A novel non-independent fibronectin assembly pathway initiated by α4β1 integrin binding to the alternatively spliced V region

Journal of Cell Science

Volumn 113, Issue 8, 2000, Pages 1491-1498

  Sechler, Jan L ^a,b   Cumiskey, Anne Marie ^a   Gazzola, Deana M ^a   Schwarzbauer, Jean E ^a  

^a PRINCETON UNIVERSITY   (United States)

^b GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Alternative splicing; Cytoskeleton; Extracellular matrix; Fibronectin; Integrin

Indexed keywords

ACTIN; FIBRONECTIN; INTEGRIN; MANGANESE; MONOCLONAL ANTIBODY; RECOMBINANT PROTEIN; ARGINYL-GLYCYL-ASPARTIC ACID; ARGINYLGLYCYLASPARTIC ACID; HOMING RECEPTOR; OLIGOPEPTIDE; VERY LATE ACTIVATION ANTIGEN 4;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; B CELL LYMPHOMA; BINDING SITE; CELL GROWTH; CHO CELL; CONTROLLED STUDY; CYTOSKELETON; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; ANIMAL; EXTRACELLULAR MATRIX; GENETIC TRANSFECTION; GENETICS; HAMSTER; METABOLISM;

ALTERNATIVE SPLICING; ANIMALS; BINDING SITES; CHO CELLS; CRICETINAE; EXTRACELLULAR MATRIX; FIBRONECTINS; HUMANS; INTEGRIN ALPHA4BETA1; INTEGRINS; OLIGOPEPTIDES; PROTEIN BINDING; RECEPTORS, LYMPHOCYTE HOMING; RECOMBINANT PROTEINS; TRANSFECTION;

EID: 0034092910     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. Ali, I. U and Hynes, R. O. (1977). Effects of cytochalasin B and colchicine on attachment of a major surface protein of fibroblasts. Biochim Biophys. Acta 471, 16-24.
2. Aumailley, M., Mann, K., von der Mark, H. and Timpl, R. (1989). Cell attachment properties of collagen type VI and Arg-Gly-Asp dependent binding to its α2(VI) and α3(VI) chains. Exp. Cell Res. 181, 463-474.
3. 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.
4. 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.
5. Dominguez-Jimenez, C., Sanchez-Aparicio, P., Labar, J. P. and Garcia-Pardo, A. ( 1996). The α4β1 fibronectin ligands CS-1, HEP II, and RGD induce different intracellular events in B lymphoid cells. Comparison with the effects of the endothelial ligand VCAM-1. Cell Adhes. Commun. 4, 251-267.
6. Dunon, D., Piali, L. and Imhof, B. A. (1996). To stick or not to stick: the new leukocyte homing paradigm. Curr. Opin. Cell Biol. 8, 714-723.
7. Elices, M. J. (1994). Leukocyte integrins. In lntegrins: Molecular and Biological Responses to the Extracellular Matrix (ed. D. A. Cheresh and R. P. Mecham), pp. 163-194. San Diego: Academic Press.
8. Gailit, J. and Ruoslahti, E. ( 1988). Regulation of fibronectin receptor affinity by divalent cations. J. Biol. Chem. 263, 12927-12932.
9. Garcia-Pardo, A., Wayner, E. A., Carter, W. G. and Ferreira, O. C. (1990). Human B lymphocytes define an alternative mechanism of adhesion to fibronectin: the interaction of the a4b1 integrin with the LHGPEILDVPST sequence of the type III connecting segment is sufficient to promote cell attachment. J. lmmunol. 144, 3361-3366.
10. 1. Cell 60, 53-61.
11. Hemler, M. E. (1990). VLA proteins in the integrin family: Structures, functions, and their role on leukocytes. Annu. Rev. lmmunol. 8, 365-400.
12. Hemler, M. E., Sanchez-Madrid, F., Flotte, T. J., Krensky, A. M., Burakoff, S. J., Bhan, A. K., Springer, T. A. and Strominger, J. L. (1984). Glycoproteins of 210,000 and 130,000 MW on activated T cells: cell distribution and antigenic relation to components on resting cells and T cell lines. J. lmmunol 132, 3011-3018.
13. Hotchin, N. A. and Hall, A. (1995). The assembly of integrin adhesion complexes requires both extracellular matrix and inlracellular rho/rac GTPases. J. Cell Biol. 131, 1857-65.
14. Humphries, M. J., Komoriya, A., Akiyama, S. K., Olden, K. and Yamada, K. M. (1987). Identification of two distinct regions of the type III connecting segment of human plasma fibronectin that promote cell type-specific adhesion. J. Biol. Chem. 262, 6886-6892.
15. Hynes, R. O. (1990). Fibronectins. New York: Springer-Verlag.
16. lrie, A., Kamata, T. and Takada, Y. (1997). Multiple loop structures critical for ligand binding of the integrin α4 subunit in the upper face of the β-propeller mode 1. Proc. Natl Acad Sci. USA 94, 7198-7203.
17. Kassner, P. D., Alon, R., Springer, T. A. and Hemler, M. E. (1995). Specialized functional properties of the integrin α4 cytoplasmic domain. Mol. Biol Cell 6, 661-674.
18. Kassner, P. D., Teixido, J., Chan, B. M., Parker, C. M. and Hemler, M. E. (1992). Analyses of VLA-4 structure and function. Adv. Exp. Med. Biol. 323, 163-170.
19. Leahy, D. J., Hendrickson, W. A., Aukhil, I. and Erickson, H. P. (1992). Structure of a fibronectin type III domain from tenascin phased by MAD analysis of the selenomethionyl protein. Science 258, 987-991.
20. Liu, S., Thomas, S. M., Woodside, D. G., Rose, D. M., Kiosses, W. B., Pfaff, M. and Ginsberg, M. H. (1999). Binding of paxillin to α4 integrins modifies integrin-dependent biological responses. Nature 402, 676-681.
21. Lobb, R. R. and Hemler, M. E. ( 1994). The pathophysiologic role of α4 integrins in vivo. J. Clin. Invest. 94, 1722-1728.
22. Main, A. L., Harvey, T. S., Baron, M., Boyd, J. and Campbell, I. D. (1992). The three-dimensional structure of the tenth type III module of fibronectin: An insight into RGD-mediated interactions. Cell 71, 671-678.
23. Masumoto, A. and Hemler, M. E. (1993). Multiple activation states of VLA-4: Mechanistic differences between adhesion to CSl/fibronectin and to vascular cell adhesion molecule. J. Biol. Chem. 268, 228-234.
24. McDonald, J. A., Quade, B. J., Broekelman, T. J., LaChance, R., Forsman, K., Hasegawa, E. and Akiyama, S. ( 1987). Fibronectin's cell-adhesive domain and an amino-terminal matrix assembly domain participate in its assembly into fibroblast pericellular matrix. J. Biol. Chem. 262, 2957-2967.
25. McMurray, R. W. (1996). Adhesion molecules in autoimmune disease. Semin Arthritis Rheum. 25, 215-233.
26. Mosher, D. F. (1993). Assembly of fibronectin into extracellular matrix. Curr. Opin. Struct. Biol. 3, 214-222.
27. Mould, A. P. and Humphries, M. J. ( 1991). Identification of a novel recognition sequence for the integrin α4β1 in the COOH-terminal heparin-binding domain of fibronectin. EMBO J. 10, 4089-4095.
28. Mould, A. P., Komoriya, A., Yamada, K.M. and Humphries, M. J. ( 1991 ). The CS5 peptide is a second site in the IIICS region of fibronectin recognized by the integrin α4β1: Inhibition of α4β1 function by RGD peptide homologues J. Biol. Chem. 266, 3579-3585.
29. Moyano, J. V., Carnemolla, B., Dominguez-Jimenez, C., Carcia-Gila, M., Albar, J. P., Sanchez-Aparicio, P., Leprini, A., Querze, G., Zardi, L. and Garcia-Pardo, A. (1997). Fibronectin type III5 repeat contains a novel cell adhesion sequence, KLDAPT, which binds activated α4β1 and α4β7 integrins. J. Biol. Chem. 272, 24832-24836.
30. Nagai, T., Yamakawa, N., Aota, S., Yamada, S. S., Akiyama, S. K., Olden, K. and Yamada, K. M. (1991). Monoclonal antibody characterizaion of two distant sites required for function of the central cell-binding domain of fibronectin in cell adhesion, cell migration, and matrix assembly. J. Cell Biol. 114, 1295-1305.
31. Ohashi, T., Kiehart, D. P. and Erickson, H. P. (1999). Dynamics and elasticity of the fibronectin matrix in living cell culture visualized by fibronectin-green fluorescent protein. Proc. Natl. Acad. Sci. USA 96, 2153-2158.
32. Rose, D. M., Cardarelli, P. M., Cobb, R. R. and Ginsberg, M. H. (2000). Soluble VCAM-1 binding to α4 integrins is cell type-specific, activation-dependent, and disrupted during apoptosis in T cells. Blood 95, 602-609.
33. Rosen, G. D., Sanes, J. R., LaChance, R., Cunningham, J. M., Roman, J. and Dean, D. C. (1992). Roles for the integrin VLA-4 and its counter receptor VCAM-1 in myogenesis. Cell 69, 1107-1119.
34. Sanchez-Aparicio, P., Domingues-Jimenez, C. and Garcia-Pardo, A. ( 1994). Activation of the α4β1 integrin through the β1 subunit induces recognition of the RGDS sequence in fibronectin. J. Cell Biol. 126, 271-279.
35. Schreiner, C. L., Bauer, J. S., Danilov, Y. N., Hussein, S., Sczekan, M. M. and Juliano, R. L. (1989). Isolation and characterization of Chinese hamster ovary cell variants deficient in the expression of fibronectin receptor. J. Cell Biol. 109, 3157-3167.
36. Schwarzbauer, J. E., Mulligan, R. C. and Hynes, R. O. (1987). Efficient and stable expression of recombinant fibronectin polypeptides. Proc. Natl Acad. Sci. USA 84, 754-8.
37. Schwarzbauer, J. E. and Sechler, J. L. (1999). Fibronectin fibrillogenesis: a paradigm for extracellular matrix assembly. Curr. Opin. Cell Biol. 11, 622-627.
38. Sechler, J. L., Corbett, S. A. and Schwarzbauer, J. E. ( 1997). Modulalory roles for integrin activation and the synergy site of fibronectin during matrix assembly. Mol. Biol. Cell 8, 2563-2573.
39. Sechler, J. L., Corbett, S. A., Wenk, M. B. and Schwarzbauer, J. E. ( 1998). Modulation of cell-extracellular matrix interactions. Ann. NY Acad. Sci. 857, 143-154.
40. Sechler, J. L. and Schwarzbauer, J. E. (1998). Control of cell cycle progression by fibronectin matrix architecture. J. Biol. Chem. 273, 25533-25536.
41. Sechler, J. L. and Schwarzbauer, J. E. (1997). Coordinated regulation of fibronectin fibril assembly and actin stress fiber formation. Cell Adhes. Commun. 4, 413-424.
42. Sechler, J. L., Takada, Y. and Schwarzbauer, J. E. (1996). Altered rate of fibronectin matrix assembly by deletion of the first type III repeats. J. Cell Biol. 134, 573-583.
43. Wahl, S. M., Allen, J. B., Hines, K. L., Imamichi, T., Wahl, A. M., Furcht, L. T. and McCarthy, J. B. ( 1994). Synthetic fibronectin peptides suppress arthritis in rats by interrupting leukocyte adhesion and recruitment. J. Clin Invest. 94, 655-662.
44. Wayner, E. A., Garcia-Pardo, A., Humphries, M. J., McDonald, J. A. and Carter, W. G. (1989). Identification and characterization of the T lymphocyte adhesion receptor for an alternative cell attachment domain (CS-1) in plasma fibronectin. J. Cell Biol. 109, 1321-1330.
45. Wennerberg, K., Lohikangas, L., Gullberg, D., Pfaff, M., Johansson, S. and Fassler, R. (1996). β1 integrin-dependent and -independent polymerization of fibronectin. J. Cell Biol. 132, 227-238.
46. Wu, C. (1997). Roles of integrins in fibronectin matrix assembly. Histol. Histopathol. 12, 233-240.
47. Wu, C., Bauer, J. S., Juliano, R. L. and McDonald, J. A. (1993). The alpha 5 beta 1 integrin fibronectin receptor, but not the alpha 5 cytoplasmic domain, functions in an early and essential step in fibronectin matrix assembly. J. Biol. Chem. 268, 21883-21888.
48. Wu, C., Fields, A. J., Kapteijin, B. A. E. and McDonald, J. A. (1995). The role of alpha 4 beta 1 integrin in cell motility and fibronectin matrix assembly. J. Cell Sci. 108, 821-829.
49. Wu, C., Hughes, P. E., Ginsberg, M. H. and McDonald, J. A. (1996). Identification of a new biological function for the integrin αvβ3: Initiation of fibronectin matrix assembly. Cell Adhes. Commun. 4, 149-158.
50. Wu, C., Kevins, V., O'Toole, T. E., McDonald, J. A. and Ginsberg, M. H. ( 1995). Integrin activation and cytoskeletal interaction are critical steps in the assembly of a fibronectin matrix. Cell 83, 715-724.
51. Zhang, Q., Checovich, W. J., Peters, D. M., Albrecht, R. M. and Mosher, D. F. (1994). Modulation of cell surface fibronectin assembly sites by lysophosphatidic acid. J. Cell Biol. 127, 1447-1459.
52. Zhong, C., Chrzanowska-Wodnicka, M., Brown, J., Shaub, A., Belkin, A. M. and Burridge, K. (1998). Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 141, 539-551.