 5327–30.CrossRefGoogle ScholarPubMed
Metcalf, D. & Burgess, A. W.Clonal analysis of progenitor cell commitment to granulocyte or macrophage production. J Cell Physiol, 1982; 111: 275–83.CrossRefGoogle ScholarPubMed
Metcalf, D.Lineage commitment in the progeny of murine hematopoietic preprogenitor cells: influence of thrombopoietin and interleukin 5. Proc Natl Acad Sci U S A, 1998; 95: 6408–12.CrossRefGoogle ScholarPubMed
Campbell, K. H., McWhir, J., Ritchie, W. A., & Wilmut, I.Sheep cloned by nuclear transfer from a cultured cell line. Nature, 1996; 380: 64–6.CrossRefGoogle ScholarPubMed
Orlic, D., Kajstura, J., Chimenti, S., et al.Bone marrow cells regenerate infarcted myocardium. Nature, 2001; 410: 701–5.CrossRefGoogle ScholarPubMed
Orlic, D., Kajstura, J., Chimenti, S., et al.Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A, 2001; 98: 10 344–9.CrossRefGoogle Scholar
Jackson, K. A., Majka, S. M., Wang, H., et al.Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest, 2001; 107: 1395–402.CrossRefGoogle ScholarPubMed
Strauer, B. E., Brehm, M., Zeus, T., et al.Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation, 2002; 106: 1913–18.CrossRefGoogle ScholarPubMed
Ferrari, G., Cusella-De Angelis, G., Coletta, M., et al.Muscle regeneration by bone marrow-derived myogenic progenitors. Science, 1998; 279: 1528–30.CrossRefGoogle ScholarPubMed
Jackson, K. A., Mi, T., & Goodell, M. A.Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci U S A, 1999; 96: 14482–6.CrossRefGoogle ScholarPubMed
Petersen, B. E., Bowen, W. C., Patrene, K. D., et al.Bone marrow as a potential source of hepatic oval cells. Science, 1999; 284: 1168–70.CrossRefGoogle ScholarPubMed
Lagasse, E., Connors, H., Al-Dhalimy, M., et al.Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med, 2000; 6: 1229–34.CrossRefGoogle ScholarPubMed
Theise, N. D., Badve, S., Saxena, R., et al.Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology, 2000; 31: 235–40.CrossRefGoogle ScholarPubMed
Theise, N. D., Nimmakayalu, M., Gardner, R., et al.Liver from bone marrow in humans. Hepatology, 2000; 32: 11–16.CrossRefGoogle ScholarPubMed
Alison, M. R., Poulsom, R., Jeffery, R., et al.Hepatocytes from non-hepatic adult stem cells. Nature, 2000; 406: 257.CrossRefGoogle ScholarPubMed
Krause, D. S., Theise, N. D., Collector, M. I., et al.Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell, 2001; 105: 369–77.CrossRefGoogle ScholarPubMed
Wang, X., Ge, S., McNamara, G., et al.Albumin-expressing hepatocyte-like cells develop in the livers of immune-deficient mice that received transplants of highly purified human hematopoietic stem cells. Blood, 2003; 101: 4201–8.CrossRefGoogle ScholarPubMed
Ishikawa, F., Drake, C. J., Yang, S., et al.Transplanted human cord blood cells give rise to hepatocytes in engrafted mice. Ann N Y Acad Sci, 2003; 996: 174–85.CrossRefGoogle ScholarPubMed
Eglitis, M. A. & Mezey, E.Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci U S A, 1997; 94: 4080–5.CrossRefGoogle ScholarPubMed
Kopen, G. C., Prockop, D. J., & Phinney, D. G.Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci U S A, 2000; 96: 10711–16.CrossRefGoogle Scholar
Brazelton, T. R., Rossi, F. M., Keshet, G. I., & Blau, H. M.From marrow to brain: expression of neuronal phenotypes in adult mice. Science, 2000; 290: 1775–9.CrossRefGoogle ScholarPubMed
Mezey, E., Chandross, K. J., Harta, G., Maki, R. A., & McKercher, S. R.Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science, 2000; 290: 1779–82.CrossRefGoogle ScholarPubMed
Wagers, A. J., Sherwood, R. I., Christensen, J. L., & Weissman, I. L.Little evidence for developmental plasticity of adult hematopoietic stem cells. Science, 2002; 297: 2256–9.CrossRefGoogle ScholarPubMed
Castro, R. F., Jackson, K. A., Goodell, M. A., et al.Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science, 2002; 297: 1299.CrossRefGoogle ScholarPubMed
Wang, X., Willenbring, H., Akkari, Y., et al.Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature, 2003; 422: 897–901.CrossRefGoogle ScholarPubMed
Balsam, L. B., Wagers, A. J., Christensen, J. L., et al.Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature, 2004; 428: 668–73.CrossRefGoogle ScholarPubMed
Murry, C. E., Soonpaa, M. H., Reinecke, H., et al.Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature, 2004; 428: 664–8.CrossRefGoogle Scholar
Taniguchi, H., Toyoshima, T., Fukao, K., & Nakauchi, H.Presence of hematopoietic stem cells in the adult liver. Nat Med, 1996; 2: 198–203.CrossRefGoogle ScholarPubMed
Iwatani, H., Ito, T., Imai, E., et al.Hematopoietic and nonhematopoietic potentials of Hoechst/side population cells isolated from adult rat kidney. Kidney Int, 2004; 65: 1604–14.CrossRefGoogle ScholarPubMed
Ying, Q. L., Nichols, J., Evans, E. P., & Smith, A. G.Changing potency by spontaneous fusion. Nature, 2002; 416: 545–8.CrossRefGoogle ScholarPubMed
Terada, N., Hamazaki, T., Oka, M., et al.Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature, 2002; 416: 542–5.CrossRefGoogle ScholarPubMed
Weimann, J. M., Johansson, C. B., Trejo, A., & Blau, H. M.Stable reprogrammed heterokaryons form spontaneously in Purkinje neurons after bone marrow transplant. Nat Cell Biol, 2003; 5: 959–66.CrossRefGoogle ScholarPubMed
Corbel, S. Y., Lee, A., Yi, L., et al.Contribution of hematopoietic stem cells to skeletal muscle. Nat Med, 2003; 9: 1528–32.CrossRefGoogle ScholarPubMed
Camargo, F. D., Green, R., Capetenaki, Y., Jackson, K. A., & Goodell, M. A.Single hematopoietic stem cells generate skeletal muscle through myeloid intermediates. Nat Med, 2003; 9: 1520–7.CrossRefGoogle ScholarPubMed
Van der Loo, J. C. M., Hanenberg, H., Cooper, R. J., et al.Nonobese diabetic/severe combined immunodeficiency (NOD/SCID) mouse as a model system to study the engraftment and mobilization of human peripheral blood stem cells. Blood, 1998; 92: 2556–70.Google Scholar
Eaves, C., Cashman, J., & Eaves, A.Defective regulation of leukemic hematopoiesis in chronic myeloid leukemia. Leuk Res, 1998; 22: 1085–96.CrossRefGoogle ScholarPubMed

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