Integrin cytoplasmic tail interactions

Biochemistry

Volumn 53, Issue 5, 2014, Pages 810-820

  Morse, Elizabeth M ^a   Brahme, Nina N ^a   Calderwood, David A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CYTOPLASM; CYTOSKELETON; HUMANS; INTEGRINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MECHANOTRANSDUCTION, CELLULAR; SIGNAL TRANSDUCTION;

EID: 84894181114     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401596q     Document Type: Review

References (129)

1. Harburger, D. S. and Calderwood, D. A. (2009) Integrin signalling at a glance J. Cell Sci. 122, 159-163
2. Fu, G., Wang, W., and Luo, B. H. (2012) Overview: Structural biology of integrins Methods Mol. Biol. 757, 81-99
3. Zhu, J., Zhu, J., and Springer, T. A. (2013) Complete integrin headpiece opening in eight steps J. Cell Biol. 201, 1053-1068
4. Kim, C., Ye, F., Hu, X., and Ginsberg, M. H. (2012) Talin activates integrins by altering the topology of the β transmembrane domain J. Cell Biol. 197, 605-611
5. Legate, K. R. and Fassler, R. (2009) Mechanisms that regulate adaptor binding to β-integrin cytoplasmic tails J. Cell Sci. 122, 187-198
6. Calderwood, D. A. (2004) Integrin activation J. Cell Sci. 117, 657-666
7. Vinogradova, O., Velyvis, A., Velyviene, A., Hu, B., Haas, T., Plow, E., and Qin, J. (2002) A structural mechanism of integrin αIIbβ3 "inside-out" activation as regulated by its cytoplasmic face Cell 110, 587-597
8. Bhunia, A., Tang, X. Y., Mohanram, H., Tan, S. M., and Bhattacharjya, S. (2009) NMR solution conformations and interactions of integrin αLβ2 cytoplasmic tails J. Biol. Chem. 284, 3873-3884
9. Metcalf, D. G., Moore, D. T., Wu, Y., Kielec, J. M., Molnar, K., Valentine, K. G., Wand, A. J., Bennett, J. S., and DeGrado, W. F. (2010) NMR analysis of the αIIbβ3 cytoplasmic interaction suggests a mechanism for integrin regulation Proc. Natl. Acad. Sci. U.S.A. 107, 22481-22486
10. Garcia-Alvarez, B., de Pereda, J. M., Calderwood, D. A., Ulmer, T. S., Critchley, D., Campbell, I. D., Ginsberg, M. H., and Liddington, R. C. (2003) Structural determinants of integrin recognition by talin Mol. Cell 11, 49-58
11. Kiema, T., Lad, Y., Jiang, P., Oxley, C. L., Baldassarre, M., Wegener, K. L., Campbell, I. D., Ylanne, J., and Calderwood, D. A. (2006) The molecular basis of filamin binding to integrins and competition with talin Mol. Cell 21, 337-347
12. Liu, S., Calderwood, D. A., and Ginsberg, M. H. (2000) Integrin cytoplasmic domain-binding proteins J. Cell Sci. 113 (Part 20) 3563-3571
13. Geiger, T. and Zaidel-Bar, R. (2012) Opening the floodgates: Proteomics and the integrin adhesome Curr. Opin. Cell Biol. 24, 562-568
14. Gahmberg, C. G., Fagerholm, S. C., Nurmi, S. M., Chavakis, T., Marchesan, S., and Gronholm, M. (2009) Regulation of integrin activity and signalling Biochim. Biophys. Acta 1790, 431-444
15. Calderwood, D. A., Campbell, I. D., and Critchley, D. R. (2013) Talins and kindlins: Partners in integrin-mediated adhesion Nat. Rev. Mol. Cell Biol. 14, 503-517
16. Anthis, N. J., Haling, J. R., Oxley, C. L., Memo, M., Wegener, K. L., Lim, C. J., Ginsberg, M. H., and Campbell, I. D. (2009) β integrin tyrosine phosphorylation is a conserved mechanism for regulating talin-induced integrin activation J. Biol. Chem. 284, 36700-36710
17. Xi, X., Flevaris, P., Stojanovic, A., Chishti, A., Phillips, D. R., Lam, S. C., and Du, X. (2006) Tyrosine phosphorylation of the integrin β3 subunit regulates β3 cleavage by calpain J. Biol. Chem. 281, 29426-29430
18. Takala, H., Nurminen, E., Nurmi, S. M., Aatonen, M., Strandin, T., Takatalo, M., Kiema, T., Gahmberg, C. G., Ylanne, J., and Fagerholm, S. C. (2008) β2 integrin phosphorylation on Thr758 acts as a molecular switch to regulate 14-3-3 and filamin binding Blood 112, 1853-1862
19. Tadokoro, S., Shattil, S. J., Eto, K., Tai, V., Liddington, R. C., de Pereda, J. M., Ginsberg, M. H., and Calderwood, D. A. (2003) Talin binding to integrin β tails: A final common step in integrin activation Science 302, 103-106
20. Shattil, S. J., Kim, C., and Ginsberg, M. H. (2010) The final steps of integrin activation: The end game Nat. Rev. Mol. Cell Biol. 11, 288-300
21. Ye, F., Kim, C., and Ginsberg, M. H. (2011) Molecular mechanism of inside-out integrin regulation J. Thromb. Haemostasis 9 (Suppl. 1) 20-25
22. Ye, F., Hu, G., Taylor, D., Ratnikov, B., Bobkov, A. A., McLean, M. A., Sligar, S. G., Taylor, K. A., and Ginsberg, M. H. (2010) Recreation of the terminal events in physiological integrin activation J. Cell Biol. 188, 157-173
23. Calderwood, D. A., Fujioka, Y., de Pereda, J. M., Garcia-Alvarez, B., Nakamoto, T., Margolis, B., McGlade, C. J., Liddington, R. C., and Ginsberg, M. H. (2003) Integrin β cytoplasmic domain interactions with phosphotyrosine-binding domains: A structural prototype for diversity in integrin signaling Proc. Natl. Acad. Sci. U.S.A. 100, 2272-2277
24. Goult, B. T., Bouaouina, M., Elliott, P. R., Bate, N., Patel, B., Gingras, A. R., Grossmann, J. G., Roberts, G. C., Calderwood, D. A., Critchley, D. R., and Barsukov, I. L. (2010) Structure of a double ubiquitin-like domain in the talin head: A role in integrin activation EMBO J. 29, 1069-1080
25. Moore, D. T., Nygren, P., Jo, H., Boesze-Battaglia, K., Bennett, J. S., and DeGrado, W. F. (2012) Affinity of talin-1 for the β3-integrin cytosolic domain is modulated by its phospholipid bilayer environment Proc. Natl. Acad. Sci. U.S.A. 109, 793-798
26. Goult, B. T., Zacharchenko, T., Bate, N., Tsang, R., Hey, F., Gingras, A. R., Elliott, P. R., Roberts, G. C., Ballestrem, C., Critchley, D. R., and Barsukov, I. L. (2013) RIAM and vinculin binding to talin are mutually exclusive and regulate adhesion assembly and turnover J. Biol. Chem. 288, 8238-8249
27. Lee, H. S., Anekal, P., Lim, C. J., Liu, C. C., and Ginsberg, M. H. (2013) Two modes of integrin activation form a binary molecular switch in adhesion maturation Mol. Biol. Cell 24, 1354-1362
28. Goksoy, E., Ma, Y. Q., Wang, X., Kong, X., Perera, D., Plow, E. F., and Qin, J. (2008) Structural basis for the autoinhibition of talin in regulating integrin activation Mol. Cell 31, 124-133
29. Song, X., Yang, J., Hirbawi, J., Ye, S., Perera, H. D., Goksoy, E., Dwivedi, P., Plow, E. F., Zhang, R., and Qin, J. (2012) A novel membrane-dependent on/off switch mechanism of talin FERM domain at sites of cell adhesion Cell Res. 22, 1533-1545
30. Goult, B. T., Bate, N., Anthis, N. J., Wegener, K. L., Gingras, A. R., Patel, B., Barsukov, I. L., Campbell, I. D., Roberts, G. C., and Critchley, D. R. (2009) The structure of an interdomain complex that regulates talin activity J. Biol. Chem. 284, 15097-15106
31. Elliott, P. R., Goult, B. T., Kopp, P. M., Bate, N., Grossmann, J. G., Roberts, G. C., Critchley, D. R., and Barsukov, I. L. (2010) The structure of the talin head reveals a novel extended conformation of the FERM domain Structure 18, 1289-1299
32. Huang, C., Rajfur, Z., Yousefi, N., Chen, Z., Jacobson, K., and Ginsberg, M. H. (2009) Talin phosphorylation by Cdk5 regulates Smurf1-mediated talin head ubiquitylation and cell migration Nat. Cell Biol. 11, 624-630
33. Brahme, N. N. and Calderwood, D. A. (2012) Cell adhesion: A FERM grasp of the tail sorts out integrins Curr. Biol. 22, R692-R694
34. Karakose, E., Schiller, H. B., and Fassler, R. (2010) The kindlins at a glance J. Cell Sci. 123, 2353-2356
35. Larjava, H., Plow, E. F., and Wu, C. (2008) Kindlins: Essential regulators of integrin signalling and cell-matrix adhesion EMBO Rep. 9, 1203-1208
36. Bandyopadhyay, A., Rothschild, G., Kim, S., Calderwood, D. A., and Raghavan, S. (2012) Functional differences between kindlin-1 and kindlin-2 in keratinocytes J. Cell Sci. 125, 2172-2184
37. Herz, C., Aumailley, M., Schulte, C., Schlotzer-Schrehardt, U., Bruckner-Tuderman, L., and Has, C. (2006) Kindlin-1 is a phosphoprotein involved in regulation of polarity, proliferation, and motility of epidermal keratinocytes J. Biol. Chem. 281, 36082-36090
38. Tu, Y., Wu, S., Shi, X., Chen, K., and Wu, C. (2003) Migfilin and Mig-2 link focal adhesions to filamin and the actin cytoskeleton and function in cell shape modulation Cell 113, 37-47
39. Brahme, N. N., Harburger, D. S., Kemp O'Brien, K., Stewart, R., Raghavan, S., Parsons, M., and Calderwood, D. A. (2013) Kindlin binds migfilin tandem LIM domains and regulates migfilin focal adhesion localization and recruitment dynamics J. Biol. Chem. 288, 35604-35616
40. Das, M., Ithychanda, S. S., Qin, J., and Plow, E. F. (2011) Migfilin and filamin as regulators of integrin activation in endothelial cells and neutrophils PLoS One 6, e26355
41. Ithychanda, S. S., Das, M., Ma, Y. Q., Ding, K., Wang, X., Gupta, S., Wu, C., Plow, E. F., and Qin, J. (2009) Migfilin, a molecular switch in regulation of integrin activation J. Biol. Chem. 284, 4713-4722
42. Lad, Y., Jiang, P., Ruskamo, S., Harburger, D. S., Ylanne, J., Campbell, I. D., and Calderwood, D. A. (2008) Structural basis of the migfilin-filamin interaction and competition with integrin β tails J. Biol. Chem. 283, 35154-35163
43. 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 anchorage-dependent growth by a new β1-integrin-linked protein kinase Nature 379, 91-96
44. Honda, S., Shirotani-Ikejima, H., Tadokoro, S., Maeda, Y., Kinoshita, T., Tomiyama, Y., and Miyata, T. (2009) Integrin-linked kinase associated with integrin activation Blood 113, 5304-5313
45. Tucker, K. L., Sage, T., Stevens, J. M., Jordan, P. A., Jones, S., Barrett, N. E., St-Arnaud, R., Frampton, J., Dedhar, S., and Gibbins, J. M. (2008) A dual role for integrin-linked kinase in platelets: Regulating integrin function and α-granule secretion Blood 112, 4523-4531
46. Ye, F., Petrich, B. G., Anekal, P., Lefort, C. T., Kasirer-Friede, A., Shattil, S. J., Ruppert, R., Moser, M., Fassler, R., and Ginsberg, M. H. (2013) The mechanism of kindlin-mediated activation of integrin αIIbβ3 Curr. Biol. 23, 2288-2295
47. Saltel, F., Mortier, E., Hytonen, V. P., Jacquier, M. C., Zimmermann, P., Vogel, V., Liu, W., and Wehrle-Haller, B. (2009) New PI(4,5)P2- and membrane proximal integrin-binding motifs in the talin head control β3-integrin clustering J. Cell Biol. 187, 715-731
48. Feigelson, S. W., Grabovsky, V., Manevich-Mendelson, E., Pasvolsky, R., Shulman, Z., Shinder, V., Klein, E., Etzioni, A., Aker, M., and Alon, R. (2011) Kindlin-3 is required for the stabilization of TCR-stimulated LFA-1:ICAM-1 bonds critical for lymphocyte arrest and spreading on dendritic cells Blood 117, 7042-7052
49. Wang, H. V., Chang, L. W., Brixius, K., Wickstrom, S. A., Montanez, E., Thievessen, I., Schwander, M., Muller, U., Bloch, W., Mayer, U., and Fassler, R. (2008) Integrin-linked kinase stabilizes myotendinous junctions and protects muscle from stress-induced damage J. Cell Biol. 180, 1037-1049
50. Katagiri, K., Maeda, A., Shimonaka, M., and Kinashi, T. (2003) RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1 Nat. Immunol. 4, 741-748
51. Ohmori, T., Kashiwakura, Y., Ishiwata, A., Madoiwa, S., Mimuro, J., Honda, S., Miyata, T., and Sakata, Y. (2010) Vinculin activates inside-out signaling of integrin αIIbβ3 in Chinese hamster ovary cells Biochem. Biophys. Res. Commun. 400, 323-328
52. Bouaouina, M., Jani, K., Long, J. Y., Czerniecki, S., Morse, E. M., Ellis, S. J., Tanentzapf, G., Schock, F., and Calderwood, D. A. (2012) Zasp regulates integrin activation J. Cell Sci. 125, 5647-5657
53. Bouvard, D., Pouwels, J., De Franceschi, N., and Ivaska, J. (2013) Integrin inactivators: Balancing cellular functions in vitro and in vivo Nat. Rev. Mol. Cell Biol. 14, 430-442
54. Pouwels, J., Nevo, J., Pellinen, T., Ylanne, J., and Ivaska, J. (2012) Negative regulators of integrin activity J. Cell Sci. 125, 3271-3280
55. Baldassarre, M., Razinia, Z., Burande, C. F., Lamsoul, I., Lutz, P. G., and Calderwood, D. A. (2009) Filamins regulate cell spreading and initiation of cell migration PLoS One 4, e7830
56. Chen, H. S., Kolahi, K. S., and Mofrad, M. R. (2009) Phosphorylation facilitates the integrin binding of filamin under force Biophys. J. 97, 3095-3104
57. Chen, H., Zou, Z., Sarratt, K. L., Zhou, D., Zhang, M., Sebzda, E., Hammer, D. A., and Kahn, M. L. (2006) In vivo β1 integrin function requires phosphorylation-independent regulation by cytoplasmic tyrosines Genes Dev. 20, 927-932
58. Czuchra, A., Meyer, H., Legate, K. R., Brakebusch, C., and Fassler, R. (2006) Genetic analysis of β1 integrin "activation motifs" in mice J. Cell Biol. 174, 889-899
59. Meves, A., Geiger, T., Zanivan, S., DiGiovanni, J., Mann, M., and Fassler, R. (2011) β1 integrin cytoplasmic tyrosines promote skin tumorigenesis independent of their phosphorylation Proc. Natl. Acad. Sci. U.S.A. 108, 15213-15218
60. Liu, W., Draheim, K. M., Zhang, R., Calderwood, D. A., and Boggon, T. J. (2013) Mechanism for KRIT1 release of ICAP1-mediated suppression of integrin activation Mol. Cell 49, 719-729
61. Millon-Fremillon, A., Brunner, M., Abed, N., Collomb, E., Ribba, A. S., Block, M. R., Albiges-Rizo, C., and Bouvard, D. (2013) Calcium and calmodulin-dependent serine/threonine protein kinase type II (CaMKII)-mediated intramolecular opening of integrin cytoplasmic domain-associated protein-1 (ICAP-1α) negatively regulates β1 integrins J. Biol. Chem. 288, 20248-20260
62. Roca-Cusachs, P., del Rio, A., Puklin-Faucher, E., Gauthier, N. C., Biais, N., and Sheetz, M. P. (2013) Integrin-dependent force transmission to the extracellular matrix by α-actinin triggers adhesion maturation Proc. Natl. Acad. Sci. U.S.A. 110, E1361-E1370
63. Tadokoro, S., Nakazawa, T., Kamae, T., Kiyomizu, K., Kashiwagi, H., Honda, S., Kanakura, Y., and Tomiyama, Y. (2011) A potential role for α-actinin in inside-out αIIbβ3 signaling Blood 117, 250-258
64. Bridgewater, R. E., Norman, J. C., and Caswell, P. T. (2012) Integrin trafficking at a glance J. Cell Sci. 125, 3695-3701
65. Onodera, Y., Nam, J. M., and Sabe, H. (2013) Intracellular trafficking of integrins in cancer cells Pharmacol. Ther. 140, 1-9
66. Ezratty, E. J., Bertaux, C., Marcantonio, E. E., and Gundersen, G. G. (2009) Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells J. Cell Biol. 187, 733-747
67. Lee, M., Skoura, A., Park, E., Landskroner-Eiger, S., Jozsef, L., Luciano, A., Murata, T., Pasula, S., Dong, Y., Bouaouina, M., Calderwood, D. A., Ferguson, S. M., De Camilli, P., and Sessa, W. C. (2014) Dynamin-2 regulation of integrin endocytosis, but not VEGF signaling, is critical for developmental angiogenesis Development in press
68. Chao, W. T. and Kunz, J. (2009) Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins FEBS Lett. 583, 1337-1343
69. Nishimura, T. and Kaibuchi, K. (2007) Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3 Dev. Cell 13, 15-28
70. Bogdanovic, O., Delfino-Machin, M., Nicolas-Perez, M., Gavilan, M. P., Gago-Rodrigues, I., Fernandez-Minan, A., Lillo, C., Rios, R. M., Wittbrodt, J., and Martinez-Morales, J. R. (2012) Numb/Numbl-Opo antagonism controls retinal epithelium morphogenesis by regulating integrin endocytosis Dev. Cell 23, 782-795
71. Pellinen, T., Tuomi, S., Arjonen, A., Wolf, M., Edgren, H., Meyer, H., Grosse, R., Kitzing, T., Rantala, J. K., Kallioniemi, O., Fassler, R., Kallio, M., and Ivaska, J. (2008) Integrin trafficking regulated by Rab21 is necessary for cytokinesis Dev. Cell 15, 371-385
72. Pellinen, T., Arjonen, A., Vuoriluoto, K., Kallio, K., Fransen, J. A., and Ivaska, J. (2006) Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of β1-integrins J. Cell Biol. 173, 767-780
73. Roberts, M., Barry, S., Woods, A., van der Sluijs, P., and Norman, J. (2001) PDGF-regulated rab4-dependent recycling of αvβ3 integrin from early endosomes is necessary for cell adhesion and spreading Curr. Biol. 11, 1392-1402
74. Woods, A. J., White, D. P., Caswell, P. T., and Norman, J. C. (2004) PKD1/PKCmu promotes αvβ3 integrin recycling and delivery to nascent focal adhesions EMBO J. 23, 2531-2543
75. White, D. P., Caswell, P. T., and Norman, J. C. (2007) αvβ3 and α5β1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration J. Cell Biol. 177, 515-525
76. Medeiros, R. B., Dickey, D. M., Chung, H., Quale, A. C., Nagarajan, L. R., Billadeau, D. D., and Shimizu, Y. (2005) Protein kinase D1 and the β1 integrin cytoplasmic domain control β1 integrin function via regulation of Rap1 activation Immunity 23, 213-226
77. Caswell, P. T., Spence, H. J., Parsons, M., White, D. P., Clark, K., Cheng, K. W., Mills, G. B., Humphries, M. J., Messent, A. J., Anderson, K. I., McCaffrey, M. W., Ozanne, B. W., and Norman, J. C. (2007) Rab25 associates with α5β1 integrin to promote invasive migration in 3D microenvironments Dev. Cell 13, 496-510
78. Dozynkiewicz, M. A., Jamieson, N. B., Macpherson, I., Grindlay, J., van den Berghe, P. V., von Thun, A., Morton, J. P., Gourley, C., Timpson, P., Nixon, C., McKay, C. J., Carter, R., Strachan, D., Anderson, K., Sansom, O. J., Caswell, P. T., and Norman, J. C. (2012) Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression Dev. Cell 22, 131-145
79. Mai, A., Veltel, S., Pellinen, T., Padzik, A., Coffey, E., Marjomaki, V., and Ivaska, J. (2011) Competitive binding of Rab21 and p120RasGAP to integrins regulates receptor traffic and migration J. Cell Biol. 194, 291-306
80. Margadant, C., Kreft, M., de Groot, D. J., Norman, J. C., and Sonnenberg, A. (2012) Distinct roles of talin and kindlin in regulating integrin α5β1 function and trafficking Curr. Biol. 22, 1554-1563
81. Steinberg, F., Heesom, K. J., Bass, M. D., and Cullen, P. J. (2012) SNX17 protects integrins from degradation by sorting between lysosomal and recycling pathways J. Cell Biol. 197, 219-230
82. Bottcher, R. T., Stremmel, C., Meves, A., Meyer, H., Widmaier, M., Tseng, H. Y., and Fassler, R. (2012) Sorting nexin 17 prevents lysosomal degradation of β1 integrins by binding to the β1-integrin tail Nat. Cell Biol. 14, 584-592
83. Hoffman, B. D., Grashoff, C., and Schwartz, M. A. (2011) Dynamic molecular processes mediate cellular mechanotransduction Nature 475, 316-323
84. Legate, K. R., Wickstrom, S. A., and Fassler, R. (2009) Genetic and cell biological analysis of integrin outside-in signaling Genes Dev. 23, 397-418
85. Schiller, H. B. and Fassler, R. (2013) Mechanosensitivity and compositional dynamics of cell-matrix adhesions EMBO Rep. 14, 509-519
86. Gingras, A. R., Bate, N., Goult, B. T., Hazelwood, L., Canestrelli, I., Grossmann, J. G., Liu, H., Putz, N. S., Roberts, G. C., Volkmann, N., Hanein, D., Barsukov, I. L., and Critchley, D. R. (2008) The structure of the C-terminal actin-binding domain of talin EMBO J. 27, 458-469
87. del Rio, A., Perez-Jimenez, R., Liu, R., Roca-Cusachs, P., Fernandez, J. M., and Sheetz, M. P. (2009) Stretching single talin rod molecules activates vinculin binding Science 323, 638-641
88. Margadant, F., Chew, L. L., Hu, X., Yu, H., Bate, N., Zhang, X., and Sheetz, M. (2011) Mechanotransduction in vivo by repeated talin stretch-relaxation events depends upon vinculin PLoS Biol. 9, e1001223
89. Giannone, G., Jiang, G., Sutton, D. H., Critchley, D. R., and Sheetz, M. P. (2003) Talin1 is critical for force-dependent reinforcement of initial integrin-cytoskeleton bonds but not tyrosine kinase activation J. Cell Biol. 163, 409-419
90. Carisey, A., Tsang, R., Greiner, A. M., Nijenhuis, N., Heath, N., Nazgiewicz, A., Kemkemer, R., Derby, B., Spatz, J., and Ballestrem, C. (2013) Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner Curr. Biol. 23, 271-281
91. Razinia, Z., Makela, T., Ylanne, J., and Calderwood, D. A. (2012) Filamins in mechanosensing and signaling Annu. Rev. Biophys. 41, 227-246
92. Lad, Y., Kiema, T., Jiang, P., Pentikainen, O. T., Coles, C. H., Campbell, I. D., Calderwood, D. A., and Ylanne, J. (2007) Structure of three tandem filamin domains reveals auto-inhibition of ligand binding EMBO J. 26, 3993-4004
93. Rognoni, L., Stigler, J., Pelz, B., Ylanne, J., and Rief, M. (2012) Dynamic force sensing of filamin revealed in single-molecule experiments Proc. Natl. Acad. Sci. U.S.A. 109, 19679-19684
94. Ehrlicher, A. J., Nakamura, F., Hartwig, J. H., Weitz, D. A., and Stossel, T. P. (2011) Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A Nature 478, 260-263
95. Reinhard, M., Zumbrunn, J., Jaquemar, D., Kuhn, M., Walter, U., and Trueb, B. (1999) An α-actinin binding site of zyxin is essential for subcellular zyxin localization and α-actinin recruitment J. Biol. Chem. 274, 13410-13418
96. Hoffman, L. M., Jensen, C. C., Chaturvedi, A., Yoshigi, M., and Beckerle, M. C. (2012) Stretch-induced actin remodeling requires targeting of zyxin to stress fibers and recruitment of actin regulators Mol. Biol. Cell 23, 1846-1859
97. Yoshigi, M., Hoffman, L. M., Jensen, C. C., Yost, H. J., and Beckerle, M. C. (2005) Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement J. Cell Biol. 171, 209-215
98. Lo, S. H. (2004) Tensin Int. J. Biochem. Cell Biol. 36, 31-34
99. Mouneimne, G. and Brugge, J. S. (2007) Tensins: A new switch in cell migration Dev. Cell 13, 317-319
100. Grashoff, C., Hoffman, B. D., Brenner, M. D., Zhou, R., Parsons, M., Yang, M. T., McLean, M. A., Sligar, S. G., Chen, C. S., Ha, T., and Schwartz, M. A. (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics Nature 466, 263-266
101. Hu, K., Ji, L., Applegate, K. T., Danuser, G., and Waterman-Storer, C. M. (2007) Differential transmission of actin motion within focal adhesions Science 315, 111-115
102. Dumbauld, D. W., Lee, T. T., Singh, A., Scrimgeour, J., Gersbach, C. A., Zamir, E. A., Fu, J., Chen, C. S., Curtis, J. E., Craig, S. W., and Garcia, A. J. (2013) How vinculin regulates force transmission Proc. Natl. Acad. Sci. U.S.A. 110, 9788-9793
103. Shams, H., Golji, J., and Mofrad, M. R. (2012) A molecular trajectory of α-actinin activation Biophys. J. 103, 2050-2059
104. Ghatak, S., Morgner, J., and Wickstrom, S. A. (2013) ILK: A pseudokinase with a unique function in the integrin-actin linkage Biochem. Soc. Trans. 41, 995-1001
105. Qin, J. and Wu, C. (2012) ILK: A pseudokinase in the center stage of cell-matrix adhesion and signaling Curr. Opin. Cell Biol. 24, 607-613
106. Grashoff, C., Aszodi, A., Sakai, T., Hunziker, E. B., and Fassler, R. (2003) Integrin-linked kinase regulates chondrocyte shape and proliferation EMBO Rep. 4, 432-438
107. Akhtar, N. and Streuli, C. H. (2013) An integrin-ILK-microtubule network orients cell polarity and lumen formation in glandular epithelium Nat. Cell Biol. 15, 17-27
108. Wickstrom, S. A., Lange, A., Hess, M. W., Polleux, J., Spatz, J. P., Kruger, M., Pfaller, K., Lambacher, A., Bloch, W., Mann, M., Huber, L. A., and Fassler, R. (2010) Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae Dev. Cell 19, 574-588
109. Nayak, R. C., Chang, K. H., Vaitinadin, N. S., and Cancelas, J. A. (2013) Rho GTPases control specific cytoskeleton-dependent functions of hematopoietic stem cells Immunol. Rev. 256, 255-268
110. Hall, A. (2012) Rho family GTPases Biochem. Soc. Trans. 40, 1378-1382
111. Nakamura, F. (2013) FilGAP and its close relatives: A mediator of Rho-Rac antagonism that regulates cell morphology and migration Biochem. J. 453, 17-25
112. Jacquemet, G., Morgan, M. R., Byron, A., Humphries, J. D., Choi, C. K., Chen, C. S., Caswell, P. T., and Humphries, M. J. (2013) Rac1 is deactivated at integrin activation sites through an IQGAP1-filamin-A-RacGAP1 pathway J. Cell Sci. 126, 4121-4135
113. Has, C., Herz, C., Zimina, E., Qu, H. Y., He, Y., Zhang, Z. G., Wen, T. T., Gache, Y., Aumailley, M., and Bruckner-Tuderman, L. (2009) Kindlin-1 is required for RhoGTPase-mediated lamellipodia formation in keratinocytes Am. J. Pathol. 175, 1442-1452
114. Jung, G. Y., Park, Y. J., and Han, J. S. (2011) Mediation of Rac1 activation by kindlin-2: An essential function in osteoblast adhesion, spreading, and proliferation J. Cell. Biochem. 112, 2541-2548
115. Xue, Z. H., Feng, C., Liu, W. L., and Tan, S. M. (2013) A role of kindlin-3 in integrin αMβ2 outside-in signaling and the Syk-Vav1-Rac1/Cdc42 signaling axis PLoS One 8, e56911
116. Nishiya, N., Kiosses, W. B., Han, J., and Ginsberg, M. H. (2005) An α4 integrin-paxillin-Arf-GAP complex restricts Rac activation to the leading edge of migrating cells Nat. Cell Biol. 7, 343-352
117. Goldfinger, L. E., Han, J., Kiosses, W. B., Howe, A. K., and Ginsberg, M. H. (2003) Spatial restriction of α4 integrin phosphorylation regulates lamellipodial stability and α4β1-dependent cell migration J. Cell Biol. 162, 731-741
118. Mitra, S. K. and Schlaepfer, D. D. (2006) Integrin-regulated FAK-Src signaling in normal and cancer cells Curr. Opin. Cell Biol. 18, 516-523
119. Schaller, M. D., Otey, C. A., Hildebrand, J. D., and Parsons, J. T. (1995) Focal adhesion kinase and paxillin bind to peptides mimicking β integrin cytoplasmic domains J. Cell Biol. 130, 1181-1187
120. Lawson, C., Lim, S. T., Uryu, S., Chen, X. L., Calderwood, D. A., and Schlaepfer, D. D. (2012) FAK promotes recruitment of talin to nascent adhesions to control cell motility J. Cell Biol. 196, 223-232
121. Huveneers, S. and Danen, E. H. (2009) Adhesion signaling: Crosstalk between integrins, Src and Rho J. Cell Sci. 122, 1059-1069
122. 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. U.S.A. 100, 13298-13302
123. Warren, M. S., Bradley, W. D., Gourley, S. L., Lin, Y. C., Simpson, M. A., Reichardt, L. F., Greer, C. A., Taylor, J. R., and Koleske, A. J. (2012) Integrin β1 signals through Arg to regulate postnatal dendritic arborization, synapse density, and behavior J. Neurosci. 32, 2824-2834
124. Woodside, D. G., Obergfell, A., Talapatra, A., Calderwood, D. A., Shattil, S. J., and Ginsberg, M. H. (2002) The N-terminal SH2 domains of Syk and ZAP-70 mediate phosphotyrosine-independent binding to integrin β cytoplasmic domains J. Biol. Chem. 277, 39401-39408
125. Li, Z., Lock, J. G., Olofsson, H., Kowalewski, J. M., Teller, S., Liu, Y., Zhang, H., and Stromblad, S. (2010) Integrin-mediated cell attachment induces a PAK4-dependent feedback loop regulating cell adhesion through modified integrin αvβ5 clustering and turnover Mol. Biol. Cell 21, 3317-3329
126. Gushiken, F. C., Patel, V., Liu, Y., Pradhan, S., Bergeron, A. L., Peng, Y., and Vijayan, K. V. (2008) Protein phosphatase 2A negatively regulates integrin αIIbβ3 signaling J. Biol. Chem. 283, 12862-12869
127. Ivaska, J. and Heino, J. (2011) Cooperation between integrins and growth factor receptors in signaling and endocytosis Annu. Rev. Cell Dev. Biol. 27, 291-320
128. Shen, B., Delaney, M. K., and Du, X. (2012) Inside-out, outside-in, and inside-outside-in: G protein signaling in integrin-mediated cell adhesion, spreading, and retraction Curr. Opin. Cell Biol. 24, 600-606
129. Das, M., Subbayya Ithychanda, S., Qin, J., and Plow, E. F. (2014) Mechanisms of talin-dependent integrin signaling and crosstalk Biochim. Biophys. Acta 1838, 579-588