Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells

Journal of Cell Science

Volumn 116, Issue 22, 2003, Pages 4605-4613

  Zaidel Bar, Ronen ^a   Ballestrem, Christoph ^a   Kam, Zvi ^a   Geiger, Benjamin ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Cell motility; Endothelial cells; Focal adhesions; Focal complexes; Lamellipodia; Zyxin

Indexed keywords

ACTIN; ALPHA ACTININ; BETA3 INTEGRIN; CELL PROTEIN; FOCAL ADHESION KINASE; PAXILLIN; PHOSPHOTYROSINE; TALIN; VASODILATOR STIMULATED PHOSPHOPROTEIN; VINCULIN; ZYXIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL COMPOSITION; CELL MIGRATION; CELL MOTILITY; CELL TRANSFORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FOCAL ADHESION; IN VITRO STUDY; NONHUMAN; PHASE CONTRAST MICROSCOPY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ACTININ; ACTINS; ACTOMYOSIN; ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; CLONING, MOLECULAR; CYTOSKELETAL PROTEINS; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; GLYCOPROTEINS; INTEGRIN BETA3; MICROFILAMENT PROTEINS; MICROSCOPY, FLUORESCENCE; PAXILLIN; PHOSPHOPROTEINS; PHOSPHOTYROSINE; PSEUDOPODIA; TALIN; VINCULIN; WOUND HEALING;

ANIMALIA;

EID: 0344465841     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00792     Document Type: Article

References (43)

1. Ballestrem, C., Hinz, B., Imhof, B. A. and Wehrle-Haller, B. (2001). Marching at the front and dragging behind: differential alphaVbeta3-integrin turnover regulates focal adhesion behavior. J. Cell Biol. 155, 1319-1332.
2. Bear, J. E., Loureiro, J. J., Libova, I., Fassler, R., Wehland, J. and Gertler, F. B. (2000). Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101, 717-728.
3. Borisy, G. G. and Svitkina, T. M. (2000). Actin machinery: pushing the envelope. Curr. Opin. Cell Biol. 12, 104-112.
4. Chen, H., Duncan, I. C., Bozorgchami, H. and Lo, S. H. (2002). Tensin1 and a previously undocumented family member, tensin2, positively regulate cell migration. Proc. Natl. Acad. Sci. USA 99, 733-738.
5. Chrzanowska-Wodnicka, M. and Burridge, K. (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415.
6. Critchley, D. R. (2000). Focal adhesions - the cytoskeletal connection. Curr. Opin. Cell Biol. 12, 133-139.
7. DeMali, K. A., Barlow, C. A. and Burridge, K. (2002). Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion. J. Cell Biol. 159, 881-891.
8. Drees, B. E., Andrews, K. M. and Beckerle, M. C. (1999). Molecular dissection of zyxin function reveals its involvement in cell motility. J. Cell Biol. 147, 1549-1560.
9. Galbraith, C. G., Yamada, K. M. and Sheetz, M. P. (2002). The relationship between force and focal complex development. J. Cell Biol. 159, 695-705.
10. Geiger, B. and Bershadsky, A. (2001). Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. 13, 584-592.
11. Geiger, B., Bershadsky, A., Pankov, R. and Yamada, K. M. (2001). Transmembrane extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2, 793-805.
12. Hahne, P., Sechi, A., Benesch, S. and Small, J. V. (2001). Scar/WAVE is localised at the tips of protruding lamellipodia in living cells. FEBS Lett. 492, 215-220.
13. Helfman, D. M., Levy, E. T., Berthier, C., Shtutman, M., Riveline, D., Grosheva, L, Lachish-Zalait, A., Elbaum, M. and Bershadsky, A. D. (1999). Caldesmon inhibits nonmuscle cell contractility and interferes with the formation of focal adhesions. Mol. Biol. Cell 10, 3097-3112.
14. Huttenlocher, A., Ginsberg, M. and Horwitz, A. (1996). Modulation of cell migration by integrin-mediated cytoskeletal linkages and ligand-binding affinity. J. Cell Biol. 134, 1551-1562.
15. Hynes, R. O. (1992). Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
16. Ilic, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M. and Yamamoto, T. (1995). Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544.
17. Jiang, G., Giannone, G., Critchley, D. R., Fukumoto, E. and Sheetz, M. P. (2003). Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 424, 334-337.
18. Kaverina, I., Krylyshkina, O. and Small, J. V. (2002). Regulation of substrate adhesion dynamics during cell motility. Int. J. Biochem. Cell Biol. 34, 746-761.
19. Kiosses, W. B., Shattil, S. J., Pampori, N. and Schwartz, M. A. (2001). Rac recruits high-affinity integrin alphavbeta3 to lamellipodia in endothelial cell migration. Nat. Cell Biol. 3, 316-320.
20. Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
21. Laukaitis, C. M., Webb, D. J., Donais, K. and Horwitz, A. F. (2001). Differential dynamics of alpha 5 integrin, paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells. J. Cell Biol. 153, 1427-1440.
22. Lee, J. and Jacobson, K. (1997). The composition and dynamics of cell-substratum adhesions in locomoting fish keratocytes. J. Cell Sci. 110, 2833-2844.
23. Martin, K. H., Slack, J. K., Boerner, S. A., Martin, C. C. and Parsons, J. T. (2002). Integrin connections map: to infinity and beyond. Science 296, 1652-1653.
24. Narumiya, S., Ishizaki, T. and Uehata, M. (2000). Use and properties of ROCK-specific inhibitor Y-27632. Methods Enzymol. 325, 273-284.
25. Nix, D. A., Fradelizi, J., Bockholt, S., Menichi, B., Louvard, D., Friederich, E. and Beckerle, M. (2001). Targeting of zyxin to sites of actin membrane interaction and to the nucleus. J Biol. Chem. 276, 34759-34767.
26. Nobes, C. D. and Hall, A. (1995). Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 23, 456-459.
27. Owen, J. D., Ruest, P. J., Fry, D. W. and Hanks, S. K. (1999). Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2. Mol. Cell Biol. 19, 4806-4818.
28. Pankov, R., Cukierman, E., Katz, B. Z., Matsumoto, K., Ling D. C., Lin, S., Hahn, C. and Yamada, K. M. (2000). Integrin dynamics and matrix assembly: tensin-dependent translocation of alpha(5)beta(1) integrins promotes early fibronectin fibrillogenesis. J Cell Biol. 148, 1075-1090.
29. Petit, V. and Thiery, J. P. (2000). Focal adhesions: structure and dynamics. Biol. Cell 92, 477-494.
30. Riveline, D., Zamir, E., Balaban, N. Q., Schwarz, U. S., Ishizaki, T., Narumiya, S., Kam, Z., Geiger, B. and Bershadsky, A. D. (2001). Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153, 1175-1186.
31. Rottner, K., Behrendt, B., Small, J. V. and Wehland, J. (1999a). VASP dynamics during lamellipodia protrusion. Nat. Cell Biol. 1, 321-322.
32. Rottner, K., Hall, A. and Small, J. V. (1999b). Interplay between Rac and Rho in the control of substrate contact dynamics. Curr. Biol. 9, 640-648.
33. Rottner, K., Krause, M., Gimona, M., Small, J. V. and Wehland, J. (2001). Zyxin is not colocalized with vasodilator-stimulated phosphoprotein (VASP) at lamellipodial tips and exhibits different dynamics to vinculin, paxillin and VASP in focal adhesions. Mol. Biol. Cell 12, 3103-3113.
34. Small, J. V., Anderson, K. and Rottner, K. (1996). Actin and the coordination of protrusion, attachment and retraction in cell crawling. Biosci. Rep. 16, 351-368.
35. Stradal, T., Courtney, K. D., Rottner, K., Hahne, P., Small, J. V. and Pendergast, A. M. (2001). The Ab1 interactor proteins localize to sites of actin polymerization at the tips of lamellipodia and filopodia. Curr. Biol. 11, 891-895.
36. Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., Tamakawa, H., Yamagami, K., Inui, J., Maekawa, M. et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
37. Vasiliev, J. M. (1985). Spreading of non-transformed and transformed cells. Biochim. Biophys. Acta 780, 21-65.
38. Volberg, T., Geiger, B., Citi, S. and Bershadsky, A. (1994). Effect of protein kinase inhibitor H-7 on the contractility, integrity, and membrane anchorage of the microfilament system. Cell Motil. Cytoskel. 29, 321-338.
39. von Wichert, G., Jiang, G., Kostic, A., De Vos, K., Sap, J. and Sheetz, M. P. (2003). RPTP-alpha acts as a transducer of mechanical force on alphav/beta3-integrin-cytoskeleton linkages. J. Cell Biol. 161, 143-153.
40. Webb, D. J., Parsons, J. T. and Horwitz, A. F. (2002). Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again. Nat. Cell Biol. 4, E97-E100.
41. Zamir, E. and Geiger, B. (2001). Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci. 114, 3583-3590.
42. Zamir, E., Katz, B. Z., Aota, S., Yamada, K. M., Geiger, B. and Kam, Z. (1999). Molecular diversity of cell-matrix adhesions. J. Cell Sci. 112, 1655-1669.
43. Zamir, E., Katz, M., Posen, Y., Erez, N., Yamada, K. M., Katz, B. Z., Lin, S., Lin, D. C., Bershadsky, A., Kam, Z. et al. (2000). Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts. Nat. Cell Biol. 2, 191-196.