The role of integrin-linked kinase in the molecular architecture of focal adhesions

Journal of Cell Science

Volumn 126, Issue 18, 2013, Pages 4099-4107

  Elad, Nadav ^a,g   Volberg, Tova ^b   Patla, Israel ^a   Hirschfeld Warneken, Vera ^c,d   Grashoff, Carsten ^e   Spatz, Joachim P ^c,d   Fässler, Reinhard ^e   Geiger, Benjamin ^b   Medalia, Ohad ^a,f  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^f UNIVERSITY OF ZURICH   (Switzerland)

^g UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Cell adhesion; Correlated microscopy; Cryo electron tomography; Focal adhesion; Integrin; Integrin linked kinase

Indexed keywords

FIBRONECTIN; INTEGRIN; INTEGRIN LINKED KINASE; LIGAND;

ACTIN FILAMENT; ADHESION; ANIMAL CELL; ARTICLE; CELL MUTANT; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; EXTRACELLULAR MATRIX; FIBROBLAST; FOCAL ADHESION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; REGULATORY MECHANISM;

CELL ADHESION; CORRELATED MICROSCOPY; CRYO-ELECTRON TOMOGRAPHY; FOCAL ADHESION; INTEGRIN; INTEGRIN-LINKED KINASE;

ANIMALS; CELL ADHESION; CYTOSKELETON; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; HUMANS; MICE; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 84885463020     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.120295     Document Type: Article

References (49)

1. Arnold, M., Hirschfeld-Warneken, V. C., Lohmüller, T., Heil, P., Blümmel, J., Cavalcanti-Adam, E. A., López-García, M., Walther, P., Kessler, H., Geiger, B. et al. (2008). Induction of cell polarization and migration by a gradient of nanoscale variations in adhesive ligand spacing. Nano Lett. 8, 2063-2069.
2. Aspenström, P., Fransson, A., and Saras, J. (2004). Rho GTPases have diverse effects on the organization of the actin filament system. Biochem. J. 377, 327-337.
3. Azimifar, S. B., Böttcher, R. T., Zanivan, S., Grashoff, C., Krüger, M., Legate, K. R., Mann, M., and Fässler, R. (2012). Induction ofmembrane circular dorsal ruffles requires co-signalling of integrin-ILK-complex, and EGF receptor. J. Cell Sci. 125, 435-448.
4. Blümmel, J., Perschmann, N., Aydin, D., Drinjakovic, J., Surrey, T., Lopez-Garcia, M., Kessler, H., and Spatz, J. P. (2007). Protein repellent properties of covalently attached PEG coatings on nanostructured SiO(2)-based interfaces. Biomaterials 28, 4739-4747.
5. Burridge, K., Fath, K., Kelly, T., Nuckolls, G., and Turner, C. (1988). Focal adhesions: transmembrane junctions between the extracellular matrix, and the cytoskeleton. Annu. Rev. Cell Biol. 4, 487-525.
6. Byron, A., Humphries, J. D., Bass, M. D., Knight, D., and Humphries, M. J. (2011). Proteomic analysis of integrin adhesion complexes. Sci. Signal. 4, pt2.
7. Byron, A., Humphries, J. D., Craig, S. E., Knight, D., and Humphries, M. J. (2012). Proteomic analysis of a4b1 integrin adhesion complexes reveals a-subunit-dependent protein recruitment. Proteomics 12, 2107-2114.
8. Campbell, I. D. (2008). Studies of focal adhesion assembly. Biochem. Soc. Trans. 36, 263-266.
9. Cavalcanti-Adam, E. A., Volberg, T., Micoulet, A., Kessler, H., Geiger, B., and Spatz, J. P. (2007). Cell spreading, and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys. J. 92, 2964-2974.
10. Choi, C. K., Vicente-Manzanares, M., Zareno, J., Whitmore, L. A., Mogilner, A., and Horwitz, A. R. (2008). Actin, and alpha-actinin orchestrate the assembly, and maturation of nascent adhesions in a myosin II motor-independent manner. Nat. Cell Biol. 10, 1039-1050.
11. Dubochet, J., Adrian, M., Chang, J. J., Homo, J. C., Lepault, J., McDowall, A. W., and Schultz, P. (1988). Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21, 129-228.
12. Efimov, A., and Kaverina, I. (2009). Significance of microtubule catastrophes at focal adhesion sites. Cell Adh. Migr. 3, 285-287.
13. Frangakis, A. S., and Hegerl, R. (2001). Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J. Struct. Biol. 135, 239-250.
14. Fridman, K., Mader, A., Zwerger, M., Elia, N., and Medalia, O. (2012). Advances in tomography: probing the molecular architecture of cells. Nat. Rev. Mol. Cell Biol. 13, 736-742.
15. Geiger, B., and Yamada, K. M. (2011). Molecular architecture, and function of matrix adhesions. Cold Spring Harb. Perspect. Biol. 3, a005033.
16. Geiger, B., Spatz, J. P., and Bershadsky, A. D. (2009). Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10, 21-33.
17. Hannigan, G. E., Leung-Hagesteijn, C., Fitz-Gibbon, L., Coppolino, M.G., Radeva, G., Filmus, J., Bell, J. C., and Dedhar, S. (1996). Regulation of cell adhesion, and anchoragedependent growth by a new beta 1-integrin-linked protein kinase. Nature 379, 91-96.
18. Kanchanawong, P., Shtengel, G., Pasapera, A. M., Ramko, E. B., Davidson, M. W., Hess, H. F., and Waterman, C. M. (2010). Nanoscale architecture of integrin-based cell adhesions. Nature 468, 580-584.
19. Klotzsch, E., Smith, M. L., Kubow, K. E., Muntwyler, S., Little, W. C., Beyeler, F., Gourdon, D., Nelson, B. J., and Vogel, V. (2009). Fibronectin forms the most extensible biological fibers displaying switchable force-exposed cryptic binding sites. Proc. Natl. Acad. Sci. USA 106, 18267-18272.
20. Kuo, J. C., Han, X., Hsiao, C. T., Yates, J. R., III, and Waterman, C. M. (2011). Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for b-Pix in negative regulation of focal adhesion maturation. Nat. Cell Biol. 13, 383-393.
21. Legate, K. R., Montañez, E., Kudlacek, O., and Fässler, R. (2006). ILK, PINCH, and parvin: the tIPP of integrin signalling. Nat. Rev. Mol. Cell Biol. 7, 20-31.
22. Legate, K. R., Wickström, S. A., and Fässler, R. (2009). Genetic, and cell biological analysis of integrin outside-in signaling. Genes Dev. 23, 397-418.
23. Montanez, E., Wickström, S. A., Altstätter, J., Chu, H., and Fässler, R. (2009). Alpha-parvin controls vascular mural cell recruitment to vessel wall by regulating RhoA/ROCK signalling. EMBO J. 28, 3132-3144.
24. Nickell, S., Förster, F., Linaroudis, A., Net, W. D., Beck, F., Hegerl, R., Baumeister, W., and Plitzko, J. M. (2005). TOM software toolbox: acquisition, and analysis for electron tomography. J. Struct. Biol. 149, 227-234.
25. Nikolopoulos, S. N., and Turner, C. E. (2001). Integrin-linked kinase (ILK) binding to paxillin LD1 motif regulates ILK localization to focal adhesions. J. Biol. Chem. 276, 23499-23505.
26. Pankov, R., Cukierman, E., Katz, B. Z., Matsumoto, K., Lin, D. C., Lin, S., Hahn, C., and Yamada, K. M. (2000). Integrin dynamics, and matrix assembly: tensindependent translocation of alpha(5)beta(1) integrins promotes early fibronectin fibrillogenesis. J. Cell Biol. 148, 1075-1090.
27. Patla, I., Volberg, T., Elad, N., Hirschfeld-Warneken, V., Grashoff, C., Fässler, R., Spatz, J. P., Geiger, B., and Medalia, O. (2010). Dissecting the molecular architecture of integrin adhesion sites by cryo-electron tomography. Nat. Cell Biol. 12, 909-915.
28. Sakai, T., Li, S., Docheva, D., Grashoff, C., Sakai, K., Kostka, G., Braun, A., Pfeifer, A., Yurchenco, P. D., and Fässler, R. (2003). Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion,, and controlling actin accumulation. Genes Dev. 17, 926-940.
29. Sayedyahossein, S., Nini, L., Irvine, T. S., andDagnino, L. (2012). Essential role of integrinlinked kinase in regulation of phagocytosis in keratinocytes. FASEB J. 26, 4218-4229.
30. Schiller, H. B., Friedel, C. C., Boulegue, C., and Fässler, R. (2011). Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins. EMBO Rep. 12, 259-266.
31. Stanchi, F., Grashoff, C., Nguemeni Yonga, C. F., Grall, D., Fässler, R., and Van Obberghen-Schilling, E. (2009). Molecular dissection of the ILK-PINCH-parvin triad reveals a fundamental role for the ILK kinase domain in the late stages of focaladhesion maturation. J. Cell Sci. 122, 1800-1811.
32. Torgler, C. N., Narasimha, M., Knox, A. L., Zervas, C. G., Vernon, M. C., and Brown, N. H. (2004). Tensin stabilizes integrin adhesive contacts in Drosophila. Dev. Cell 6, 357-369.
33. Ulmer, J., Spatz, J. P., and Geiger, B. (2008). Force-induced fibronectin fibrillogenesis in vivo. Soft Matter 4, 1998-2007.
34. Vakaloglou, K., and Zervas, C. (2012). Parvin-ILK: An intimate relationship. BioArchitecture 2, 91-94.
35. Vicente-Manzanares, M., and Horwitz, A. R. (2011). Adhesion dynamics at a glance. J. Cell Sci. 124, 3923-3927.
36. Vicente-Manzanares, M., Choi, C. K., and Horwitz, A. R. (2009). Integrins in cell migration -the actin connection. J. Cell Sci. 122, 199-206.
37. Vicente-Manzanares, M., Newell-Litwa, K., Bachir, A. I., Whitmore, L. A., and Horwitz, A. R. (2011). Myosin IIA/IIB restrict adhesive, and protrusive signaling to generate front-back polarity in migrating cells. J. Cell Biol. 193, 381-396.
38. Volberg, T., Romer, L., Zamir, E., and Geiger, B. (2001). pp60(c-src), and related tyrosine kinases: a role in the assembly, and reorganization of matrix adhesions. J. Cell Sci. 114, 2279-2289.
39. Vouret-Craviari, V., Boulter, E., Grall, D., Matthews, C., and Van Obberghen-Schilling, E. (2004). ILK is required for the assembly of matrix-forming adhesions, and capillary morphogenesis in endothelial cells. J. Cell Sci. 117, 4559-4569.
40. Wang, H. V., Chang, L. W., Brixius, K., Wickström, S. A., Montanez, E., Thievessen, I., Schwander, M., Müller, U., Bloch, W., Mayer, U. et al. (2008). Integrin-linked kinase stabilizes myotendinous junctions, and protects muscle from stress-induced damage. J. Cell Biol. 180, 1037-1049.
41. Wickström, S. A., and Fässler, R. (2011). Regulation of membrane traffic by integrin signaling. Trends Cell Biol. 21, 266-273.
42. Wickström, S. A., Lange, A., Hess, M. W., Polleux, J., Spatz, J. P., Krüger, M., Pfaller, K., Lambacher, A., Bloch, W., Mann, M. et al. (2010). Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae. Dev. Cell 19, 574-588.
43. Winograd-Katz, S. E., Itzkovitz, S., Kam, Z., and Geiger, B. (2009). Multiparametric analysis of focal adhesion formation by RNAi-mediated gene knockdown. J. Cell Biol. 186, 423-436.
44. Zaidel-Bar, R., Cohen, M., Addadi, L., and Geiger, B. (2004). Hierarchical assembly of cell-matrix adhesion complexes. Biochem. Soc. Trans. 32, 416-420.
45. Zaidel-Bar, R., Itzkovitz, S., Ma'ayan, A., Iyengar, R., and Geiger, B. (2007a). Functional atlas of the integrin adhesome. Nat. Cell Biol. 9, 858-867.
46. Zaidel-Bar, R., Milo, R., Kam, Z., and Geiger, B. (2007b). A paxillin tyrosine phosphorylation switch regulates the assembly, and form of cell-matrix adhesions. J. Cell Sci. 120, 137-148.
47. 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.
48. 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 cellmatrix adhesions in cultured fibroblasts. Nat. Cell Biol. 2, 191-196.
49. Zervas, C. G., Psarra, E., Williams, V., Solomon, E., Vakaloglou, K. M., and Brown, N. H. (2011). A central multifunctional role of integrin-linked kinase at muscle attachment sites. J. Cell Sci. 124, 1316-1327.