Biochemical and structural properties of the integrin-associated cytoskeletal protein talin

Annual Review of Biophysics

Volumn 38, Issue 1, 2009, Pages 235-254

  Critchley, David R ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Actin; Cytoskeleton; Focal adhesions; PIP2; Rap1; Vinculin

Indexed keywords

ACTIN; BETA3 INTEGRIN; CELL PROTEIN; INTEGRIN; LIGAND; LIPID; PHOSPHATIDYLINOSITIDE; TALIN; VINCULIN;

BINDING AFFINITY; BINDING SITE; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CELL MEMBRANE; CONFORMATIONAL TRANSITION; EXTRACELLULAR SPACE; FOCAL ADHESION; HUMAN; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; ULTRASTRUCTURE;

INTEGRINS; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; TALIN;

EID: 67650288199     PISSN: 1936122X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.biophys.050708.133744     Document Type: Review

References (113)

1. Bakolitsa C, Cohen DM, Bankston LA, Bobkov AA, Cadwell GW, et al. 2004. Structural basis for vinculin activation at sites of cell adhesion. Nature 430:583-586 (Pubitemid 38998634)
2. Barsukov IL, Prescot A, Bate N, Patel B, Floyd DN, et al. 2003. Phosphatidylinositol phosphate kinase type 1gamma and beta1-integrin cytoplasmic domain bind to the same region in the talin FERM domain. J. Biol. Chem. 278:31202-31209 (Pubitemid 36994636)
3. Bass MD, Patel B, Barsukov IG, Fillingham IJ, Mason R, et al. 2002. Further characterization of the interaction between the cytoskeletal proteins talin and vinculin. Biochem. J. 362:761-768 (Pubitemid 34242330)
4. Bass MD, Smith BJ, Prigent SA, Critchley DR. 1999. Talin contains three similar vinculin-binding sites predicted to form an amphipathic helix. Biochem. J. 341:257-263
5. Becam IE, Tanentzapf G, Lepesant JA, Brown NH, Huynh JR. 2005. Integrin-independent repression of cadherin transcription by talin during axis formation in Drosophila. Nat. Cell Biol. 7:510-516 (Pubitemid 40637411)
6. Bois PR, O'Hara BP, Nietlispach D, Kirkpatrick J, Izard T. 2006. The vinculin binding sites of talin and alpha-actinin are sufficient to activate vinculin. J. Biol. Chem. 281:7228-7236 (Pubitemid 43847490)
7. Borgon RA, Vonrhein C, Bricogne G, Bois PR, Izard T. 2004. Crystal structure of human vinculin. Structure 12:1189-1197
8. Borowsky ML, Hynes RO. 1998. Layilin, a novel talin-binding transmembrane protein homologous with C-type lectins, is localized in membrane ruffles. J. Cell Biol. 143:429-442
9. Bos JL. 2005. Linking Rap to cell adhesion. Curr. Opin. Cell Biol. 17:123-128
10. Bouaouina M, Lad Y, Calderwood DA. 2008. The N-terminal domains of talin cooperate with the phosphotyrosine binding-like domain to activate beta1 and beta3 integrins. J. Biol. Chem. 283:6118-6125
11. Brett TJ, Legendre-Guillemin V, McPherson PS, Fremont DH. 2006. Structural definition of the F-actin- binding THATCH domain from HIP1R. Nat. Struct. Mol. Biol. 13:121-130 (Pubitemid 43214715)
12. Burridge K, Connell L. 1983. A new protein of adhesion plaques and ruffling membranes. J. Cell Biol. 97:359-367
13. Burridge K, Mangeat P. 1984. An interaction between vinculin and talin. Nature 308:744-746
14. Calderwood DA. 2004. Integrin activation. J. Cell Sci. 117:657-666
15. Calderwood DA, Yan B, de Pereda JM, Alvarez BG, Fujioka Y, et al. 2002. The phosphotyrosine bindinglike domain of talin activates integrins. J. Biol. Chem. 277:21749-21758 (Pubitemid 34952326)
16. Campbell ID, Ginsberg MH. 2004. The talin-tail interaction places integrin activation on FERM ground. Trends Biochem. Sci. 29:429-435
17. Chen H, Choudhury DM, Craig SW. 2006. Coincidence of actin filaments and talin is required to activate vinculin. J. Biol. Chem. 281:40389-40398 (Pubitemid 46041842)
18. Chen H, Cohen DM, Choudhury DM, Kioka N, Craig SW. 2005. Spatial distribution and functional significance of activated vinculin in living cells. J. Cell Biol. 169:459-470 (Pubitemid 40686696)
19. Chen HC, Appeddu PA, Parsons JT, Hildebrand JD, Schaller MD, Guan JL. 1995. Interaction of focal adhesion kinase with the cytoskeletal protein talin. J. Biol. Chem. 270:16995-16999
20. Chen NT, Lo SH. 2005. The N-terminal half of talin2 is sufficient for mouse development and survival. Biochem. Biophys. Res. Commun. 337:670-676
21. Cluzel C, Saltel F, Lussi J, Paulhe F, Imhof BA, Wehrle-Haller B. 2005. The mechanisms and dynamics of (alpha)v(beta)3 integrin clustering in living cells. J. Cell Biol. 171:383-392 (Pubitemid 41540029)
22. Conti FJ, Felder A, Monkley S, Schwander M, Wood MR, et al. 2008. Progressive myopathy and defects in the maintenance of myotendinous junctions in mice that lack talin 1 in skeletal muscle. Development 135:2043-2053 (Pubitemid 351943368)
23. Cram EJ, Clark SG, Schwarzbauer JE. 2003. Talin loss-of-function uncovers roles in cell contractility and migration in C. elegans. J. Cell Sci. 116:3871-3878
24. de Pereda JM, Wegener KL, Santelli E, Bate N, Ginsberg MH, et al. 2005. Structural basis for phosphatidylinositol phosphate kinase type Igamma binding to talin at focal adhesions. J. Biol. Chem. 280:8381-8386 (Pubitemid 40349742)
25. del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. 2009. Stretching single talin rod molecules activates vinculin binding. Science 323:638-641
26. Denker SP, Barber DL. 2002. Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J. Cell Biol. 159:1087-1096
27. Devenport D, Bunch TA, Bloor JW, Brower DL, Brown NH. 2007. Mutations in the Drosophila alphaPS2 integrin subunit uncover new features of adhesion site assembly. Dev. Biol. 308:294-308 (Pubitemid 47223095)
28. Dietrich C, Goldmann WH, Sackmann E, Isenberg G. 1993. Interaction of NBD-talin with lipid monolayers - a film balance study. FEBS Lett. 324:37-40 (Pubitemid 23165032)
29. Di Paolo G, Pellegrini L, Letinic K, Cestra G, Zoncu R, et al. 2002. Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin. Nature 420:85-89 (Pubitemid 35291444)
30. Fillingham I, Gingras AR, Papagrigoriou E, Patel B, Emsley J, et al. 2005. A vinculin binding domain from the talin rod unfolds to form a complex with the vinculin head. Structure 13:65-74 (Pubitemid 40092475)
31. Franco SJ, Rodgers MA, Perrin BJ, Han J, Bennin DA, et al. 2004. Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat. Cell Biol. 6:977-983 (Pubitemid 39359850)
32. Galbraith CG, Yamada KM, Sheetz MP. 2002. The relationship between force and focal complex development. J. Cell Biol. 159:695-705
33. García-Alvarez B, de Pereda JM, Calderwood DA, Ulmer TS, Critchley D, et al. 2003. Structural determinants of integrin recognition by talin. Mol. Cell 11:49-58 (Pubitemid 36131107)
34. Gingras AR, Bate N, Goult BT, Hazelwood L, Canestrelli I, et al. 2008. The structure of the C-terminal actin-binding domain of talin. EMBO J. 27:458-469 (Pubitemid 351161654)
35. Gingras AR, Vogel KP, Steinhoff HJ, Ziegler WH, Patel B, et al. 2006. Structural and dynamic characterization of a vinculin binding site in the talin rod. Biochemistry 45:1805-1817 (Pubitemid 43222124)
36. Gingras AR, Ziegler WH, Frank R, Barsukov IL, Roberts GC, et al. 2005. Mapping and consensus sequence identification for multiple vinculin binding sites within the talin rod. J. Biol. Chem. 280:37217-37224 (Pubitemid 41587806)
37. Goksoy E, Ma YQ, Wang X, Kong X, Perera D, et al. 2008. Structural basis for the autoinhibition of talin in regulating integrin activation. Mol. Cell 31:124-133 (Pubitemid 351905930)
38. Goldfinger LE, Ptak C, Jeffery ED, Shabanowitz J, Han J, et al. 2007. An experimentally derived database of candidate Ras-interacting proteins. J. Proteome Res. 6:1806-1811 (Pubitemid 46814504)
39. Goldmann WH, Isenberg G. 1991. Kinetic determination of talin-actin binding. Biochem. Biophys. Res. Commun. 178:718-723
40. Goldmann WH, Niggli V, Kaufmann S, Isenberg G. 1992. Probing actin and liposome interaction of talin and talin vinculin complexes - a kinetic, thermodynamic and lipid labeling study. Biochemistry 31:7665-7671
41. Han J, Lim CJ, Watanabe N, Soriani A, Ratnikov B, et al. 2006. Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr. Biol. 16:1796-1806 (Pubitemid 44354146)
42. Heise H, Bayerl T, Isenberg G, Sackmann E. 1991. Human platelet p-235, a talin-like actin binding-protein, binds selectively to mixed lipid bilayers. Biochim. Biophys. Acta 1061:121-131
43. Hemmings L, Rees DJG, Ohanian V, Bolton SJ, Gilmore AP, et al. 1996. Talin contains three actin-binding sites each of which is adjacent to a vinculin-binding site. J. Cell Sci. 109:2715-2726 (Pubitemid 26388356)
44. Horwitz A, Duggan K, Buck C, Beckerle MC, Burridge K. 1986. Interaction of plasma-membrane fibronectin receptor with talin - a transmembrane linkage. Nature 320:531-533 (Pubitemid 16045116)
45. Hytonen VP, Vogel V. 2008. How force might activate talin's vinculin binding sites: SMD reveals a structural mechanism. PLoS Comput. Biol. 4:e24 (Pubitemid 351328503)
46. Isenberg G, Doerhoefer S, Hoekstra D, Goldmann WH. 2002. Membrane fusion induced by the major lipid-binding domain of the cytoskeletal protein talin. Biochem. Biophys. Res. Commun. 295:636-643 (Pubitemid 34756896)
47. Izard T, Evans G, Borgon RA, Rush CL, Bricogne G, Bois PR. 2004. Vinculin activation by talin through helical bundle conversion. Nature 427:171-175 (Pubitemid 38094959)
48. Izard T, Vonrhein C. 2004. Structural basis for amplifying vinculin activation by talin. J. Biol. Chem. 279:27667-27678 (Pubitemid 38812608)
49. Jiang G, Giannone G, Critchley DR, Fukumoto E, Sheetz MP. 2003. Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 424:334-337 (Pubitemid 36899377)
50. Kaufmann S, Piekenbrock T, Goldmann WH, Barmann M, Isenberg G. 1991. Talin binds to actin and promotes filament nucleation. FEBS Lett. 284:187-191
51. Kim M, Carman CV, Springer TA. 2003. Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science 301:1720-1725 (Pubitemid 37174365)
52. Lammermann T, Bader BL, Monkley SJ, Worbs T, Wedlich-Soldner R, et al. 2008. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453:51-55 (Pubitemid 351630331)
53. Lee HS, Bellin RM, Walker DL, Patel B, Powers P, et al. 2004. Characterization of an actin-binding site within the talin FERM domain. J. Mol. Biol. 343:771-784 (Pubitemid 39311621)
54. Lee HS, Lim CJ, Puzon-McLaughlin W, Shattil SJ, Ginsberg MH. 2009. RIAM activates integrins by linking talin to Ras GTPase membrane-targeting sequences. J. Biol. Chem. 284:5119-5127
55. Lee SE, Chunsrivirot S, Kamm RD, Mofrad MR. 2008. Molecular dynamics study of talin-vinculin binding. Biophys. J. 95:2027-2036
56. Lee SE, Kamm RD, Mofrad MR. 2007. Force-induced activation of talin and its possible role in focal adhesion mechanotransduction. J. Biomech. 40:2096-2106
57. Lee SY, Voronov S, Letinic K, Nairn AC, Di Paolo G, De Camilli P. 2005. Regulation of the interaction between PIPKI gamma and talin by proline-directed protein kinases. J. Cell Biol. 168:789-799 (Pubitemid 40328162)
58. Legate KR, Montanez E, Kudlacek O, Fassler R. 2006. ILK, PINCH and parvin: the tIPP of integrin signalling. Nat. Rev. Mol. Cell Biol. 7:20-31 (Pubitemid 43361569)
59. Ling K, Doughman RL, Firestone AJ, Bunce MW, Anderson RA. 2002. Type I gamma phosphatidyli-nositol phosphate kinase targets and regulates focal adhesions. Nature 420:89-93 (Pubitemid 35291445)
60. Ling K, Doughman RL, Iyer VV, Firestone AJ, Bairstow SF, et al. 2003. Tyrosine phosphorylation of type Igamma phosphatidylinositol phosphate kinase by Src regulates an integrin-talin switch. J. Cell Biol. 163:1339-1349 (Pubitemid 38032094)
61. Loer B, Bauer R, Bornheim R, Grell J, Kremmer E, et al. 2008. The NHL-domain protein Wech is crucial for the integrin-cytoskeleton link. Nat. Cell Biol. 10:422-428
62. Ma YQ, Qin J, Wu C, Plow EF. 2008. Kindlin-2 (Mig-2): a coactivator of beta3 integrins. J. Cell Biol. 181:439-446
63. Martel V, Racaud-Sultan C, Dupe S, Marie C, Paulhe F, et al. 2001. Conformation, localization, and integrin binding of talin depend on its interaction with phosphoinositides. J. Biol. Chem. 276:21217-21227 (Pubitemid 37413110)
64. McCann RO, Craig SW.1997. The I/LWEQmodule: a conserved sequence that signifies F-actin binding in functionally diverse proteins from yeast to mammals. Proc. Natl. Acad. Sci. USA 94:5679-5684
65. McLachlan AD, Stewart M, Hynes RO, Rees DJG. 1994. Analysis of repeated motifs in the talin rod. J. Mol. Biol. 235:1278-1290 (Pubitemid 24148930)
66. McNamee HP, Ingber DE, Schwartz MA. 1993. Adhesion to fibronectin stimulates inositol lipid synthesis and enhances PDGF-induced inositol lipid breakdown. J. Cell Biol. 121:673-678 (Pubitemid 23131278)
67. Millon-Frémillon A, Bouvard D, Grichine A, Manet-Dupé S, Block MR, Albiges-Rizo C. 2008. Cell adaptive response to extracellular matrix density is controlled by ICAP-1-dependent beta1-integrin affinity. J. Cell Biol. 180:427-441 (Pubitemid 351185926)
68. Moes M, Rodius S, Coleman SJ, Monkley SJ, Goormaghtigh E, et al. 2007. The integrin binding site 2 (IBS2) in the talin rod domain is essential for linking integrin beta subunits to the cytoskeleton. J. Biol. Chem. 282:17280-17288 (Pubitemid 47093206)
69. Molony L, McCaslin D, Abernethy J, Paschal B, Burridge K. 1987. Properties of talin from chicken gizzard smooth muscle. J. Biol. Chem. 262:7790-7795
70. Monkley SJ, Pritchard CA, Critchley DR. 2001. Analysis of the mammalian talin2 gene TLN2. Biochem. Biophys. Res. Commun. 286:880-885
71. Monkley SJ, Zho X-H, Kinston SJ, Giblett SM, Hemmings L, et al. 2000. Disruption of the talin gene arrests mouse development at the gastrulation stage. Dev. Dyn. 219:560-574
72. Montanez E, Ussar S, Schifferer M, Bosl M, Zent R, et al. 2008. Kindlin-2 controls bidirectional signaling of integrins. Genes Dev. 22:1325-1330 (Pubitemid 351717522)
73. Moser M, Nieswandt B, Ussar S, Pozgajova M, Fassler R. 2008. Kindlin-3 is essential for integrin activation and platelet aggregation. Nat. Med. 14:325-330 (Pubitemid 351347914)
74. Muguruma M, Matsumura S, Fukazawa T. 1990. Direct interactions between talin and actin. Biochem. Biophys. Res. Commun. 171:1217-1223
75. Muguruma M, Matsumura S, Fukazawa T. 1992. Augmentation of alpha-actinin-induced gelation of actin by talin. J. Biol. Chem. 267:5621-5624
76. Muguruma M, Nishimuta S, Tomisaka Y, Ito T, Matsumara S. 1995. Organisation of the functional domains in membrane cytoskeletal protein talin. J. Biochem. 117:1036-1042
77. Nakamura F, Osborn TM, Hartemink CA, Hartwig JH, Stossel TP. 2007. Structural basis of filamin A functions. J. Cell Biol. 179:1011-1025
78. Nieswandt B, Moser M, Pleines I, Varga-Szabo D, Monkley S, et al. 2007. Loss of talin1 in platelets abrogates integrin activation, platelet aggregation, and thrombus formation in vitro and in vivo. J. Exp. Med. 204:3113-3118
79. Niggli V, Kaufmann S, Goldmann WH, Weber T, Isenberg G. 1994. Identification of functional domains in the cytoskeletal protein talin. Eur. J. Biochem. 224(3):951-957 (Pubitemid 24288858)
80. Oxley CL, Anthis NJ, Lowe ED, Vakonakis I, Campbell ID, Wegener KL. 2008. An integrin phosphorylation switch: the effect of beta3 integrin tail phosphorylation on Dok1 and talin binding. J. Biol. Chem. 283:5420-5426
81. Papagrigoriou E, Gingras AR, Barsukov IL, Bate N, Fillingham IJ, et al. 2004. Activation of a vinculin-binding site in the talin rod involves rearrangement of a five-helix bundle. EMBO J. 23:2942-2951 (Pubitemid 39093589)
82. Parsons M, Messent AJ, Humphries JD, Deakin NO, Humphries MJ. 2008. Quantification of integrin receptor agonism by fluorescence lifetime imaging. J. Cell Sci. 121:265-271 (Pubitemid 351356697)
83. Patel B, Gingras AR, Bobkov AA, Fujimoto LM, Zhang M, et al. 2006. The activity of the vinculin binding sites in talin is influenced by the stability of the helical bundles that make up the talin rod. J. Biol. Chem. 281:7458-7467 (Pubitemid 43847518)
84. Petrich BG, Marchese P, Ruggeri ZM, Spiess S, Weichert RA, et al. 2007. Talin is required for integrin-mediated platelet function in hemostasis and thrombosis. J. Exp. Med. 204:3103-3111
85. Pfaff M, Liu S, Erle DJ, Ginsberg MH. 1998. Integrin beta cytoplasmic domains differentially bind to cytoskeletal proteins. J. Biol. Chem. 273:6104-6109 (Pubitemid 28144690)
86. Piccolo E, Innominato PF, Mariggio MA, Maffucci T, Iacobelli S, Falasca M. 2002. The mechanism involved in the regulation of phospholipase Cgamma1 activity in cell migration. Oncogene 21:6520-6529 (Pubitemid 35155456)
87. Priddle H, Hemmings L, Monkley S, Woods A, Patel B, et al. 1998. Disruption of the talin gene compromises focal adhesion assembly in undifferentiated but not differentiated ES cells. J. Cell Biol. 142:1121-1133 (Pubitemid 28402065)
88. Ratnikov B, Ptak C, Han J, Shabanowitz J, Hunt DF, Ginsberg MH. 2005. Talin phosphorylation sites mapped by mass spectrometry. J. Cell Sci. 118:4921-4923 (Pubitemid 41672423)
89. Rees DJG, Ades SE, Singer SJ, Hynes RO. 1990. Sequence and domain-structure of talin. Nature 347:685-689
90. Rodius S, Chaloin O, Moes M, Schaffner-Reckinger E, Landrieu I, et al. 2008. The talin rod IBS2 alpha-helix interacts with the beta3 integrin cytoplasmic tail membrane proximal helix by establishing charge complementary salt bridges. J. Biol. Chem. 283:24212-24223
91. Saitoh A, Takiguchi K, Tanaka Y, Hotani H. 1998. Opening-up of liposomal membranes by talin. Proc. Natl. Acad. Sci. USA 95:1026-1031
92. Schmidt JM, Zhang J, Lee H-S, Stromer MH, Robson RM. 1999. Interaction of talin with actin: sensitive modulation of filament crosslinking activity. Arch. Biochem. Biophys. 366:139-150 (Pubitemid 29394239)
93. Seelig A, Blatter XL, Frentzel A, Isenberg G. 2000. Phospholipid binding of synthetic talin peptides provides evidence for an intrinsic membrane anchor of talin. J. Biol. Chem. 275:17954-17961 (Pubitemid 30414739)
94. Senetar MA, Foster SJ, McCann RO. 2004. Intrasteric inhibition mediates the interaction of the I/LWEQ module proteins Talin1, Talin2, Hip1, and Hip12 with actin. Biochemistry 43:15418-15428
95. Senetar MA, McCann RO. 2005. Gene duplication and functional divergence during evolution of the cytoskeletal linker protein talin. Gene 362:141-152
96. Smith SJ, McCann RO. 2007. A C-terminal dimerization motif is required for focal adhesion targeting of Talin1 and the interaction of the Talin1 I/LWEQ module with F-actin. Biochemistry 46:10886-10898
97. Srivastava J, Barreiro G, Groscurth S, Gingras AR, Goult BT, et al. 2008. Structural model and functional significance of pH-dependent talin-actin binding for focal adhesion remodelling. Proc. Natl. Acad. Sci. USA 105:14436-14441
98. Sun N, Critchley DR, Paulin D, Li Z, Robson RM. 2008. Identification of a repeated domain within mammalian alpha-synemin that interacts directly with talin. Exp. Cell Res. 314:1839-1849
99. Sun Y, Ling K, Wagoner MP, Anderson RA. 2007. Type I gamma phosphatidylinositol phosphate kinase is required for EGF-stimulated directional cell migration. J. Cell Biol. 178:297-308 (Pubitemid 47076465)
100. Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC, et al. 2003. Talin binding to integrin beta tails: a final common step in integrin activation. Science 302:103-106 (Pubitemid 37210697)
101. Tanentzapf G, Martin-Bermudo MD, Hicks MS, Brown NH. 2006. Multiple factors contribute to integrin-talin interactions in vivo. J. Cell Sci. 119:1632-1644 (Pubitemid 43732989)
102. Tran Van Nhieu G, Izard T. 2007. Vinculin binding in its closed conformation by a helix addition mechanism. EMBO J. 26:4588-4596 (Pubitemid 350036624)
103. Tremuth L, Kreis S, Melchior C, Hoebeke J, Ronde P, et al. 2004. A fluorescence cell biology approach to map the second integrin-binding site of talin to a 130-amino acid sequence within the rod domain. J. Biol. Chem. 279:22258-22266 (Pubitemid 38679422)
104. Tsujioka M, Yoshida K, Nagasaki A, Yonemura S, Müller-Taubenberger A, Uyeda TQ. 2008. Overlapping functions of the two talin homologues in Dictyostelium. Eukaryot. Cell 7:906-916 (Pubitemid 351968833)
105. Wang Y, Litvinov RI, Chen X, Bach TL, Lian L, et al. 2008. Loss of PIP5KIgamma, unlike other PIP5KI isoforms, impairs the integrity of the membrane cytoskeleton in murine megakaryocytes. J. Clin. Invest. 118:812-819 (Pubitemid 351206568)
106. Watanabe N, Bodin L, Pandey M, Krause M, Coughlin S, et al. 2008. Mechanisms and consequences of agonist-induced talin recruitment to platelet integrin alphaIIbbeta3. J. Cell Biol. 181:1211-1222 (Pubitemid 351915493)
107. Wegener KL, Basran J, Bagshaw CR, Campbell ID, Roberts GC, et al. 2008. Structural basis for the interaction between the cytoplasmic domain of the hyaluronate receptor layilin and the talin F3 subdomain. J. Mol. Biol. 382:112-126
108. Wegener KL, Partridge AW, Han J, Pickford AR, Liddington RC, et al. 2007. Structural basis of integrin activation by talin. Cell 128:171-182 (Pubitemid 46048890)
109. Winkler J, Lunsdorf H, Jockusch BM. 1997. Energy-filtered electron microscopy reveals that talin is a highly flexible protein composed of a series of globular domains. Eur. J. Biochem. 243:430-436 (Pubitemid 27060432)
110. Xing B, Jedsadayanmata A, Lam SC. 2001. Localization of an integrin binding site to the C terminus of talin. J. Biol. Chem. 276:44373-44378 (Pubitemid 37391205)
111. Zaidel-Bar R, Itzkovitz S, Ma'ayan A, Iyengar R, Geiger B. 2007. Functional atlas of the integrin adhesome. Nat. Cell Biol. 9:858-867
112. Zhang X, Jiang G, Cai Y, Monkley SJ, Critchley DR, Sheetz MP. 2008. Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat. Cell Biol. 10:1062-1068
113. Ziegler WH, Liddington RC, Critchley DR. 2006. The structure and regulation of vinculin. Trends Cell Biol. 16:453-460