Recruitment of vimentin to the cell surface by β3 integrin and plectin mediates adhesion strength

Journal of Cell Science

Volumn 122, Issue 9, 2009, Pages 1390-1400

  Bhattacharya, Ramona ^a   Gonzalez, Annette M ^a   DeBiase, Phillip J ^a   Trejo, Humberto E ^a   Goldman, Robert D ^a   Flitney, Frederick W ^a   Jones, Jonathan C R ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Adhesion; Integrin; Intermediate filament

Indexed keywords

BETA3 INTEGRIN; PLECTIN; TYROSINE; VIMENTIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL NUCLEUS; CELL SURFACE; CHO CELL; CYTOPLASM; FOCAL ADHESION; HUMAN; HUMAN CELL; INTERMEDIATE FILAMENT; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL ADHESION; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; CYTOSKELETON; ENDOTHELIAL CELLS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; HUMANS; INTEGRIN BETA3; INTERMEDIATE FILAMENTS; MICROTUBULES; MOLECULAR MOTOR PROTEINS; PAXILLIN; PLECTIN; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; VIMENTIN;

EID: 67650558915     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.043042     Document Type: Article

References (47)

1. Arias-Salgado, E. G., Lizano, S., Sarkar, S., Brugge, J. S., Ginsberg, M. H. and Shattil, S. J. (2003). Src kinase activation by direct interaction with the integrin β-cytoplasmic domain. Proc. Natl. Acad. Sci. USA 100, 13298-13302.
2. Axelrod, D. (1989). Total internal reflection fluorescence microscopy. Methods Cell Biol. 30, 245-270.
3. Bershadsky, A. D., Tint, I. S. and Svitkina, T. M. (1987). Association of intermediate filaments with vinculin-containing adhesion plaques of fibroblasts. Cell Motil. Cytoskeleton 8, 274-283.
4. Blystone, S. D. (2004). Integrating an integrin: A direct route to actin. Biochim. Biophys. Acta 1692, 47-54.
5. Blystone, S. D., Lindberg, F. P., Williams, M. P., McHugh, K. P. and Brown, E. J. (1996). Inducible tyrosine phosphorylation of the β3 integrin requires the αv integrin cytoplasmic tail. J. Biol. Chem. 271, 31458-31462.
6. Blystone, S. D., Williams, M. P., Slater, S. E. and Brown, E. J. (1997). Requirement of integrin β3 tyrosine 747 for β3 tyrosine phosphorylation and regulation of αvβ3 avidity. J. Biol. Chem. 272, 28757-28761.
7. Boettiger, D., Huber, F., Lynch, L. and Blystone, S. (2001). Activation of αvβ3-vitronectin binding is a multistage process in which increases in bond strength are dependent on Y747 and Y759 in the cytoplasmic domain of β3. Mol. Biol. Cell 12, 1227-1237.
8. Chen, Y. P., Djaffar, I., Pidard, D., Steiner, B., Cieutat, A. M., Caen, J. P. and Rosa, J. P. (1992). Ser-752->Pro mutation in the cytoplasmic domain of integrin β3 subunit and defective activation of platelet integrin αIIbβ3 (glycoprotein IIb-IIIa) in a variant of Glanzmann thrombasthenia. Proc. Natl. Acad. Sci. USA 89, 10169-10173.
9. DePaola, N., Davies, P. F., Pritchard, W. F., Jr, Florez, L., Harbeck, N. and Polacek, D. C. (1999). Spatial and temporal regulation of gap junction connexin43 in vascular endothelial cells exposed to controlled disturbed flows in vitro. Proc. Natl. Acad. Sci. USA 96, 3154-3159.
10. Eckes, B., Dogic, D., Colucci-Guyon, E., Wang, N., Maniotis, A., Ingber, D., Merckling, A., Langa, F., Aumailley, M., Delouvee, A. et al. (1998). Impaired mechanical stability, migration and contractile capacity in vimentin-deficient fibroblasts. J. Cell Sci. 111 1897-1907.
11. Ezratty, E. J., Partridge, M. A. and Gundersen, G. G. (2005). Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7, 581-590.
12. Faccio, R., Novack, D. V., Zallone, A., Ross, F. P. and Teitelbaum, S. L. (2003). Dynamic changes in the osteoclast cytoskeleton in response to growth factors and cell attachment are controlled by β3 integrin. J. Cell Biol. 162, 499-509.
13. Gailit, J. and Ruoslahti, E. (1988). Regulation of the fibronectin receptor affinity by divalent cations. J. Biol. Chem. 263, 12927-12932.
14. Giancotti, F. G. and Ruoslahti, E. (1999). Integrin signaling. Science 285, 1028-1032.
15. Gonzales, M., Weksler, B., Tsuruta, D., Goldman, R. D., Yoon, K. J., Hopkinson, S. B., Flitney, F. W. and Jones, J. C. R. (2001). Structure and function of a vimentin-associated matrix adhesion in endothelial cells. Mol. Biol. Cell 12, 85-100.
16. Gonzalez, A. M., Gonzales, M., Herron, G. S., Nagavarapu, U., Hopkinson, S. B., Tsuruta, D. and Jones, J. C. R. (2002). Complex interactions between the laminin α4 subunit and integrins regulate endothelial cell behavior in vitro and argiogenesis in vivo. Proc. Natl. Acad. Sci. USA 99, 16075-16080.
17. Helfand, B. T., Chang, L. and Goldman, R. D. (2004). Intermediate filaments are dynamic and motile elements of cellular architecture. J. Cell Sci. 117, 133-141.
18. Homan, S. M., Martinez, R., Benware, A. and LaFlamme, S. E. (2002). Regulation of the association of α6β4 with vimentin intermediate filaments in endothelial cells. Exp. Cell Res. 281 107-114.
19. Hughes, P. E., O'Toole, T. E., Ylanne, J., Shattil, S. J. and Ginsberg, M. H. (1995). The conserved membrane-proximal region of an integrin cytoplasmic domain specifies ligand binding affinity. J. Biol. Chem. 270, 12411-12417.
20. Hynes, R. O. (2007). Cell-matrix adhesion in vascular development. J. Thromb. Haemost. 5 Suppl. 1, 32-40.
21. Hynes, R. O., Bader, B. L. and Hodivala-Dilke, K. (1999). Integrins in vascular development. Braz. J. Med. Biol. Res. 12 501-510.
22. Jefferson, J. J., Ciatto, C., Shapiro, L. and Liem, R. K. (2007). Structural analysis of the plakin domain of bullous pemphigoid antigen1 (BPAG1) suggests that plakin are members of the spectrin superfamily. J. Mol. Biol. 366, 244-257.
23. Jenkins, A. L., Nannizzi-Alaimo, L., Silver, D., Sellers, J. R., Ginsberg, M. H., Law, D. A. and Phillips, D. R. (1998). Tyrosine phosphorylation of the Β3 cytoplasmic domain mediates integrin-cytoskeletal interactions. J. Biol Chem. 273, 13878-13885.
24. Jones, J. C. R., Hopkinson, S. B. and Goldfinger, L. E. (1998). Structure and assembly of hemidesmosomes. Bioassays 20, 488-494.
25. Kreis, S., Schonfeld, H. J., Melchior, C., Steiner, B. and Kieffer, N. (2005). The intermediate filament protein vimentin binds specifically to a recombinant integrin α2/β1 cytoplasmic tail complex and co-localizes with native α2/β1 in endothetial cell focal adhesions. Exp. Cell Res. 305, 110-121.
26. Krylyshkina, O, Anderyn, K. I., Kaverina, I., Upmann, I., Manstein, D. J., Small, J. V. and Toonare, D. K. (2003), Nanometer targeting of microtubules to focal adhesions. J. Cell Biol. 161, 853-859.
27. Ortiz-Urda, S., Garcia, J., Green, C. L., Chen, L., Lin, Q., Veitch, D. P., Sakai, L. Y., Lee, H., Marinkovich, M. P. and Khavari, P. A. (2005). Type VII collagen is required for Ras-driven human epidermal tumorigenesis. Science 307, 1773-1776.
28. Prahlad, V., Yoon, M., Moir, R. D., Vale, R. D. and Goldman, R. D. (1998). Rapid movements of vimentin on microtubule tracks: kinesin-dependent assembly of intermediate filament networks. J. Cell Biol. 143, 159-170.
29. Rupp, P. A. and Little, C. D. (2001). Integrins in vascular development. Circ. Res. 89, 566-572.
30. Schaffner-Reckinger, E., Gotten, V., Melchior, C., Plancon, S. and Kieffer, N. (1998). Distinct involvement of β3 integrin cytoplasmic domain tyrosine residues 747 and 759 in integrin-mediated cytoskeletal assembly and phosphotyrosine signaling. J. Biol. Chem. 273, 12623-12632.
31. Schweitzer, K. M., Vicart, P., Delouis, C., Paulin, D., Dräger, A. M., Langenhuijsen, M. M. A. C. and Wekster, B. B. (1997). Characterization of a newly established human bone marrow endothelial cell line: Distinct adhesive properties for hematopoietic progenitors compared with human umbilical vein endothelial cells. Lab. Invest. 76, 25-36.
32. Seifert, G. J., Lawson, D. and Wiche, G. (1992). Immunolocalization of the intermediate filament-associated protein plectin at focal contacts and actin stress fibers. Eur. J. Cell Biol. 59, 138-147.
33. Simon, K. O. and Burridge, K. (1994). Interactions between integrins and the cytoskeleton: Structure and regulation. In Integrins: Molecular and Biological Responses to the Extracellular Matrix (ed. D. A. Cheresh and R. P. Mecham), pp. 49-78. San Diego, CA: Academic Press.
34. Small, J. V., Geiger, B., Kaverins, I. and Bershadsky, A. (2002). How do microtubules guide migrating cells? Nat. Rev. Mol. Cell. Biol. 3, 957-964.
35. Spurny, R., Abdoulrahman, K., Janda, L., Runzler, D., Kohler, G., Castanon, M. J. and Wiche, G. (2007). Oxidation and nitrosylation of cysteines proximal to the intermediate filament (IF)-binding site of plectin: Effects on structure and vimentin binding and involvement in IF collapse. J. Biol. Chem. 282, 8175-8187.
36. Steyer, J. A. and Almers, W. (2001). A real-time view of life within 100 nm of the plasma membrane. Nat. Rev. Mol. Cell. Biol. 2, 268-275.
37. Toomre, D. and Manstein, D. J. (2001). Lighting up the cell surface with evanescent wave microscopy. Trends Cell Biol. 11 298-303.
38. Tsuruta, D. and Jones, J. C. (2003). The vimentin cytoskeleton regulates focal contact size and adhesion of endothelial cells subjected to shear stress. J. Cell. Sci. 116, 4977-4984
39. Tsuruta, D., Gonzales, M., Hopkinson, S. B., Otey, C., Khuon, S., Goldman, R. D. and Jones, J. C. (2002). Microfilament-dependent movement of the β3 integrin subunit within focal contacts of endothelial cells. FASEB J. 16, 866-868.
40. Wiche, G., Hermann, H., Leichtfried, F. and Pytela, R. (1982). Plectin: A high-molecular weight cytoskeletal polypeptide component that copurifies with intermediate filaments of the vimentin type. Cold Spring Harb. Symp. Quant. Biol. 46, 475-482.
41. Windoffer, R., Kolsch, A., Woll, & and Leube, R. E. (2006). Focal adhesions are hotspots for keratin filament precursor formation. J. Cell Biol. 173, 341-348.
42. Winter, L., Abrahamsberg, C. and Wiche, G. (2008). Plectin isoform 1b mediates mitochondrion-intermediate filament network linkage and controls organelle shape. J Cell Biol. 181, 903-911.
43. Wozniak, M. A., Modzelewska, K., Kwong, L. and Keely, P. J. (2004). Focal adhesion regulation of cell behavior. Biochim. Biophys. Acta 1692, 103-119.
44. Wu, X., Kodsma, A. and Fuchs, E. (2008). ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 135, 137-148.
45. Ylanne, J., Chen, Y., O'Toole, T. E., Loftus, J. C., Takada, Y. and Ginsberg, M. H. (1993). Distinct functions of integrin alpha and beta subunit cytoplasmic domains in cell spreading and formation of focal adhesions. J. Cell Biol 122, 223-233.
46. Yoon, M., Moir, R. D., Prahlad, V. and Goldman, R. D. (1998). Motile properties of vimentin intermediate filament networks in living cells. J. Cell Biol. 143, 147-157.
47. Zaric, J. and Ruegg, C. (2005). Integrin-mediated adhesion and soluble ligand binding stabilize COX-2 protein levels in endothelial cells by inducing expression and preventing degradation. J. Biol. Chem. 280, 1077-1085.