Studies on the morphology and spreading of human endothelial cells define key inter- and intramolecular interactions for talin1

European Journal of Cell Biology

Volumn 89, Issue 9, 2010, Pages 661-673

  Kopp, Petra M ^a   Bate, Neil ^a   Hansen, Tania M ^b   Brindle, Nicholas P J ^b   Praekelt, Uta ^a   Debrand, Emmanuel ^a   Coleman, Stacey ^a   Mazzeo, Daniela ^a   Goult, Benjamin T ^a   Gingras, Alexandre R ^a   Pritchard, Catrin A ^a   Critchley, David R ^a   Monkley, Susan J ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b Sir Robert Kilpatrick Clin Sci B   (United Kingdom)

Author keywords

Actin cytoskeleton; Focal adhesions; Integrins; Talin

Indexed keywords

CELL PROTEIN; GREEN FLUORESCENT PROTEIN; INTEGRIN; PROTEIN TALIN 1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRUCTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE MUTATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; UMBILICAL VEIN;

EID: 77954957343     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2010.05.003     Document Type: Article

References (55)

1. Albiges-Rizo C., Frachet P., Block M.R. Down regulation of talin alters cell adhesion and the processing of the a5b1 integrin. J. Cell Sci. 1995, 108:3317-3329.
2. Anthis N.J., Wegener K.L., Ye F., Kim C., Goult B.T., Lowe E.D., Vakonakis I., Bate N., Critchley D.R., Ginsberg M.H., Campbell I.D. The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J. 2009, 28:3623-3632.
3. Arias-Salgado E.G., Lizano S., Shattil S.J., Ginsberg M.H. Specification of the direction of adhesive signaling by the integrin beta cytoplasmic domain. J. Biol. Chem. 2005, 280:29699-29707.
4. Bolton S.J., Barry S.T., Mosley H., Patel B., Jockusch B., Wilkinson J.M., Critchley D.R. Monoclonal antibodies recognizing the N- and C-terminal regions of talin disrupt actin stress fibers when microinjected into human fibroblasts. Cell Motil. Cytoskeleton 1997, 36:363-376.
5. Bouaouina M., Lad Y., Calderwood D.A. The N-terminal domains of talin cooperate with the phosphotyrosine binding-like domain to activate beta1 and beta3 integrins. J. Biol. Chem. 2008, 283:6118-6125.
6. Burridge K., Connell L. A new protein of adhesion plaques and ruffling membranes. J. Cell Biol. 1983, 97:359-367.
7. Calderwood D.A. Integrin activation. J. Cell Sci. 2004, 117:657-666.
8. Chen N.T., Lo S.H. The N-terminal half of talin2 is sufficient for mouse development and survival. Biochem. Biophys. Res. Commun. 2005, 337:670-676.
9. Conti F.J., Felder A., Monkley S., Schwander M., Wood M.R., Lieber R., Critchley D., Muller U. Progressive myopathy and defects in the maintenance of myotendinous junctions in mice that lack talin 1 in skeletal muscle. Development 2008, 135:2043-2053.
10. Conti F.J., Monkley S.J., Wood M.R., Critchley D.R., Muller U. Talin 1 and 2 are required for myoblast fusion, sarcomere assembly and the maintenance of myotendinous junctions. Development 2009, 136:3597-3606.
11. Critchley D.R. Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu. Rev. Biophys. 2009, 38:235-254.
12. Debrand E., El Jai Y., Spence L., Bate N., Praekelt U., Pritchard C.A., Monkley S.J., Critchley D.R. Talin 2 is a large and complex gene encoding multiple transcripts and protein isoforms. FEBS J. 2009, 276:1610-1628.
13. del Rio A., Perez-Jimenez R., Liu R., Roca-Cusachs P., Fernandez J.M., Sheetz M.P. Stretching single talin rod molecules activates vinculin binding. Science 2009, 323:638-641.
14. Di Paolo G., Pellegrini L., Letinic K., Cestra G., Zoncu R., Voronov S., Chang S., Guo J., Wenk M.R., De Camilli P. Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin. Nature 2002, 420:85-89.
15. Garcia-Alvarez B., de Pereda J.M., Calderwood D.A., Ulmer T.S., Critchley D., Campbell I.D., Ginsberg M.H., Liddington R.C. Structural determinants of integrin recognition by talin. Mol. Cell 2003, 11:49-58.
16. Gingras A.R., Ziegler W.H., Frank R., Barsukov I.L., Roberts G.C., Critchley D.R., Emsley J. Mapping and consensus sequence identification for multiple vinculin binding sites within the talin rod. J. Biol. Chem. 2005, 280:37217-37224.
17. 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., Critchley D.R. The structure of the C-terminal actin-binding domain of talin. EMBO J. 2008, 27:458-469.
18. Gingras A.R., Ziegler W.H., Bobkov A.A., Joyce M.G., Fasci D., Himmel M., Rothemund S., Ritter A., Grossmann J.G., Patel B., Bate N., Goult B.T., Emsley J., Barsukov I.L., Roberts G.C., Liddington R.C., Ginsberg M.H., Critchley D.R. Structural determinants of integrin binding to the talin rod. J. Biol. Chem. 2009, 284:8866-8876.
19. Goksoy E., Ma Y.Q., Wang X., Kong X., Perera D., Plow E.F., Qin J. Structural basis for the autoinhibition of talin in regulating integrin activation. Mol. Cell 2008, 31:124-133.
20. 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., Critchley D.R. The structure of an interdomain complex that regulates talin activity. J. Biol. Chem. 2009, 284:15097-15106.
21. Goult B.T., Bouaouina M., Harburger D.S., Bate N., Patel B., Anthis N.J., Campbell I.D., Calderwood D.A., Barsukov I.L., Roberts G.C., Critchley D.R. The structure of the N-terminus of kindlin-1: a domain important for alphaIIbbeta3 integrin activation. J. Mol. Biol. 2009, 394:944-956.
22. 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., Barsukov I.L. Structure of a double ubiquitin-like domain in the talin head: a role in integrin activation. EMBO J. 2010, 29:1069-1080.
23. Han J., Lim C.J., Watanabe N., Soriani A., Ratnikov B., Calderwood D.A., Puzon-McLaughlin W., Lafuente E.M., Boussiotis V.A., Shattil S.J., Ginsberg M.H. Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr. Biol. 2006, 16:1796-1806.
24. Hemmings L., Rees D.J.G., Ohanian V., Bolton S.J., Gilmore A.P., Patel N., Priddle H., Trevithick J.E., Hynes R.O., Critchley D.R. Talin contains three actin-binding sites each of which is adjacent to a vinculin-binding site. J. Cell Sci. 1996, 109:2715-2726.
25. Himmel M., Ritter A., Rothemund S., Pauling B.V., Rottner K., Gingras A.R., Ziegler W.H. Control of high affinity interactions in the talin C terminus: how talin domains coordinate protein dynamics in cell adhesions. J. Biol. Chem. 2009, 284:13832-13842.
26. Humphries J.D., Wang P., Streuli C., Geiger B., Humphries M.J., Ballestrem C. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 2007, 179:1043-1057.
27. Jiang G., Giannone G., Critchley D.R., Fukumoto E., Sheetz M.P. Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 2003, 424:334-337.
28. Jones M.C., Caswell P.T., Moran-Jones K., Roberts M., Barry S.T., Gampel A., Mellor H., Norman J.C. VEGFR1 (Flt1) regulates Rab4 recycling to control fibronectin polymerization and endothelial vessel branching. Traffic 2009, 10:754-766.
29. Lammermann T., Bader B.L., Monkley S.J., Worbs T., Wedlich-Soldner R., Hirsch K., Keller M., Forster R., Critchley D.R., Fassler R., Sixt M. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 2008, 453:51-55.
30. Lee H.S., Bellin R.M., Walker D.L., Patel B., Powers P., Liu H., Garcia-Alvarez B., de Pereda J.M., Liddington R.C., Volkmann N., Hanein D., Critchley D.R., Robson R.M. Characterization of an actin-binding site within the talin FERM domain. J. Mol. Biol. 2004, 343:771-784.
31. Lee H.S., Lim C.J., Puzon-McLaughlin W., Shattil S.J., Ginsberg M.H. RIAM activates integrins by linking talin to ras GTPase membrane-targeting sequences. J. Biol. Chem. 2009, 284:5119-5127.
32. Ling K., Doughman R.L., Firestone A.J., Bunce M.W., Anderson R.A. Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 2002, 420:89-93.
33. Martel V., Racaud-Sultan C., Dupe S., Marie C., Paulhe F., Galmiche A., Block M.R., Albiges-Rizo C. Conformation, localization, and integrin binding of talin depend on its interaction with phosphoinositides. J. Biol. Chem. 2001, 276:21217-21227.
34. Moes M., Rodius S., Coleman S.J., Monkley S.J., Goormaghtigh E., Tremuth L., Kox C., van der Holst P.P., Critchley D.R., Kieffer N. The integrin binding site 2 (IBS2) in the talin rod domain is essential for linking integrin beta subunits to the cytoskeleton. J. Biol. Chem. 2007, 282:17280-17288.
35. Molony L., Mccaslin D., Abernethy J., Paschal B., Burridge K. Properties of talin from chicken gizzard smooth-muscle. J. Biol. Chem. 1987, 262:7790-7795.
36. Monkley S.J., Zho X.-H., Kinston S.J., Giblett S.M., Hemmings L., Priddle H., Brown J.E., Pritchard C.A., Critchley D.R., Fassler R. Disruption of the talin gene arrests mouse development at the gastrulation stage. Dev. Dynamics 2000, 219:560-574.
37. Moser M., Legate K.R., Zent R., Fassler R. The tail of integrins, talin, and kindlins. Science 2009, 324:895-899.
38. Nieswandt B., Moser M., Pleines I., Varga-Szabo D., Monkley S., Critchley D., Fassler R. Loss of talin1 in platelets abrogates integrin activation, platelet aggregation, and thrombus formation in vitro and in vivo. J. Exp. Med. 2007, 204:3113-3118.
39. Nuckolls G.H., Romer L.H., Burridge K. Microinjection of antibodies against talin inhibits the spreading and migration of fibroblasts. J. Cell Sci. 1992, 102:753-762.
40. Pertz O.C., Wang Y., Yang F., Wang W., Gay L.J., Gristenko M.A., Clauss T.R., Anderson D.J., Liu T., Auberry K.J., Camp D.G., Smith R.D., Klemke R.L. Spatial mapping of the neurite and soma proteomes reveals a functional Cdc42/Rac regulatory network. Proc. Natl. Acad. Sci. USA 2008, 105:1931-1936.
41. Petrich B.G., Marchese P., Ruggeri Z.M., Spiess S., Weichert R.A., Ye F., Tiedt R., Skoda R.C., Monkley S.J., Critchley D.R., Ginsberg M.H. Talin is required for integrin-mediated platelet function in hemostasis and thrombosis. J. Exp. Med. 2007, 204:3103-3111.
42. Priddle H., Hemmings L., Monkley S., Woods A., Patel B., Sutton D., Dunn G.A., Zicha D., Critchley D.R. Disruption of the talin gene compromises focal adhesion assembly in undifferentiated but not differentiated ES cells. J. Cell Biol. 1998, 142:1121-1133.
43. Ratnikov B., Ptak C., Han J., Shabanowitz J., Hunt D.F., Ginsberg M.H. Talin phosphorylation sites mapped by mass spectrometry. J. Cell Sci. 2005, 118:4921-4923.
44. Rodius S., Chaloin O., Moes M., Schaffner-Reckinger E., Landrieu I., Lippens G., Lin M., Zhang J., Kieffer N. 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. 2008, 283:24212-24223.
45. Roca-Cusachs P., Gauthier N.C., Del Rio A., Sheetz M.P. Clustering of alpha(5)beta(1) integrins determines adhesion strength whereas alpha(v)beta(3) and talin enable mechanotransduction. Proc. Natl. Acad. Sci. USA 2009, 106:16245-16250.
46. Saltel F., Mortier E., Hytonen V.P., Jacquier M.C., Zimmermann P., Vogel V., Liu W., Wehrle-Haller B. New PI(4,5)P2- and membrane proximal integrin-binding motifs in the talin head control beta3-integrin clustering. J. Cell Biol. 2009, 187:715-731.
47. Smith S.J., McCann R.O. 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 2007, 46:10886-10898.
48. Tadokoro S., Shattil S.J., Eto K., Tai V., Liddington R.C., de Pereda J.M., Ginsberg M.H., Calderwood D.A. Talin binding to integrin beta tails: a final common step in integrin activation. Science 2003, 302:103-106.
49. Tanentzapf G., Brown N.H. An interaction between integrin and the talin FERM domain mediates integrin activation but not linkage to the cytoskeleton. Nat. Cell Biol. 2006, 8:601-606.
50. Vicente-Manzanares M., Choi C.K., Horwitz A.R. Integrins in cell migration--the actin connection. J. Cell Sci. 2009, 122:199-206.
51. Wang Y., Litvinov R.I., Chen X., Bach T.L., Lian L., Petrich B.G., Monkley S.J., Critchley D.R., Sasaki T., Birnbaum M.J., Weisel J.W., Hartwig J., Abrams C.S. Loss of PIP5KIgamma, unlike other PIP5KI isoforms, impairs the integrity of the membrane cytoskeleton in murine megakaryocytes. J. Clin. Invest. 2008, 118:812-819.
52. Watanabe N., Bodin L., Pandey M., Krause M., Coughlin S., Boussiotis V.A., Ginsberg M.H., Shattil S.J. Mechanisms and consequences of agonist-induced talin recruitment to platelet integrin alphaIIbbeta3. J. Cell Biol. 2008, 181:1211-1222.
53. Wegener K.L., Partridge A.W., Han J., Pickford A.R., Liddington R.C., Ginsberg M.H., Campbell I.D. Structural basis of integrin activation by talin. Cell 2007, 128:171-182.
54. Winkler J., Lunsdorf H., Jockusch B.M. Energy-filtered electron microscopy reveals that talin is a highly flexible protein composed of a series of globular domains. Eur. J. Biochem. 1997, 243:430-436.
55. Zhang X., Jiang G., Cai Y., Monkley S.J., Critchley D.R., Sheetz M.P. Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat. Cell Biol. 2008, 10:1062-1068.