Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-12T11:00:29.323Z Has data issue: false hasContentIssue false
  • English
  • Français

The Significant Role of Centrosomes in Stem Cell Division and Differentiation

Published online by Cambridge University Press:  11 July 2011

Heide Schatten  and
Qing-Yuan Sun
Heide Schatten*
Affiliation:
Department of Veterinary Pathobiology, University of Missouri, Columbia, MO 65211, USA
Qing-Yuan Sun
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China
*
Corresponding author. E-mail: SchattenH@missouri.edu
Get access

Abstract

The role of centrosomes in stem cell division has recently been highlighted and further ascribes important functions to centrosomes in stem cell maintenance, cellular differentiation, and development. Advanced cell and molecular studies coupled with immunofluorescence, electron microscopy, and live cell imaging of specific centrosome proteins have contributed greatly to our knowledge of centrosome composition, structure, and dynamics and have uncovered new insights into mechanisms of centrosome functions in asymmetric cell division. The establishment of asymmetry and differential positioning of mother and daughter centrosomes during stem cell mitosis is important for allowing one cell to maintain stem cell characteristics while the sibling cell undergoes differentiation. Another key role for centrosomes has been revealed in primary cilia of embryonic stem cells that play significant roles in cellular signaling and are therefore critically important for stem cell decisions. Studies of signaling through primary cilia may contribute important information that may aid in the production of specific cells that are suitable for tissue repair and regeneration in the field of regenerative medicine.

Keywords

stem cellsasymmetric cell divisioncentriolescentrosomescytoskeletonprimary cilia
Type
Research Article
Information
Microscopy and Microanalysis , Volume 17 , Issue 4 , August 2011 , pp. 506 - 512
Copyright
Copyright © Microscopy Society of America 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alieva, I.B. & Uzbekov, R.E. (2008). The centrosome is a polyfunctional multiprotein cell complex. Biochemistry (Moscow) 73(6), 782–803.Google ScholarPubMed
Awan, A., Olivieri, R.O., Jensen, P.L., Christensen, S.T. & Andersen, C.Y. (2010). Immunofluorescence and mRNA analysis of human embryonic stem cells (hESCs) grown under feeder-free conditions. Methods Mol Biol 584, 195–210.CrossRefGoogle ScholarPubMed
Azimzadeh, J. & Bornens, M. (2007). Structure and duplication of the centrosome. J Cell Sci 120, 2139–2142.CrossRefGoogle ScholarPubMed
Bisgrove, B.W. & Yost, H.J. (2006). The roles of cilia in developmental disorders and disease. Development 133, 4131–4143.CrossRefGoogle ScholarPubMed
Boveri, T. (1887). Ueber die Befruchtung der Eier von Ascaris megalocephala. Sitz-Ber Ges Morph Phys München. Bd. III.Google Scholar
Boveri, T. (1888). Zellen-Studien II. Die Befruchtung und Teilung des Eies von Ascaris megalocephala. Z Naturwissen 22, 685–882.Google Scholar
Boveri, T. (1901). Zellen-Studien: Űber die Natur der Centrosomen. Z Med Naturw, vol. 28, pp. 1–220. Jena, Germany: Fisher.Google Scholar
Boveri, T. (1914). Zur Frage der Entstehung maligner Tumoren. Jena, Germany: G. Fisher.Google Scholar
Breunig, J.J., Sarkisian, M.R., Arellano, J.I., Morozov, Y.M., Ayoub, A.E., Sojitra, S., Wang, B., Flavell, R.A., Rakic, P. & Town, T. (2008). Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc Natl Acad Sci USA 105(35), 13127–13132.CrossRefGoogle ScholarPubMed
Cabernard, C. & Doe, C.Q. (2007). Stem cell self-renewal: Centrosomes on the move. Curr Biol 17(12), R465–R467.CrossRefGoogle ScholarPubMed
D'Angelo, A. & Franco, B. (2009). The dynamic cilium in human diseases. PathoGenetics 2(3), 1–15.CrossRefGoogle ScholarPubMed
Davenport, J.R. & Yoder, B.K. (2005). An incredible decade for the primary cilium: A look at a once-forgotten organelle. Am J Physiol Renal Physiol 289, F1159–F1169.CrossRefGoogle Scholar
Fuentealba, L.C., Eivers, E., Geissert, D., Taelman, V. & DeRobertis, E.M. (2008). Asymmetric mitosis: Unequal segregation of proteins destined for degradation. Proc Natl Acad Sci USA 105, 7732–7737.CrossRefGoogle ScholarPubMed
Gonzalez, C. (2008). Centrosome function during stem cell division: The devil is in the details. Curr Opin Cell Biol 20(6), 694–698.CrossRefGoogle ScholarPubMed
Han, Y.G., Spassky, N., Romaguera-Ros, M., Garcia-Verdugo, J.M., Aguilar, A., Schneider-Maunoury, S. & Alvarez-Buylla, A. (2008). Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11, 277–284.CrossRefGoogle ScholarPubMed
Hildebrandt, F. & Otto, E. (2005). Cilia and centrosomes: A unifying pathogenic concept for cystic kidney disease? Nat Rev Gen 6, 928–940.CrossRefGoogle ScholarPubMed
Kiprilov, E.N., Awan, A., Desprat, R., Velho, M., Clement, C.A., Byskov, A.G., Andersen, C.Y., Satir, P., Bouhassira, E.E., Christensen, S.T. & Hirsch, R.E. (2008). Human embryonic stem cells in culture possess primary cilia with hedgehog signaling machinery. J Cell Biol 180(5), 897–904.CrossRefGoogle ScholarPubMed
Kodani, A., Kristensen, I., Huang, L. & Sütterlin, C. (2009). GM130-dependent control of Cdc42 activity at the Golgi regulates centrosome function. Mol Biol Cell 20, 1192–1200.CrossRefGoogle Scholar
Kodani, A. & Sütterlin, C. (2008). The Golgi protein GM130 regulates centrosome organization and function. Mol Biol Cell 19, 745–753.CrossRefGoogle Scholar
Lehtonen, S., Shah, M., Nielsen, R., Iino, N., Ryan, J.J., Zhou, H. & Farquhar, M.G. (2008). The endocytic adaptor protein ARH associates with motor and centrosomal proteins and is involved in centrosome assembly and cytokinesis. Mol Biol Cell 19(7), 2949–2961.CrossRefGoogle ScholarPubMed
Malone, A.M.D., Anderson, C.T., Tummala, P., Kwon, R.Y., Johnston, T.R., Stearns, T. & Jacobs, C.R. (2007). Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc Natl Acad Sci 104, 13325.CrossRefGoogle ScholarPubMed
Michaud, E.J. & Yoder, B.K. (2006). The primary cilium in cell signaling and cancer. Cancer Res 66, 6463–6467.CrossRefGoogle Scholar
Neumüller, R.A. & Knoblich, J.A. (2009). Dividing cellular asymmetry: Asymmetric cell division and its implications for stem cells and cancer. Genes Dev 23, 2675–2699.CrossRefGoogle ScholarPubMed
Nigg, E.A. (2007). Centrosome duplication: Of rules and licenses. Trends Cell Biol 17(5), 215–221.CrossRefGoogle ScholarPubMed
Oliferenko, S., Chew, T.G. & Balasubramanian, M.K. (2009). Positioning cytokinesis. Genes Dev 23, 660–674.CrossRefGoogle ScholarPubMed
Pan, J. & Snell, W. (2007). The primary cilium: Keeper of the key to cell division. Cell 129, 1255–1257.CrossRefGoogle ScholarPubMed
Pebay, A., Wong, R.C., Pitson, S.M., Wolvetang, E.J., Peh, G.S., Filipczyk, A., Koh, K.L., Tellis, I., Nguyen, L.T. & Pera, M.F. (2005). Essential roles of sphingosine-1-phosphate and platelet-derived growth factor in the maintenance of human embryonic stem cells. Stem Cells 23, 1541–1548.CrossRefGoogle ScholarPubMed
Pedersen, L.B., Veland, I.R., Schroder, J.M. & Christensen, S.T. (2008). Assembly of primary cilia. Dev Dynam 237, 1993–2006.CrossRefGoogle ScholarPubMed
Quarmby, L.M. & Parker, J.D.K. (2005). Cilia and the cell cycle? J Cell Biol 169(5), 707–710.CrossRefGoogle ScholarPubMed
Rebollo, E., Sampaio, P., Januschke, J., Llamarazes, S., Varmark, H. & Gonzalez, C. (2007). Functionally unequal centrosomes drive spindle orientation in asymmetrically dividing Drosophila neural stem cells. Dev Cell 12, 467–474.CrossRefGoogle ScholarPubMed
Rusan, N.M. & Peifer, M. (2007). A role for a novel centrosome cycle in asymmetric cell division. J Cell Biol 177, 13–20.CrossRefGoogle ScholarPubMed
Santos, N. & Reiter, J.F. (2008). Building it up and taking it down: The regulation of vertebrate ciliogenesis. Dev Dynam 237, 1972–1981.CrossRefGoogle ScholarPubMed
Satir, P. & Christensen, S.T. (2007). Overview of structure and function of mammalian cilia. Annu Rev Physiol 69, 377–400.CrossRefGoogle ScholarPubMed
Satir, P. & Christensen, S.T. (2008). Structure and function of mammalian cilia. Histochem Cell Biol 129, 687–693.CrossRefGoogle ScholarPubMed
Sato, N., Meijer, L., Skaltsounis, L., Greengard, P. & Brivanlou, A.H. (2004). Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10, 55–63.CrossRefGoogle ScholarPubMed
Schatten, H. (2008). The mammalian centrosome and its functional significance. Histochem Cell Biol 129, 667–686.CrossRefGoogle ScholarPubMed
Schatten, H. & Sun, Q-Y. (2009a). The role of centrosomes in mammalian fertilization and its significance for ICSI. Mol Hum Reprod 15(9), 531–538.CrossRefGoogle ScholarPubMed
Schatten, H. & Sun, Q-Y. (2009b). The functional significance of centrosomes in mammalian meiosis, fertilization, development, nuclear transfer, and stem cell differentiation. Environ Mol Mutagen 50(8), 620–636.CrossRefGoogle ScholarPubMed
Schatten, H. & Sun, Q-Y. (2010). The role of centrosomes in fertilization, cell division and establishment of asymmetry during embryo development. Sem Cell Dev Biol 21, 174–184.CrossRefGoogle ScholarPubMed
Schneider, L., Clement, C.A., Teilmann, S.C., Pazour, G.J., Hoffmann, E.K., Satir, P. & Christensen, S.T. (2005). PDGFR signaling is regulated through the primary cilium in fibroblasts. Curr Biol 15, 1861–1866.CrossRefGoogle ScholarPubMed
Sorokin, S. (1962). Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J Cell Biol 15, 363–377.CrossRefGoogle ScholarPubMed
Tsou, M.B. & Stearns, T. (2006a). Mechanism limiting centrosome duplication to once per cell cycle. Nature 442, 947–951.CrossRefGoogle ScholarPubMed
Tsou, M.B. & Stearns, T. (2006b). Controlling centrosome number: Licenses and blocks. Curr Opin Cell Biol 18, 74–78.CrossRefGoogle ScholarPubMed
Tucker, R.W., Pardee, A.B. & Fujiwara, K. (1979). Centriole ciliation is related to quiescence and DNA synthesis in 3T3 cells. Cell 17, 527–535.CrossRefGoogle ScholarPubMed
Van Beneden, E. (1875–1876). Recherches sur les Dicyémides, survivant actuels d'un embranchement des Mesozoaires. Bull Acad R Med Belg 2me sr 41, 1160–1205and 42, 35–97.Google Scholar
Van Beneden, E. (1883). Recherches sur la maturation de l'oeuf, la fecundation et la division cellulaire. Arch Biol 4, 265–640.Google Scholar
Van Beneden, E. & Neyt, A. (1887). Nouvelles recherches sur la fecondation et la division mitosique chez l'Ascaride megalocephale. Bull Acad R Med Belg 3me sr 14, 215–295.Google Scholar
Veland, I.R., Awan, A., Pedersen, L.B., Yoder, B.K. & Christensen, S.T. (2009). Primary cilia and signaling pathways in mammalian development, health and disease. Nephron Physiol 111, 39–53.CrossRefGoogle ScholarPubMed
Wheatley, D.N., Wang, A.M. & Strugnell, G.E. (1996). Expression of primary cilia in mammalian cells. Cell Biol Int 20, 73–81.CrossRefGoogle ScholarPubMed
Whitfield, J.F. (2008). The solitary (primary) cilium—A mechanosensory toggle switch in bone and cartilage cells. Cell Signal 20, 1019–1024.CrossRefGoogle ScholarPubMed
Yamashita, Y.M., Mahold, A.P., Perlin, J.R. & Fuller, M.T. (2007). Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315, 518–521.CrossRefGoogle ScholarPubMed
Yamashita, Y.M., Yuan, H., Cheng, J. & Hunt, A. (2010). Polarity in stem cell division: Asymmetric stem cell division in tissue homeostasis. Cold Spring Harb Perspect Biol 2, a001313.CrossRefGoogle ScholarPubMed