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Endothelial Cell-Pericyte Interactions Stimulate Basement Membrane Matrix Assembly: Influence on Vascular Tube Remodeling, Maturation, and Stabilization

Published online by Cambridge University Press:  14 December 2011

Amber N. Stratman
Affiliation:
Department of Medical Pharmacology and Physiology, School of Medicine, Dalton Cardiovascular Research Center, University of Missouri-Columbia, Columbia, MO 65212, USA
George E. Davis*
Affiliation:
Department of Medical Pharmacology and Physiology, School of Medicine, Dalton Cardiovascular Research Center, University of Missouri-Columbia, Columbia, MO 65212, USA Department of Pathology and Anatomical Sciences, School of Medicine, Dalton Cardiovascular Research Center, University of Missouri-Columbia, Columbia, MO 65212, USA
*
Corresponding author. E-mail: davisgeo@health.missouri.edu
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Abstract

Extracellular matrix synthesis and deposition surrounding the developing vasculature are critical for vessel remodeling and maturation events. Although the basement membrane is an integral structure underlying endothelial cells (ECs), few studies, until recently, have been performed to understand its formation in this context. In this review article, we highlight new data demonstrating a corequirement for ECs and pericytes to properly deposit and assemble vascular basement membranes during morphogenic events. In EC only cultures or under conditions whereby pericyte recruitment is blocked, there is a lack of basement membrane assembly, decreased vessel stability (with increased susceptibility to pro-regressive stimuli), and increased EC tube widths (a marker of dysfunctional EC-pericyte interactions). ECs and pericytes both contribute basement membrane components and, furthermore, both cells induce the expression of particular components as well as integrins that recognize them. The EC-derived factors—platelet derived growth factor-BB and heparin binding-epidermal growth factor—are both critical for pericyte recruitment to EC tubes and concomitant vascular basement membrane formation in vitro and in vivo. Thus, heterotypic EC-pericyte interactions play a fundamental role in vascular basement membrane matrix deposition, a critical tube maturation event that is altered in key disease states such as diabetes and cancer.

Type
Review Article
Copyright
Copyright © Microscopy Society of America 2012

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References

REFERENCES

Abramsson, A., Lindblom, P. & Betsholtz, C. (2003). Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors. J Clin Invest 112(8), 11421151.CrossRefGoogle ScholarPubMed
Adams, R.H. & Alitalo, K. (2007). Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8(6), 464478.CrossRefGoogle ScholarPubMed
Arroyo, A.G. & Iruela-Arispe, M.L. (2010). Extracellular matrix, inflammation, and the angiogenic response. Cardiovasc Res 86(2), 226235.CrossRefGoogle ScholarPubMed
Astrof, S., Crowley, D. & Hynes, R.O. (2007). Multiple cardiovascular defects caused by the absence of alternatively spliced segments of fibronectin. Dev Biol 311(1), 1124.CrossRefGoogle ScholarPubMed
Astrof, S. & Hynes, R.O. (2009). Fibronectins in vascular morphogenesis. Angiogenesis 12(2), 165175.CrossRefGoogle ScholarPubMed
Baluk, P., Hashizume, H. & McDonald, D.M. (2005). Cellular abnormalities of blood vessels as targets in cancer. Curr Opin Genet Dev 15(1), 102111.CrossRefGoogle ScholarPubMed
Baluk, P., Morikawa, S., Haskell, A., Mancuso, M. & McDonald, D.M. (2003). Abnormalities of basement membrane on blood vessels and endothelial sprouts in tumors. Am J Pathol 163(5), 18011815.CrossRefGoogle ScholarPubMed
Bayless, K.J. & Davis, G.E. (2002). The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J Cell Sci 115(Pt 6), 11231136.CrossRefGoogle ScholarPubMed
Bayless, K.J., Salazar, R. & Davis, G.E. (2000). RGD-dependent vacuolation and lumen formation observed during endothelial cell morphogenesis in three-dimensional fibrin matrices involves the alpha(v)beta(3) and alpha(5)beta(1) integrins. Am J Pathol 156(5), 16731683.CrossRefGoogle Scholar
Bell, S.E., Mavila, A., Salazar, R., Bayless, K.J., Kanagala, S., Maxwell, S.A. & Davis, G.E. (2001). Differential gene expression during capillary morphogenesis in 3D collagen matrices: Regulated expression of genes involved in basement membrane matrix assembly, cell cycle progression, cellular differentiation and G-protein signaling. J Cell Sci 114(Pt 15), 27552773.CrossRefGoogle ScholarPubMed
Benjamin, L.E., Golijanin, D., Itin, A., Pode, D. & Keshet, E. (1999). Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J Clin Invest 103(2), 159165.CrossRefGoogle ScholarPubMed
Benjamin, L.E., Hemo, I. & Keshet, E. (1998). A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 125(9), 15911598.CrossRefGoogle ScholarPubMed
Bergers, G. & Song, S. (2005). The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 7(4), 452464.CrossRefGoogle ScholarPubMed
Bergers, G., Song, S., Meyer-Morse, N., Bergsland, E. & Hanahan, D. (2003). Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Invest 111(9), 12871295.CrossRefGoogle ScholarPubMed
Betsholtz, C., Lindblom, P. & Gerhardt, H. (2005). Role of pericytes in vascular morphogenesis. EXS 2005(94), 115125.Google Scholar
Bjarnegard, M., Enge, M., Norlin, J., Gustafsdottir, S., Fredriksson, S., Abramsson, A., Takemoto, M., Gustafsson, E., Fassler, R. & Betsholtz, C. (2004). Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 131(8), 18471857.CrossRefGoogle ScholarPubMed
Carmeliet, P. (2005). Angiogenesis in life, disease and medicine. Nature 438(7070), 932936.CrossRefGoogle ScholarPubMed
Cheng, Y.S., Champliaud, M.F., Burgeson, R.E., Marinkovich, M.P. & Yurchenco, P.D. (1997). Self-assembly of laminin isoforms. J Biol Chem 272(50), 3152531532.CrossRefGoogle ScholarPubMed
Chun, T.H., Sabeh, F., Ota, I., Murphy, H., McDonagh, K.T., Holmbeck, K., Birkedal-Hansen, H., Allen, E.D. & Weiss, S.J. (2004). MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. J Cell Biol 167(4), 757767.CrossRefGoogle ScholarPubMed
Clark, R.A., DellaPelle, P., Manseau, E., Lanigan, J.M., Dvorak, H.F. & Colvin, R.B. (1982). Blood vessel fibronectin increases in conjunction with endothelial cell proliferation and capillary ingrowth during wound healing. J Invest Dermatol 79(5), 269276.CrossRefGoogle ScholarPubMed
Davis, G.E. & Camarillo, C.W. (1996). An alpha 2 beta 1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp Cell Res 224(1), 3951.CrossRefGoogle ScholarPubMed
Davis, G.E., Koh, W. & Stratman, A.N. (2007). Mechanisms controlling human endothelial lumen formation and tube assembly in three-dimensional extracellular matrices. Birth Defects Res C Embryo Today 81(4), 270285.CrossRefGoogle ScholarPubMed
Davis, G.E. & Senger, D.R. (2005). Endothelial extracellular matrix: Biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res 97(11), 10931107.CrossRefGoogle ScholarPubMed
Davis, G.E. & Senger, D.R. (2008). Extracellular matrix mediates a molecular balance between vascular morphogenesis and regression. Curr Opin Hematol 15(3), 197203.CrossRefGoogle ScholarPubMed
Davis, G.E., Stratman, A.N., Sacharidou, A. & Koh, W. (2011). Molecular basis for endothelial lumen formation and tubulogenesis during vasculogenesis and angiogenic sprouting. Int Rev Cell Mol Biol 288, 101165.CrossRefGoogle ScholarPubMed
Drake, C.J. (2003). Embryonic and adult vasculogenesis. Birth Defects Res C Embryo Today 69(1), 7382.CrossRefGoogle ScholarPubMed
Francis, S.E., Goh, K.L., Hodivala-Dilke, K., Bader, B.L., Stark, M., Davidson, D. & Hynes, R.O. (2002). Central roles of alpha5beta1 integrin and fibronectin in vascular development in mouse embryos and embryoid bodies. Arterioscler Thromb Vasc Biol 22(6), 927933.CrossRefGoogle ScholarPubMed
Gaengel, K., Genove, G., Armulik, A. & Betsholtz, C. (2009). Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 29(5), 630638.CrossRefGoogle ScholarPubMed
George, E.L., Baldwin, H.S. & Hynes, R.O. (1997). Fibronectins are essential for heart and blood vessel morphogenesis but are dispensable for initial specification of precursor cells. Blood 90(8), 30733081.CrossRefGoogle ScholarPubMed
Hammes, H.P. (2005). Pericytes and the pathogenesis of diabetic retinopathy. Horm Metab Res 37(S1), 3943.CrossRefGoogle ScholarPubMed
Hammes, H.P., Lin, J., Renner, O., Shani, M., Lundqvist, A., Betsholtz, C., Brownlee, M. & Deutsch, U. (2002). Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 51(10), 31073112.CrossRefGoogle ScholarPubMed
Hammes, H.P., Lin, J., Wagner, P., Feng, Y., Vom Hagen, F., Krzizok, T., Renner, O., Breier, G., Brownlee, M. & Deutsch, U. (2004). Angiopoietin-2 causes pericyte dropout in the normal retina: Evidence for involvement in diabetic retinopathy. Diabetes 53(4), 11041110.CrossRefGoogle ScholarPubMed
Hanahan, D. (1997). Signaling vascular morphogenesis and maintenance. Science 277(5322), 4850.CrossRefGoogle ScholarPubMed
Handler, M., Yurchenco, P.D. & Iozzo, R.V. (1997). Developmental expression of perlecan during murine embryogenesis. Dev Dyn 210(2), 130145.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Hellstrom, M., Gerhardt, H., Kalen, M., Li, X., Eriksson, U., Wolburg, H. & Betsholtz, C. (2001). Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153(3), 543553.CrossRefGoogle ScholarPubMed
Hirschi, K.K., Rohovsky, S.A. & D'Amore, P.A. (1998). PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol 141(3), 805814.CrossRefGoogle ScholarPubMed
Ho, M.S., Bose, K., Mokkapati, S., Nischt, R. & Smyth, N. (2008). Nidogens-extracellular matrix linker molecules. Microsc Res Tech 71(5), 387395.CrossRefGoogle ScholarPubMed
Hughes, C.C. (2008). Endothelial-stromal interactions in angiogenesis. Curr Opin Hematol 15(3), 204209.CrossRefGoogle ScholarPubMed
Hynes, R.O. (2007). Cell-matrix adhesion in vascular development. J Thromb Haemost 5(S1), 3240.CrossRefGoogle ScholarPubMed
Hynes, R.O. (2009). The extracellular matrix: Not just pretty fibrils. Science 326(5957), 12161219.CrossRefGoogle ScholarPubMed
Iivanainen, E., Lauttia, S., Zhang, N., Tvorogov, D., Kulmala, J., Grenman, R., Salven, P. & Elenius, K. (2009). The EGFR inhibitor gefitinib suppresses recruitment of pericytes and bone marrow-derived perivascular cells into tumor vessels. Microvasc Res 78(3), 278285.CrossRefGoogle ScholarPubMed
Iivanainen, E., Nelimarkka, L., Elenius, V., Heikkinen, S.M., Junttila, T.T., Sihombing, L., Sundvall, M., Maatta, J.A., Laine, V.J., Yla-Herttuala, S., Higashiyama, S., Alitalo, K. & Elenius, K. (2003). Angiopoietin-regulated recruitment of vascular smooth muscle cells by endothelial-derived heparin binding EGF-like growth factor. FASEB J 17(12), 16091621.CrossRefGoogle ScholarPubMed
Iruela-Arispe, M.L. & Davis, G.E. (2009). Cellular and molecular mechanisms of vascular lumen formation. Dev Cell 16(2), 222231.CrossRefGoogle ScholarPubMed
Jain, R.K. (2003). Molecular regulation of vessel maturation. Nat Med 9(6), 685693.CrossRefGoogle ScholarPubMed
Koh, W., Mahan, R.D. & Davis, G.E. (2008a). Cdc42- and Rac1-mediated endothelial lumen formation requires Pak2, Pak4 and Par3, and PKC-dependent signaling. J Cell Sci 121(Pt 7), 9891001.CrossRefGoogle ScholarPubMed
Koh, W., Sachidanandam, K., Stratman, A.N., Sacharidou, A., Mayo, A.M., Murphy, E.A., Cheresh, D.A. & Davis, G.E. (2009). Formation of endothelial lumens requires a coordinated PKC{epsilon}-, Src-, Pak- and Raf-kinase-dependent signaling cascade downstream of Cdc42 activation. J Cell Sci 122(Pt 11), 18121822.CrossRefGoogle ScholarPubMed
Koh, W., Stratman, A.N., Sacharidou, A. & Davis, G.E. (2008b). In vitro three dimensional collagen matrix models of endothelial lumen formation during vasculogenesis and angiogenesis. Methods Enzymol 443, 83101.CrossRefGoogle ScholarPubMed
Lafleur, M.A., Handsley, M.M., Knauper, V., Murphy, G. & Edwards, D.R. (2002). Endothelial tubulogenesis within fibrin gels specifically requires the activity of membrane-type-matrix metalloproteinases (MT-MMPs). J Cell Sci 115(Pt 17), 34273438.CrossRefGoogle ScholarPubMed
Leveen, P., Pekny, M., Gebre-Medhin, S., Swolin, B., Larsson, E. & Betsholtz, C. (1994). Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev 8(16), 18751887.CrossRefGoogle ScholarPubMed
Li, S., Harrison, D., Carbonetto, S., Fassler, R., Smyth, N., Edgar, D. & Yurchenco, P.D. (2002). Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. J Cell Biol 157(7), 12791290.CrossRefGoogle ScholarPubMed
Lilly, B. & Kennard, S. (2009). Differential gene expression in a coculture model of angiogenesis reveals modulation of select pathways and a role for Notch signaling. Physiol Genomics 36(2), 6978.CrossRefGoogle Scholar
Lindahl, P., Johansson, B.R., Leveen, P. & Betsholtz, C. (1997). Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277(5323), 242245.CrossRefGoogle ScholarPubMed
Lindblom, P., Gerhardt, H., Liebner, S., Abramsson, A., Enge, M., Hellstrom, M., Backstrom, G., Fredriksson, S., Landegren, U., Nystrom, H.C., Bergstrom, G., Dejana, E., Ostman, A., Lindahl, P. & Betsholtz, C. (2003). Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev 17(15), 18351840.CrossRefGoogle ScholarPubMed
Miner, J.H., Cunningham, J. & Sanes, J.R. (1998). Roles for laminin in embryogenesis: Exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J Cell Biol 143(6), 17131723.CrossRefGoogle ScholarPubMed
Miner, J.H. & Yurchenco, P.D. (2004). Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 20, 255284.CrossRefGoogle ScholarPubMed
Morikawa, S., Baluk, P., Kaidoh, T., Haskell, A., Jain, R.K. & McDonald, D.M. (2002). Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 160(3), 9851000.CrossRefGoogle ScholarPubMed
Paulsson, M. (1992). Basement membrane proteins: Structure, assembly, and cellular interactions. Crit Rev Biochem Mol Biol 27(1-2), 93127.Google ScholarPubMed
Poschl, E., Schlotzer-Schrehardt, U., Brachvogel, B., Saito, K., Ninomiya, Y. & Mayer, U. (2004). Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131(7), 16191628.CrossRefGoogle ScholarPubMed
Risau, W. & Flamme, I. (1995). Vasculogenesis. Annu Rev Cell Dev Biol 11, 7391.CrossRefGoogle ScholarPubMed
Risau, W. & Lemmon, V. (1988). Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev Biol 125(2), 441450.CrossRefGoogle ScholarPubMed
Sacharidou, A., Koh, W., Stratman, A.N., Mayo, A.M., Fisher, K.E. & Davis, G.E. (2010). Endothelial lumen signaling complexes control 3D matrix-specific tubulogenesis through interdependent Cdc42- and MT1-MMP-mediated events. Blood 115(25), 52595269.CrossRefGoogle ScholarPubMed
Sacharidou, A., Stratman, A.N. & Davis, G.E. (2012). Molecular mechanisms controlling vascular lumen formation in three-dimensional extracellular matrices. Cell Tissues Organs 195, 122143.CrossRefGoogle ScholarPubMed
Saunders, W.B., Bayless, K.J. & Davis, G.E. (2005). MMP-1 activation by serine proteases and MMP-10 induces human capillary tubular network collapse and regression in 3D collagen matrices. J Cell Sci 118(Pt 10), 23252340.CrossRefGoogle ScholarPubMed
Saunders, W.B., Bohnsack, B.L., Faske, J.B., Anthis, N.J., Bayless, K.J., Hirschi, K.K. & Davis, G.E. (2006). Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J Cell Biol 175(1), 179191.CrossRefGoogle ScholarPubMed
Scheele, S., Nystrom, A., Durbeej, M., Talts, J.F., Ekblom, M. & Ekblom, P. (2007). Laminin isoforms in development and disease. J Mol Med (Berl) 85(8), 825836.CrossRefGoogle ScholarPubMed
Schmidt, C., Pollner, R., Poschl, E. & Kuhn, K. (1992). Expression of human collagen type IV genes is regulated by transcriptional and post-transcriptional mechanisms. FEBS Lett 312(2-3), 174178.CrossRefGoogle Scholar
Senger, D.R. & Davis, G.E. (2011). Angiogenesis. Cold Spring Harb Perspect Biol 3(8), a005090.CrossRefGoogle ScholarPubMed
Sennino, B., Falcon, B.L., McCauley, D., Le, T., McCauley, T., Kurz, J.C., Haskell, A., Epstein, D.M. & McDonald, D.M. (2007). Sequential loss of tumor vessel pericytes and endothelial cells after inhibition of platelet-derived growth factor B by selective aptamer AX102. Cancer Res 67(15), 73587367.CrossRefGoogle ScholarPubMed
Seo, D.W., Li, H., Guedez, L., Wingfield, P.T., Diaz, T., Salloum, R., Wei, B.Y. & Stetler-Stevenson, W.G. (2003). TIMP-2 mediated inhibition of angiogenesis: An MMP-independent mechanism. Cell 114(2), 171180.CrossRefGoogle ScholarPubMed
Smola, H., Stark, H.J., Thiekotter, G., Mirancea, N., Krieg, T. & Fusenig, N.E. (1998). Dynamics of basement membrane formation by keratinocyte-fibroblast interactions in organotypic skin culture. Exp Cell Res 239(2), 399410.CrossRefGoogle ScholarPubMed
Somanath, P.R., Ciocea, A. & Byzova, T.V. (2009). Integrin and growth factor receptor alliance in angiogenesis. Cell Biochem Biophys 53(2), 5364.CrossRefGoogle ScholarPubMed
Stetler-Stevenson, W.G. & Seo, D.W. (2005). TIMP-2: An endogenous inhibitor of angiogenesis. Trends Mol Med 11(3), 97103.CrossRefGoogle ScholarPubMed
Stratman, A.N., Davis, M.J. & Davis, G.E. (2011). VEGF and FGF prime vascular tube morphogenesis and sprouting directed by hematopoietic stem cell cytokines. Blood 117(14), 37093719.CrossRefGoogle ScholarPubMed
Stratman, A.N., Malotte, K.M., Mahan, R.D., Davis, M.J. & Davis, G.E. (2009a). Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 114(24), 50915101.CrossRefGoogle ScholarPubMed
Stratman, A.N., Saunders, W.B., Sacharidou, A., Koh, W., Fisher, K.E., Zawieja, D.C., Davis, M.J. & Davis, G.E. (2009b). Endothelial cell lumen and vascular guidance tunnel formation requires MT1-MMP-dependent proteolysis in 3-dimensional collagen matrices. Blood 114(2), 237247.CrossRefGoogle ScholarPubMed
Stratman, A.N., Schwindt, A.E., Malotte, K.M. & Davis, G.E. (2010). Endothelial-derived PDGF-BB and HB-EGF coordinately regulate pericyte recruitment during vasculogenic tube assembly and stabilization. Blood 116(22), 47204730.CrossRefGoogle ScholarPubMed
Stupack, D.G. & Cheresh, D.A. (2004). Integrins and angiogenesis. Curr Top Dev Biol 64, 207238.CrossRefGoogle ScholarPubMed
Thyboll, J., Kortesmaa, J., Cao, R., Soininen, R., Wang, L., Iivanainen, A., Sorokin, L., Risling, M., Cao, Y. & Tryggvason, K. (2002). Deletion of the laminin alpha4 chain leads to impaired microvessel maturation. Mol Cell Biol 22(4), 11941202.CrossRefGoogle ScholarPubMed
Timpl, R. (1994). Proteoglycans of basement membranes. EXS 70, 123144.Google ScholarPubMed
Timpl, R., Dziadek, M., Fujiwara, S., Nowack, H. & Wick, G. (1983). Nidogen: A new, self-aggregating basement membrane protein. Eur J Biochem 137(3), 455465.CrossRefGoogle ScholarPubMed
Timpl, R., Fujiwara, S., Dziadek, M., Aumailley, M., Weber, S. & Engel, J. (1984). Laminin, proteoglycan, nidogen and collagen IV: Structural models and molecular interactions. Ciba Found Symp 108, 2543.Google ScholarPubMed
Vogel, V. (2006). Mechanotransduction involving multimodular proteins: Converting force into biochemical signals. Annu Rev Biophys Biomol Struct 35, 459488.CrossRefGoogle ScholarPubMed
Wagenseil, J.E. & Mecham, R.P. (2009). Vascular extracellular matrix and arterial mechanics. Physiol Rev 89(3), 957989.CrossRefGoogle ScholarPubMed
Weskamp, G., Mendelson, K., Swendeman, S., Le Gall, S., Ma, Y., Lyman, S., Hinoki, A., Eguchi, S., Guaiquil, V., Horiuchi, K. & Blobel, C.P. (2010). Pathological neovascularization is reduced by inactivation of ADAM17 in endothelial cells but not in pericytes. Circ Res 106(5), 932940.CrossRefGoogle ScholarPubMed
Yurchenco, P.D., Amenta, P.S. & Patton, B.L. (2004). Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol 22(7), 521538.CrossRefGoogle ScholarPubMed
Yurchenco, P.D. & Patton, B.L. (2009). Developmental and pathogenic mechanisms of basement membrane assembly. Curr Pharm Des 15(12), 12771294.CrossRefGoogle ScholarPubMed
Zhong, C., Chrzanowska-Wodnicka, M., Brown, J., Shaub, A., Belkin, A.M. & Burridge, K. (1998). Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J Cell Biol 141(2), 539551.CrossRefGoogle ScholarPubMed