Characterization of an actin-binding site within the talin FERM domain

Journal of Molecular Biology

Volumn 343, Issue 3, 2004, Pages 771-784

  Lee, Ho Sup ^a   Bellin, Robert M ^a   Walker, Diane L ^a   Patel, Bipin ^b   Powers, Pam ^c   Liu, Hongjun ^c   Garcia Alvarez, Begoña ^c   De Pereda, José M ^c   Liddington, Robert C ^c   Volkmann, Niels ^c   Hanein, Dorit ^c   Critchley, David R ^b   Robson, Richard M ^a  

^a Departments of Biochemistry   (United States)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c BURNHAM INSTITUTE   (United States)

Author keywords

F actin; FERM domain; focal adhesions; integrins; talin

Indexed keywords

CALPONIN; F ACTIN; INTEGRIN; POLYPEPTIDE; TALIN;

ACTIN FILAMENT; ARTICLE; BINDING SITE; CONTROLLED STUDY; ELECTRON MICROSCOPY; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PURIFICATION;

EID: 4744343552     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.08.069     Document Type: Article

References (78)

1. K. Burridge, and L. Connell A new protein of adhesion plaques and ruffling membranes J. Cell Biol. 97 1983 359 367
2. J.G. Tidball, T. O'Halloran, and K. Burridge Talin at myotendinous junctions J. Cell Biol. 103 1986 1465 1472
3. R. Sealock, B. Paschal, M. Beckerle, and K. Burridge Talin is a post-synaptic component of the rat neuromuscular junction Expt. Cell Res. 163 1986 143 150
4. A.M. Belkin, N.I. Zhidkova, and V.E. Koteliansky Localization of talin in skeletal and cardiac muscles FEBS Letters 200 1986 32 36
5. B. Geiger, T. Volk, and T. Volberg Molecular heterogeneity of adherens junctions J. Cell Biol. 101 1985 1523 1531
6. A. Kupfer, S.L. Swain, C.A. Janeway Jr, and S.J. Singer The specific direct interaction of helper T cells and antigen-presenting B cells Proc. Natl Acad. Sci. USA 83 1986 6080 6083
7. N.C. Collier, and K. Wang Purification and properties of human platelet P235. A high molecular weight protein substrate of endogenous calcium-activated protease(s) J. Biol. Chem. 257 1982 6937 6943
8. D.R. Critchley Focal adhesions - the cytoskeletal connection Curr. Opin. Cell Biol. 12 2000 133 139
9. Lee, H.-S., Bellin, R. M. & Robson, R. M. (2001). Talin. In Wiley Encylopedia of Molecular Medicine, vol. 5. pp. 3087-3089. Wiley, New York.
10. G.H. Nuckolls, L.H. Romer, and K. Burridge Microinjection of antibodies against talin inhibits the spreading and migration of fibroblasts J. Cell Sci. 102 1992 753 762
11. S.J. Bolton, S.T. Barry, H. Mosley, B. Patel, B.M. Jockusch, J.M. Wilkinson, and D.R. Critchley Monoclonal antibodies recognizing the N- and C-terminal regions of talin disrupt actin stress fibers when microinjected into human fibroblasts Cell Motil. Cytoskeleton 36 1997 363 376
12. A.M. Sydor, A.L. Su, F.S. Wang, A. Xu, and D.G. Jay Talin and vinculin play distinct roles in filopodial motility in the neuronal growth cone J. Cell Biol. 134 1996 1197 1207
13. C. Albiges-Rizo, P. Frachet, and M.R. Block Down regulation of talin alters cell adhesion and the processing of the alpha 5 beta 1 integrin J. Cell Sci. 108 1995 3317 3329
14. H. Priddle, L. Hemmings, S. Monkley, A. Woods, B. Patel, and D. Sutton Disruption of the talin gene compromises focal adhesion assembly in undifferentiated but not differentiated embryonic stem cells J. Cell Biol. 142 1998 1121 1133
15. G. Jiang, G. Giannone, D.R. Critchley, E. Fukumoto, and M.P. Sheetz Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin Nature 424 2003 334 337
16. G. Giannone, G. Jiang, D.H. Sutton, D.R. Critchley, and M.P. Sheetz Talin1 is critical for force-dependent reinforcement of initial integrin-cytoskeleton bonds but not tyrosine kinase activation J. Cell Biol. 163 2003 409 419
17. E.J. Cram, S.G. Clark, and J.E. Schwarzbauer Talin loss-of-function uncovers roles in cell contractility and migration in C. elegans J. Cell Sci. 116 2003 3871 3878
18. N.H. Brown, S.L. Gregory, W.L. Rickoll, L.I. Fessler, M. Prout, R.A. White, and J.W. Fristrom Talin is essential for integrin function in Drosophila Dev. Cell 3 2002 569 579
19. S.J. Monkley, X.H. Zhou, S.J. Kinston, S.M. Giblett, L. Hemmings, and H. Priddle Disruption of the talin gene arrests mouse development at the gastrulation stage Dev. Dyn. 219 2000 560 574
20. S. Tadokoro, S.J. Shattil, K. Eto, V. Tai, R.C. Liddington, and J.M. de Pereda Talin binding to integrin beta tails: a final common step in integrin activation Science 302 2003 103 106
21. M. Kim, C.V. Carman, and T.A. Springer Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins Science 301 2003 1720 1725
22. M.L. Borowsky, and R.O. Hynes Layilin, a novel talin-binding transmembrane protein homologous with C-type lectins, is localized in membrane ruffles J. Cell Biol. 143 1998 429 442
23. G. Di Paolo, L. Pellegrini, K. Letinic, G. Cestra, R. Zoncu, and S. Voronov Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin Nature 420 2002 85 89
24. K. Ling, R.L. Doughman, A.J. Firestone, M.W. Bunce, and R.A. Anderson Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions Nature 420 2002 89 93
25. H.C. Chen, P.A. Appeddu, J.T. Parsons, J.D. Hildebrand, M.D. Schaller, and J.L. Guan Interaction of focal adhesion kinase with cytoskeletal protein talin J. Biol. Chem. 270 1995 16995 16999
26. D. Ilic, C.H. Damsky, and T. Yamamoto Focal adhesion kinase: at the crossroads of signal transduction J. Cell Sci. 110 1997 401 407
27. B. Xing, A. Jedsadayanmata, and S.C. Lam Localization of an integrin binding site to the C terminus of talin J. Biol. Chem. 276 2001 44373 44378
28. M.D. Bass, B.J. Smith, S.A. Prigent, and D.R. Critchley Talin contains three similar vinculin-binding sites predicted to form an amphipathic helix Biochem. J. 341 1999 257 263
29. M. Muguruma, S. Matsumura, and T. Fukazawa Direct interactions between talin & actin Biochem. Biophys. Res. Commun. 171 1990 1217 1223
30. V. Niggli, S. Kaufmann, W.H. Goldmann, T. Weber, and G. Isenberg Identification of functional domains in the cytoskeletal protein talin Eur. J. Biochem. 224 1994 951 957
31. J.M. Schmidt, J. Zhang, H.S. Lee, M.H. Stromer, and R.M. Robson Interaction of talin with actin: sensitive modulation of filament crosslinking activity Arch. Biochem. Biophys. 366 1999 139 150
32. M. Muguruma, S. Nishimuta, Y. Tomisaka, T. Ito, and S. Matsumura Organization of the functional domains in membrane cytoskeletal protein talin J. Biochem. (Tokyo) 117 1995 1036 1042
33. W.H. Goldmann, A. Bremer, M. Haner, U. Aebi, and G. Isenberg Native talin is a dumbbell-shaped homodimer when it interacts with actin J. Struct. Biol. 112 1994 3 10
34. G. Isenberg, and W.H. Goldmann Peptide-specific antibodies localize the major lipid binding sites of talin dimers to oppositely arranged N-terminal 47 kDa subdomains FEBS Letters 426 1998 165 170
35. M. Muguruma, S. Matsumura, and T. Fukazawa Augmentation of alpha-actinin-induced gelation of actin by talin J. Biol. Chem. 267 1992 5621 5624
36. W.H. Goldmann, D. Hess, and G. Isenberg The effect of intact talin and talin tail fragment on actin filament dynamics and structure depends on pH and ionic strength Eur. J. Biochem. 260 1999 439 445
37. J.M. Schmidt, R.M. Robson, J. Zhang, and M.H. Stromer The marked pH dependence of the talin-actin interaction Biophys. Res. Commun. 197 1993 660 666
38. J. Zhang, R.M. Robson, J.M. Schmidt, and M.H. Stromer Talin can crosslink actin filaments into both networks and bundles Biochem. Biophys. Res. Commun. 218 1996 530 537
39. L. Hemmings, D.J. Rees, V. Ohanian, S.J. Bolton, A.P. Gilmore, and B. Patel Talin contains three actin-binding sites each of which is adjacent to a vinculin-binding site J. Cell Sci. 109 1996 2715 2726
40. R.O. McCann, and S.W. Craig The I/LWEQ module: a conserved sequence that signifies F-actin binding in functionally diverse proteins from yeast to mammals Proc. Natl Acad. Sci. USA 94 1997 5679 5684
41. R.O. McCann, and S.W. Craig Functional genomic analysis reveals the utility of the I/LWEQ module as a predictor of protein:actin interaction Biochem. Biophys. Res. Commun. 266 1999 135 140
42. D.J. Rees, S.E. Ades, S.J. Singer, and R.O. Hynes Sequence & domain structure of talin Nature 347 1990 685 689
43. B. Garcia-Alvarez, J.M. de Pereda, D.A. Calderwood, T.S. Ulmer, D. Critchley, and I.D. Campbell Structural determinants of integrin recognition by talin Mol. Cell 11 2003 49 58
44. S. Huttelmaier, B. Harbeck, N. Steffens, T. Meβerschmidt, S. Illenberger, and B.M. Jockusch Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP FEBS Letters 451 1999 68 74
45. X. Li, Y. Matsuoka, and V. Bennett Adducin preferentially recruits spectrin to the fast growing ends of actin filaments in a complex requiring the MARCKS-related domain and a newly defined oligomerization domain J. Biol. Chem. 273 1998 19329 19338
46. E.G. Yarmola, A.S. Edison, R.H. Lenox, and M.R. Bubb Actin filament cross-inking by MARCKS: characterization of two actin-binding sites within the phosphorylation site domain J. Biol. Chem. 276 2001 22351 22358
47. J.X. Tang, P.T. Szymanski, P.A. Janmey, and T. Tao Electrostatic effects of smooth muscle calponin on actin assembly Eur. J. Biochem. 247 1997 432 440
48. K.J. Amann, B.A. Renley, and J.M. Ervasti A cluster of basic repeats in the dystrophin rod domain binds F-actin through an electrostatic interaction J. Biol. Chem. 273 1998 28419 28423
49. M.V. de Arruda, H. Bazari, M. Wallek, and P. Matsudaira An actin footprint on villin. Single site substitutions in a cluster of basic residues inhibit the actin severing but not capping activity of villin J. Biol. Chem. 267 1992 13079 13085
50. J. Scheel, K. Ziegelbauer, T. Kupke, B.M. Humbel, A.A. Noegel, G. Gerisch, and M. Schleicher Hisactophilin, a histidine-rich actin-binding protein from Dictyostelium discoideum J. Biol. Chem. 264 1989 2832 2839
51. B.W. Bernstein, W.B. Painter, H. Chen, L.S. Minamide, H. Abe, and J.R. Bamburg Intracellular pH modulation of ADF/cofilin proteins Cell Motil. Cytoskeleton 47 2000 319 336
52. B.G. Han, W. Nunomura, Y. Takakuwa, N. Mohandas, and B.K. Jap Protein 4.1R core domain structure and insights into regulation of cytoskeletal organization Nature Struct. Biol. 7 2000 871 875
53. W.J. Smith, N. Nassar, A. Bretscher, R.A. Cerione, and P.A. Karplus Structure of the active N-terminal domain of ezrin. Conformational and mobility changes identify keystone interactions J. Biol. Chem. 278 2003 4949 4956
54. K. Hamada, T. Shimizu, T. Matsui, S. Tsukita, and T. Hakoshima Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain EMBO J. 19 2000 4449 4462
55. M.A. Pearson, D. Reczek, A. Bretscher, and P.A. Karplus Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain Cell 101 2000 259 270
56. I.L. Barsukov, A. Prescot, N. Bate, B. Patel, D.N. Floyd, and N. Bhanji Phosphatidylinositol phosphate kinase type 1gamma and beta1-integrin cytoplasmic domain bind to the same region in the talin FERM domain J. Biol. Chem. 278 2003 31202 31209
57. A. McGough F-actin-binding proteins Curr. Opin. Struct. Biol. 8 1998 166 176
58. A. McGough, M. Way, and D. DeRosier Determination of the alpha-actinin-binding site on actin filaments by cryoelectron microscopy and image analysis J. Cell Biol. 126 1994 433 443
59. D. Hanein, N. Volkmann, S. Goldsmith, A.M. Michon, W. Lehman, and R. Craig An atomic model of fimbrin binding to F-actin and its implications for filament crosslinking and regulation Nature Struct. Biol. 5 1998 787 792
60. V.E. Galkin, A. Orlova, M.S. VanLoock, and E.H. Egelman Do the utrophin tandem calponin homology domains bind F-actin in a compact or extended conformation? J. Mol. Biol. 331 2003 967 972
61. A.J. Sutherland-Smith, C.A. Moores, F.L. Norwood, V. Hatch, R. Craig, J. Kendrick-Jones, and W. Lehman An atomic model for actin binding by the CH domains and spectrin-repeat modules of utrophin and dystrophin J. Mol. Biol. 329 2003 15 33
62. S.P. Denker, and D.L. Barber Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1 J. Cell Biol. 159 2002 1087 1096
63. A.Y. Chan, M. Bailly, N. Zebda, J.E. Segall, and J.S. Condeelis Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion J. Cell Biol. 148 2000 531 542
64. M. Hawkins, B. Pope, S.K. Maciver, and A.G. Weeds Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments Biochemistry 32 1993 9985 9993
65. B. Yan, D.A. Calderwood, B. Yaspan, and M.H. Ginsberg Calpain cleavage promotes talin binding to the beta 3 integrin cytoplasmic domain J. Biol. Chem. 276 2001 28164 28170
66. L. Tranqui, and M.R. Block Intracellular processing of talin occurs within focal adhesions Expt. Cell Res. 217 1995 149 156
67. M.E. Bertagnolli, S.J. Locke, M.E. Hensler, P.F. Bray, and M.C. Beckerle Talin distribution and phosphorylation in thrombin-activated platelets J. Cell Sci. 106 1993 1189 1199
68. M. Hayashi, H. Suzuki, S. Kawashima, T.C. Saido, and M. Inomata The behavior of calpain-generated N- and C-terminal fragments of talin in integrin-mediated signaling pathways Arch. Biochem. Biophys. 371 1999 133 141
69. T. Edmunds, P.A. Nagainis, S.K. Sathe, V.F. Thompson, and D.E. Doll Comparison of the autolyzed and unautolyzed forms of mu- and m-calpain from bovine skeletal muscle Biochim. Biophys. Acta 1077 1991 197 208
70. J.A. Spudich, and S. Watt The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin J. Biol. Chem. 246 1971 4866 4871
71. N. Volkmann, D. Hanein, G. Ouyang, K.M. Trybus, D.J. DeRosier, and S. Lowey Evidence for cleft closure in actomyosin upon ADP release Nature Struct. Biol. 7 2000 1147 1155
72. C.H. Owen, D.G. Morgan, and D.J. DeRosier Image analysis of helical objects: the Brandeis Helical Package J. Struct. Biol. 116 1996 167 175
73. E.H. Egelman A robust algorithm for the reconstruction of helical filaments using single-particle methods Ultramicroscopy 85 2000 225 234
74. S.J. Ludtke, P.R. Baldwin, and W. Chiu EMAN: semiautomated software for high-resolution single-particle reconstructions J. Struct. Biol. 128 1999 82 97
75. N. Volkmann, and D. Hanein Quantitative fitting of atomic models into observed densities derived by electron microscopy J. Struct. Biol. 125 1999 176 184
76. K.C. Holmes, I. Angert, F.J. Kull, W. Jahn, and R.R. Schroder Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide Nature 425 2003 423 427
77. S. Yang, X. Yu, V.E. Galkin, and E.H. Egelman Issues of resolution and polymorphism in single-particle reconstruction J. Struct. Biol. 144 2003 162 171
78. L. Hemmings, P.A. Kuhlman, and D.R. Critchley Analysis of the actin-binding domain of alpha-actinin by mutagenesis and demonstration that dystrophin contains a functionally homologous domain J. Cell Biol. 116 1992 1369 1380