Adhesion and migration of avian neural crest cells on fibronectin require the cooperating activities of multiple integrins of the β1 and β3 families

Journal of Cell Science

Volumn 112, Issue 24, 1999, Pages 4715-4728

  Testaz, Sandrine ^a   Delannet, Muriel ^a   Duband, Jean Loup ^a  

^a Université René Descartes   (France)

Author keywords

Avian embryo; Cell adhesion; Cell migration; Fibronectin; Integrin; Neural crest

Indexed keywords

BETA1 INTEGRIN; BETA3 INTEGRIN; CD31 ANTIGEN; FIBRONECTIN; FIBRONECTIN RECEPTOR; INTEGRIN; INTEGRIN RECEPTOR; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ARTICLE; BIRD; CELL ADHESION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURFACE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; IMMUNOPRECIPITATION; MICROFILAMENT; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, CD31; CELL ADHESION; CELL MOVEMENT; FIBRONECTINS; INTEGRINS; NEURAL CREST; QUAIL; RECOMBINANT PROTEINS; VASCULAR CELL ADHESION MOLECULE-1;

EID: 0033373786     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (109)

1. Adams, J. C. and Watt, F. M. (1990). Changes in keratinocyte adhesion during terminal differentiation: Reduction in fibronectin binding precedes α5β1 integrin loss from the cell surface. Cell 63, 425-435.
2. Akiyama, S. K., Yamada, S. S., Chen, W.-T. and Yamada, K. M. (1989). Analysis of fibronectin receptor function with monoclonal antibodies: Roles in cell adhesion, migration, matrix assembly, and cytoskeletal organization. J. Cell Biol. 109, 863-875.
3. Akiyama, S. K., Yamada, S. S. and Yamada, K. M. (1986). Characterization of a 140-kD avian cell surface antigen as a fibronectin-binding molecule. J. Cell Biol. 102, 442-448.
4. Albelda, S. M., Mette, S. A., Elder, D. E., Stewardt, R., Damjanovich, L., Herlyn, M. and Buck, C. A. (1990). Integrin distribution in malignant melanoma: Association of the β3 subunit with tumor progression. Cancer Res. 50, 6757-6764.
5. Altevogt, P., Hubbe, M., Ruppert, M., Lohr, J., von Hoegen, P., Sammar, M., Andrew, D. P., McEvoy, L., Humphries, M. J. and Butcher, E. C. (1995). The α4 integrin chain is a ligand for α4β7 and α4β1. J. Exp. Med. 182, 345-355.
6. Bader, B. L., Rayburn, H., Crowley, D. and Hynes, R. O. (1998). Extensive vasculogenesis, angiogenesis, and organogenesis precede lethality in mice lacking all αv integrins. Cell 95, 507-519.
7. Beauvais, A., Erickson, C. A., Goins, T., Craig, S. E., Humphries, M. J., Thiery, J. P. and Dufour, S. (1995). Changes in the fibronectin-specific integrin expression pattern modify the migratory behavior of sarcoma S180 cells in vitro and in the embryonic environment. J. Cell Biol. 128, 699-713.
8. Beauvais-Jouneau, A., Delouvée, A., Craig, S. E., Humphries, M. J., Thiery, J. P. and Dufour, S. (1997). Direct role of the carboxy-terminal cell-binding domain of fibronectin in neural crest cell motility. Exp. Cell Res. 233, 1-10.
9. Boettiger, D., Enomoto-Iwamoto, M., Yoon, E. Y., Hofer, U., Menko, A. S. and Chiquet-Ehrismann, R. (1995). Regulation of integrin α5β1 affinity during myogenic differentiation. Dev. Biol. 169, 261-272.
10. Bossy, B., Bossy-Wetzel, E. and Reichardt, L. F. (1991). Characterization of the integrin α8 subunit: A new integrin β1-associated subunit, which is prominently expressed on axons and on cells in contact with basal laminae in chick embryos. EMBO J. 10, 2375-2385.
11. Bossy, B. and Reichardt, L. F. (1990). Chick integrin αV subunit molecular analysis reveals high conservation of structural domains and association with multiple β subunits in embryo fibroblasts. Biochemistry 29, 10191-10198.
12. Boucaut, J.-C., Darribère, T., Poole, T. J., Aoyama, H., Yamada, K. M. and Thiery, J. P. (1984). Biological active synthetic peptides as probes of embryonic development: A competitive peptide inhibitor of fibronectin function inhibits gastrulation in amphibian embryos and neural crest cell migration in avian embryos. J. Cell Biol. 99, 1822-1830.
13. Breuss, J. M., Gallo, J., DeLisser, H. M., Klimanskaya, I. V., Folkesson, H. G., Pittet, J. F., Nishimura, S. L., Aldape, K., Landers, D. V., Carpenter, W., Gillett, N., Sheppard, D., Matthay, M. A., Albelda, S. M., Kramer, R. H. and Pytela, R. (1995). Expression of the β6 integrin subunit in development, neoplasia and tissue repair suggests a role in epithelial remodeling. J. Cell Sci. 108, 2241-2251.
14. Bronner-Fraser, M. (1986). An antibody to a receptor for fibronectin and laminin perturbs cranial neural crest development in vivo. Dev. Biol. 117, 528-536.
15. Bronner-Fraser, M. (1993). Neural crest cell migration in the developing embryo. Trends Cell Biol. 3, 392-397.
16. Bronner-Fraser, M. (1994). Neural crest cell formation and migration in the developing embryo. FASEB J. 8, 699-706.
17. Bronner-Fraser, M. (1995). Origins and developmental potential of the neural crest. Exp. Cell Res. 218, 405-417.
18. Bronner-Fraser, M., Artinger, M., Muschler, J. and Horwitz, A. F. (1992). Developmentally regulated expression of α6 integrin in avian embryos. Development 115, 197-211.
19. Bronner-Fraser, M. and Lallier, T. (1988). A monoclonal antibody against a laminin-heparan sulfate proteoglycan complex perturbs cranial neural crest migration in vivo. J. Cell Biol. 106, 1321-1329.
20. Brooks, P. C., Clark, R. A. F. and Cheresh, D. A. (1994). Requirement of vascular integrin αvβ3 for angiogenesis. Science 264, 569-571.
21. Camper, L., Hellman, U. and Lundgren-Akerlund, E. (1998). Isolation, cloning, and sequence analysis of the integrin subunit α10, a β1-associated collagen binding integrin expressed on chondrocytes. J. Biol. Chem. 273, 20383-20389.
22. Chan, B. M. C., Kassner, P. D., Schiro, J. A., Byers, H. R., Kupper, T. S. and Hemler, M. E. (1992). Distinct cellular functions mediated by different VLA integrin α subunit cytoplasmic domains. Cell 68, 1051-1060.
23. Chan, P.-Y. and Aruffo, A. (1993). VLA-4 integrin mediates lymphocyte migration on the inducible endothelial cell ligand VCAM-1 and the extracellular matrix ligand fibronectin. J. Biol. Chem. 268, 24655-24664.
24. Chen, W.-T., Hasegawa, E., Hasegawa, T., Weinstock, C. and Yamada, K. M. (1985). Development of cell surface linkage complexes in cultured fibroblasts. J. Cell Biol. 100, 1103-1114.
25. Cheresh, D. A. and Spiro, R. C. (1987). Biosynthetic and functional properties of an Arg-Gly-Asp-directed receptor involved in human melenoma cell attachment to vitronectin, fibrinogen and von Willebrand factor. J. Biol. Chem. 262, 17703-17711.
26. Clyman, R. I., Mauray, F. and Kramer, R. H. (1992). β1 and β3 integrins have different roles in the adhesion and migration of vascular smooth muscle cells on extracellular matrix. Exp. Cell Res. 200, 272-284.
27. Delannet, M. and Duband, J.-L. (1992). Transforming growth factor-β control of cell-substratum adhesion during avian neural crest cell emigration in vitro. Development 116, 275-287.
28. Delannet, M., Martin, F., Bossy, B., Cheresh, D. A., Reichardt, L. F. and Duband, J.-L. (1994). Specific roles of the αVβ1, αVβ3 and αVβ5 integrins in avian neural crest cell adhesion and migration on vitronectin. Development 120, 2687-2702.
29. Desban, N. and Duband, J.-L. (1997). Avian neural crest cell migration on laminin: Interaction of the α1β1 integrin with distinct laminin-1 domains mediates different adhesive responses. J. Cell Sci. 110, 2729-2744.
30. Duband, J.-L., Belkin, A. M., Syfrig, J., Thiery, J. P. and Koteliansky, V. E. (1992). Expression of α1 integrin, a laminin-collagen receptor, during myogenesis and neurogenesis in the avian embryo. Development 116, 585-600.
31. Duband, J.-L., Delannet, M. and Monier-F. (1995a). Neural crest cells: Strategies to generate lineage diversification in vitro. In Neural Cell Culture: A Practical Approach (ed. J. Cohen and C. P. Wilkin), pp. 133-152. Oxford: Oxford University Press.
32. Duband, J.-L., Dufour, S., Yamada, S. S., Yamada, K. M. and Thiery, J. P. (1991). Neural crest cell locomotion induced by antibodies to β1 integrins: A tool for studying the roles of substratum molecular avidity and density in migration. J. Cell Sci. 98, 517-532.
33. Duband, J.-L., Monier, F., Delannet, M. and Newgreen, D. F. (1995b). Epithelium-mesenchyme transition during neural crest development. Acta Anat. 154, 63-78.
34. Duband, J.-L., Nuckolls, G. H., Ishihara, A., Hasegawa, T., Yamada, K. M., Thiery, J. P. and Jacobson, K. ( 1988). The fibronectin receptor exhibits high lateral mobility in embryonic locomoting cells but is immobile in focal contacts and fibrillar streaks in stationary cells. J. Cell Biol. 107, 1385-1396.
35. Duband, J.-L., Rocher, S., Chen, W.-T., Yamada, K. M. and Thiery, J. P. (1986). Cell adhesion and migration in the early vertebrate embryo: Location and possible role of the putative fibronectin-receptor complex. J. Cell Biol. 102, 160-178.
36. Dufour, S., Duband, J.-L., Humphries, M. J., Obara, M., Yamada, K. M. and Thiery, J. P. (1988). Attachment, spreading, and locomotion of avian neural crest cells are mediated by multiple adhesion sites on fibronectin molecules. EMBO J. 7, 2661-2671.
37. Elices, M. J., Osborn, L., Takada, Y., Crouse, C., Luhowsky, S., Hemler, M. E. and Lobb, R. R. (1990). VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell 60, 577-584.
38. Erickson, C. A. and Perris, R. (1993). The role of cell-cell and cell-matrix interactions in the morphogenesis of the neural crest. Dev. Biol. 159, 60-74.
39. Fässler, R. and Meyer, M. (1995). Consequences of lack of β1 integrin gene expression in mice. Genes Dev. 9, 1896-1908.
40. Fogerty, F. J., Akiyama, S. K., Yamada, K. M. and Mosher, D. F. (1990) Inhibition of binding of fibronectin to matrix assembly sites by anti-integrin (α5β1) antibodies. J. Cell Biol. 111, 699-708.
41. Forsberg, E., Ek, B., Engström, A. and Johansson, S. (1994). Purification and characterization of integrin α9β1. Exp. Cell Res. 213, 183-190.
42. Galbraith, C. G. and Sheetz, M. P. (1998). Forces on adhesive contacts affect cell function. Curr. Opin. Cell Biol. 10, 566-571.
43. Gardner, H., Kreidberg, J., Koteliansky, V. and Jaenisch, R. (1996). Deletion of integrin α1 by homologous recombination permits normal murine development but gives rise to a specific deficit in cell adhesion. Dev. Biol. 175, 301-313.
44. George, E. L., George-Labouesse, E. N., Patel-King, R. S., Rayburn, H. and Hynes, R. O. (1993). Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119, 1079-1091.
45. Georges-Labouesse, E., Messaddeq, N., Yehia, G., Cadalbert, L., Dierich, A. and Le Meur, M. (1996). Absence of integrin α6 leads to epidermolysis bullosa and neonatal death in mice. Nature Genet. 13, 370-373.
46. Goh, K. L., Yang, J. T. and Hynes, R. O. (1997). Mesodermal defects and cranial neural crest upoptosis in α5 integrin-null embryos. Development 124, 4309-4319.
47. Hemler, M. E., Huang, C., Takada, Y., Schwartz, L., Strominger, J. L. and Clabby, M. L. (1987). Characterization of the cell surface heterodimer VLA-4 and related peptides. J. Biol. Chem. 262, 11478-11485.
48. Henion, P. D. and Weston, J. A. (1997). Timing and pattern of cell fate restrictions in the neural crest lineage. Development 1997, 4351-4359.
49. Hodivala-Dilke, K. M., McHugh, K. P., Tsakiris, D. A., Rayburn, H., Crowley, D., Ullman-Cullere, M., Ross, F. P., Coller, B. S., Teitelbaum, S. and Hynes, R. O. (1999). Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J. Clin. Invest. 103, 229-238.
50. Horwitz, A., Duggan, K., Greggs, R., Decker, C. and Buck, C. (1985) The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J. Cell Biol. 101, 2134-2144.
51. Hynes, R. O. (1992). Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
52. Hynes, R. O. (1996). Targeted mutations in cell adhesion genes: What we have learned from them? Dev. Biol. 180, 402-412.
53. Jacques, T. S., Relvas, J. B., Nishimura, S., Pytela, R., Edwards, G. M., Streuli, C. H. and ffrench-Constant, C. (1998). Neural precursor cell chain migration and division are regulated through different β1 integrins. Development 125, 3167-3177.
54. Jaffredo, T., Horwitz, A. F., Buck, C. A., Rong, P.-M. and Dieterlen-Lièvre, F. (1988). Myoblast migration specifically inhibited in the chick embryo by grafted CSAT hybridoma cells secreting an anti-integrin antibody. Development 103, 431-446.
55. Keely, P., Parise, L. and Juliano, R. (1998). Integrins and GTPases in tumour cell growth, motility and invasion. Trends Cell Biol. 8, 101-106.
56. Kil, S. H. and Bronner-Fraser, M. (1996). Expression of the avian α7-integrin in developing nervous system and myotome. Int. J. Dev. Neurosci. 14, 181-190.
57. Kil, S. H., Krull, C. E., Cann, G., Clegg, D. and Bronner-Fraser, M. (1998). The α4 subunit of integrin is important for neural crest cell migration. Dev. Biol. 202, 29-42.
58. Kil, S. H., Lallier, T. and Bronner-Fraser, M. (1996). Inhibition of cranial neural crest adhesion in vitro and migration in vivo using integrin antisens oligonucleotides. Dev. Biol. 179, 91-101.
59. Kreidberg, J. A., Donovan, M. J., Goldstein, S. L., Rennke, H., Shepherd, K., Jones, R. C. and Jaenisch, R. (1996). α3β1 integrin has a crucial role in kidney and lung organogenesis. Development 122, 3537-3547.
60. 2+-independent manner. J. Cell Biol. 119, 1335-1345.
61. Lallier, T., Deutzmann, R., Perris, R. and Bronner-Fraser, M. (1994). Neural crest cell interactions with laminin: Structural requirements and localization of the binding site for α1β1 integrin. Dev. Biol. 162, 451-464.
62. Lallier, T., Leblanc, G., Artinger, K. B. and Bronner-Fraser, M. (1992). Cranial and trunk neural crest cells use different mechanisms for attachment to extracellular matrices. Development 116, 531-541.
63. Le Douarin, N. M., Ziller, C. and Couly, G. F. (1993). Patterning of neural crest derivatives in the avian embryo: In vivo and in vitro studies. Dev. Biol. 159, 24-49.
64. Lefcort, F., Venstrom, K., McDonald, J. A. and Reichardt, L. F. (1992). Regulation of expression of fibronectin and its receptor, α5β1, during development and regeneration of peripheral nerve. Development 116, 767-782.
65. Löhler, J., Timpl, R. and Jaenish, R. (1984). Lethal mutation of mouse collagen I gene causes rupture of blood vessels and is associated with erythropoietic and mesenchymal cell death at day 12 of gestation. Cell 38, 597-607.
66. Mackie, E. J., Tucker, R. P., Halfter, W., Chiquet-Ehrismann, R. and Epperlein, H. H. (1988). The distribution of tenascin coincides with pathways of neural crest cell migration. Development 102, 237-250.
67. Makarem, R., Newham, P., Askari, J. A., Green, L. J., Clements, J., Edwards, M., Humphries, M. J. and Mould, A. P. (1994). Competitive binding of vascular cell adhesion molecule-1 and the hepII/IIICS domain of fibronectin to the integrin α4β1. J. Biol. Chem. 269, 1005-4011.
68. Mould, A. P., Askari, J. A., Craig, S. E., Garratt, A. N., Clements, J. and Humphries, M. J. ( 1994). Integrin α4β1-mediated melanoma cell adhesion and migration on vascular cell adhesion molecule-1 (VCAM-1) and the alternatively spliced IIICS region of fibronectin. J. Biol. Chem. 269, 27224-27230.
69. Müller, U., Bossy, B., Venstrom, K. and Reichardt, L. F. (1995). Integrin α8β1 promotes attachement, cell spreading, and neurite outgrowth on fibronectin. Mol. Biol. Cell 6, 433-448.
70. Müller, U., Wang, D., Dnda, S., Meneses, J. J., Pedersen, R. A. and Reichardt, L. F. (1997). Integrin α8β1 is critically important for epithelial-mesenchymal interactions during kidney morphogenesis. Cell 88, 603-613.
71. Muschler, J. L. and Horwitz, A. F. (1991). Down-regulation of the chicken α5β1 integrin fibronectin receptor during development. Development 113, 327-337.
72. Neugebauer, K. M., Emmet, C. J., Venstrom, K. A. and Reichardt, L. F. (1991). Vitronectin and thrombospondin promote retinal neurite outgrowth: Developmental regulation and role of integrins. Neuron 6, 345-358.
73. Neugebauer, K. M. and Reichardt, L. F. (1991). Cell-surface regulation of β1-integrin activity on developing retinal neurons. Nature 350, 68-71.
74. Newgreen, D. F., Gibbins, I. L., Sauter, J., Wallenfels, B. and Wütz, R. (1982). Ultrastructural and tissue-culture studies on the role of fibronectin, collagen and glycosaminoglycans in the migration of neural crest cells in the fowl embryo. Cell Tiss. Res. 221, 521-549.
75. Perris, R., Kuo, H.-J., Glanville, R. W., Leibold, S. and Bronner-Fraser, M. (1993a). Neural crest cell interaction with type VI collagen is mediated by multiple cooperative binding sites within triple-helix and globular domains. Exp. Cell Res. 209, 103-117.
76. Perris, R., Paulsson, M. and Bronner-Fraser, M. (1989). Molecular mechanisms of avian neural crest cell migration on fibronectin and laminin. Dev. Biol. 136, 222-239.
77. Perris, R., Syfrig, J., Paulsson, M. and Bronner-Fraser, M. (1993b). Molecular mechanisms of neural crest cell attachment and migration on types I and IV collagens. J. Cell Sci. 106, 1357-1368.
78. Phillips, D. R., Charo, I. F. and Scarborough, R. M. (1991). GPIIb-IIIa: The responsive integrin. Cell 65, 359-362.
79. Piali, L., Hammel, P., Dangy, J.-P. and Gisler, R. H. (1997). The use of solubilized transmembrane molecules in adhesion assays. In Immunology Methods Manual (ed. I. Leftovits), pp. 1369-1380. New York: Academic Press.
80. Piali, L., Hammel, P., Uherek, C., Gisler, R. H., Dunon, D. and Imhof, B. A. (1995). CD31/PECAM-1 is a ligand for αvβ3 integrin involved in adhesion of leukocytes to endothelium. J. Cell Biol. 130, 451-460.
81. Poole, T. J. and Thiery, J. P. (1986). Antibodies and a synthetic peptide that block cell-fibronectin adhesion arrest neural crest cell migration in vivo. Prog. Clin. Biol. Res. 217B, 235-238.
82. Pulido, R., Elices, M. J., Campanero, M. R., Osborn, L., Schiffer, S., Garcia-Pardo, A., Lobb, R., Hemler, M. E. and Sanchez-Madrid, F. (1991). Functional evidence for three distinct and independently inhibitable adhesion activities mediated by the human integrin VLA-4. Correlation with distinct α4 epitopes. J. Biol. Chem. 266, 10241-10245.
83. Qian, F., Vaux, D. L. and Weissman, I. L. (1994). Expression of the integrin α4β1 on melanoma cells can inhibit the invasive stage of metastasis formation. Cell 77, 335-347.
84. Rosen, G. D., Sanes, J. R., Lachance, R., Cunningham, J. M., Roman, J. and Dean, D. C. (1992). Roles of the integrin VLA-4 and its counter receptor VCAM1 in myogenesis. Cell 69, 1107-1119.
85. Rovasio, R. A., Delouvée, A., Yamada, K. M., Timpl, R. and Thiery, J. P. (1983). Neural crest cell migration: Requirements for exogenous fibronectin and high cell density. J. Cell Biol. 96, 462-473.
86. Saga, Y., Yagi, T., Ikawa, Y., Sakakura, T. and Aizawa, S. (1992). Mice develop normally without tenascin. Genes Dev. 6, 1821-1831.
87. Schoenwaelder, S. and Burridge, K. (1999). Bidirectional signaling between the cytoskeleton and integrins. Curr. Opin. Cell Biol. 11, 274-286.
88. Springer, T. A. (1994). Traffic signals for lymphocyte recirculation and leucocytes emigration: the multistep paradigm. Cell 76, 301-314.
89. Stemple, D. L. and Anderson, D. J. (1993). Lineage diversification of the neural crest: In vitro investigations. Dev. Biol. 159, 12-23.
90. Stephens, L. E., Sutherland, A. E., Klimanskaya, I. V., Andrieux, A., Meneses, J., Pedersen, R. A. and Damsky, C. H. (1995). Deletion of β1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev. 9, 1883-1895.
91. Stepp, M. A., Urry, L. A. and Hynes, R. O. (1994). Expression of α4 integrin mRNA and protein and fibronectin in the early chicken embryo. Cell Adhes. Commun. 2, 359-375.
92. Sutherland, A. E., Calarco, P. G. and Damsky, C. H. (1993). Developmental regulation of integrin expression at the time of implantation in the mouse embryo. Development 119, 1175-1186.
93. Thiery, J. P., Duband, J.-L. and Delouvée, A. (1982). Pathways and mechanism of avian trunk neural crest cell migration and localization. Dev. Biol. 93, 324-343.
94. Tucker, R. P. and Erickson, C. A. (1984). Morphology and behavior of quail neural crest cells in artificial three-dimensional extracellular matrices. Dev. Biol. 104, 390-405.
95. Tucker, R. P. and McKay, S. E. (1991). The expression of tenascin by neural crest cells and glia. Development 112, 1031-1039.
96. Varner, J. A. and Cheresh, D. A. (1996). Integrins and cancer. Curr. Opin. Cell Biol. 8, 724-730.
97. Varner, J. A., Emerson, D. A. and Juliano, R. L. (1995). Integrin α5β1 expression negatively regulates cell growth: Reversal by attachment to fibronectin. Mol. Biol. Cell 6, 725-740.
98. Varnum-Finney, B., Venstrom, K., Muller, U., Kypta, R., Backus, C., Chiquet, M. and Reichardt, L. F. (1995). The integrin receptor α8β1 mediates interactions of embryonic chick motor and sensory neurons with tenascin-C. Neuron 14, 1213-1222.
99. Venstrom, K. and Reichardt, J. (1995). β8 integrins mediate interactions of chick sensory neurons with laminin-1, collagen IV, and fibronectin. Mol. Biol. Cell 6, 419-431.
100. Wayner, E. A., Carter, W. G., Piotrowicz, R. S. and Kunicki, T. J. (1988). The function of multiple extracellular matrix receptors in mediating cell adhesion to extracellular matrix: Preparation of monoclonal antibodies to the fibronectin receptor that specifically inhibit cell adhesion to fibronectin and react with platelet glycoproteins Ic-IIa. J. Cell Biol. 107, 1881-1891.
101. Wennerberg, K., Lohikangas, L., Gullberg, D., Pfaff, M., Johansson, S. and Fässler, R. (1996). β1 integrin-dependent and -independent polymerization of fibronectin. J. Cell Biol. 132, 227-238.
102. Werb, Z., Tremble, P. M., Behrendsten, O., Crowley, E. and Damsky, C. H. (1989). Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression. J. Cell Biol. 109, 877-889.
103. Wu, C., Fields, A. J., Kapteijn, B. A. E. and McDonald, J. A. (1995). The role of α4β1 integrin in cell motility and fibronectin matrix assembly. J. Cell Sci. 108, 821-829.
104. Yamada, S., Brown, K. E. and Yamada, K. M. (1995). Differential mRNA regulation of integrin subunit aV, β1, β3, and β5 during mouse embryonic organogenesis. Cell Adhes. Commun. 3, 311-325.
105. Yang, J. T. and Hynes, R. O. (1996). Fibronectin receptor functions in embryonic cells deficient in α5β1 integrin can be replaced by αv integrins. Mol. Biol. Cell 7, 1737-1748.
106. Yang, J. T., Rayburn, H. and Hynes, R. O. (1993). Embryonic mesodermal defects in α5 integrin-deficient mice. Development 119, 1093-1105.
107. Yang, J. T., Rayburn, H. and Hynes, R. O. (1995). Cell adhesion events mediated by α4 integrins are essential in placental and cardiac development. Development 121, 549-560.
108. Zhang, Z., Vuori, K., Reed, J. C. and Ruoslahti, E. (1995). The α5β1 integrin supports survival of cells on fibronectin and up-regulates Bcl-2 expression. Cell Biol. 92, 6161-6165.
109. Zheng, X., Saunders, T. L., Camper, S. A., Samuelson, L. C. and Ginsburg, D. (1995). Vitronectin is not essential for normal mammalian development and fertility. Proc. Natl. Acad Sci. USA 92, 12426-12430.