Recent advances in the understanding of the molecular mechanisms regulating platelet integrin αIIbβ3 activation

Protein and Cell

Volumn 1, Issue 7, 2010, Pages 627-637

  Tao, Lanlan ^a   Zhang, Yue ^a   Xi, Xiaodong ^a   Kieffer, Nelly ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAIIBBETA3 INTEGRIN; INTEGRIN; KINDLIN 1; KINDLIN 2; KINDLIN 3; PHOSPHOLIPASE C; RAP1 PROTEIN; REGULATOR PROTEIN; TALIN; UNCLASSIFIED DRUG;

BINDING AFFINITY; CELL ADHESION; CHO CELL; CONFORMATIONAL TRANSITION; CYTOSKELETON; FOCAL ADHESION; GENE MUTATION; HUMAN; LEUKOCYTE ADHESION DEFICIENCY; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION; THROMBOCYTE;

EID: 79953225185     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-010-0089-8     Document Type: Review

References (70)

1. Abram, C. L., and Lowell, C. A. (2009). The ins and outs of leukocyte integrin signaling. Annu Rev Immunol 27, 339-362.
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., et al. (2009). The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J 28, 3623-3632.
3. 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 beta cytoplasmic domain. Proc Natl Acad Sci U S A 100, 13298-13302.
4. Beckerle, M. C., Miller, D. E., Bertagnolli, M. E., and Locke, S. J. (1989). Activation-dependent redistribution of the adhesion plaque protein, talin, in intact human platelets. J Cell Biol 109, 3333-3346.
5. Bergmeier, W., Goerge, T., Wang, H. W., Crittenden, J. R., Baldwin, A. C., Cifuni, S. M., Housman, D. E., Graybiel, A. M., and Wagner, D. D. (2007). Mice lacking the signaling molecule CalDAG-GEFI represent a model for leukocyte adhesion deficiency type III. J Clin Invest 117, 1699-1707.
6. Bouaouina, M., Lad, Y., and Calderwood, D. A. (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.
7. Bunch, T. A. (2010). Integrin alphaIIbbeta3 activation in Chinese hamster ovary cells and platelets increases clustering rather than affinity. J Biol Chem 285, 1841-1849.
8. Calderwood, D. A., and Ginsberg, M. H. (2003). Talin forges the links between integrins and actin. Nat Cell Biol 5, 694-697.
9. Calderwood, D. A., Zent, R., Grant, R., Rees, D. J., Hynes, R. O., and Ginsberg, M. H. (1999). The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J Biol Chem 274, 28071-28074.
10. Calderwood, D. A., Yan, B., de Pereda, J. M., Alvarez, B. G., Fujioka, Y., Liddington, R. C., and Ginsberg, M. H. (2002). The phosphotyrosine binding-like domain of talin activates integrins. J Biol Chem 277, 21749-21758.
11. Critchley, D. R. (2009). Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu Rev Biophys 38, 235-254.
12. Crittenden, J. R., Bergmeier, W., Zhang, Y., Piffath, C. L., Liang, Y., Wagner, D. D., Housman, D. E., and Graybiel, A. M. (2004). CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat Med 10, 982-986.
13. Dowling, J. J., Vreede, A. P., Kim, S., Golden, J., and Feldman, E. L. (2008). Kindlin-2 is required for myocyte elongation and is essential for myogenesis. BMC Cell Biol 9, 36.
14. Friedland, J. C., Lee, M. H., and Boettiger, D. (2009). Mechanically activated integrin switch controls alpha5beta1 function. Science 323, 642-644.
15. García-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.
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. 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., et al. (2009). Structural determinants of integrin binding to the talin rod. J Biol Chem 284, 8866-8876.
18. 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., et al. (2006). Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr Biol 16, 1796-1806.
19. Harburger, D. S., and Calderwood, D. A. (2009). Integrin signalling at a glance. J Cell Sci 122, 159-163.
20. Harburger, D. S., Bouaouina, M., and Calderwood, D. A. (2009). Kindlin-1 and -2 directly bind the C-terminal region of beta integrin cytoplasmic tails and exert integrin-specific activation effects. J Biol Chem 284, 11485-11497.
21. Horwitz, A., Duggan, K., Buck, C., Beckerle, M. C., and Burridge, K. (1986). Interaction of plasma membrane fibronectin receptor with talin-a transmembrane linkage. Nature 320, 531-533.
22. Hughes, P. E., Diaz-Gonzalez, F., Leong, L., Wu, C., McDonald, J. A., Shattil, S. J., and Ginsberg, M. H. (1996). Breaking the integrin hinge. A defined structural constraint regulates integrin signaling. J Biol Chem 271, 6571-6574.
23. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
24. Kim, C., Lau, T. L., Ulmer, T. S., and Ginsberg, M. H. (2009). Interactions of platelet integrin alphaIIb and beta3 transmembrane domains in mammalian cell membranes and their role in integrin activation. Blood 113, 4747-4753.
25. Kinashi, T., Aker, M., Sokolovsky-Eisenberg, M., Grabovsky, V., Tanaka, C., Shamri, R., Feigelson, S., Etzioni, A., and Alon, R. (2004). LAD-III, a leukocyte adhesion deficiency syndrome associated with defective Rap1 activation and impaired stabilization of integrin bonds. Blood 103, 1033-1036.
26. Kindler, T. (1954). Congenital poikiloderma with traumatic bulla formation and progressive cutaneous atrophy. Br J Dermatol 66, 104-111.
27. Kloeker, S., Major, M. B., Calderwood, D. A., Ginsberg, M. H., Jones, D. A., and Beckerle, M. C. (2004). The Kindler syndrome protein is regulated by transforming growth factor-beta and involved in integrin-mediated adhesion. J Biol Chem 279, 6824-6833.
28. Krüger, M., Moser, M., Ussar, S., Thievessen, I., Luber, C. A., Forner, F., Schmidt, S., Zanivan, S., Fässler, R., and Mann, M. (2008). SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function. Cell 134, 353-364.
29. Kuijpers, T. W., van de Vijver, E., Weterman, M. A., de Boer, M., Tool, A. T., van den Berg, T. K., Moser, M., Jakobs, M. E., Seeger, K., Sanal, O., et al. (2009). LAD-1/variant syndrome is caused by mutations in FERMT3. Blood 113, 4740-4746.
30. Larjava, H., Plow, E. F., and Wu, C. (2008). Kindlins: essential regulators of integrin signalling and cell-matrix adhesion. EMBO Rep 9, 1203-1208.
31. Lau, T. L., Kim, C., Ginsberg, M. H., and Ulmer, T. S. (2009). The structure of the integrin alphaIIbbeta3 transmembrane complex explains integrin transmembrane signalling. EMBO J 28, 1351-1361.
32. Lee, H. S., Lim, C. J., Puzon-McLaughlin, W., Shattil, S. J., and Ginsberg, M. H. (2009). RIAM activates integrins by linking talin to ras GTPase membrane-targeting sequences. J Biol Chem 284, 5119-5127.
33. 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.
34. Luo, B. H., Carman, C. V., and Springer, T. A. (2007). Structural basis of integrin regulation and signaling. Annu Rev Immunol 25, 619-647.
35. Ma, Y. Q., Qin, J., and Plow, E. F. (2007). Platelet integrin alpha(IIb) beta(3): activation mechanisms. J Thromb Haemost 5, 1345-1352.
36. Ma, Y. Q., Qin, J., Wu, C., and Plow, E. F. (2008). Kindlin-2 (Mig-2): a co-activator of beta3 integrins. J Cell Biol 181, 439-446.
37. Mackinnon, A. C., Qadota, H., Norman, K. R., Moerman, D. G., and Williams, B. D. (2002). C. elegans PAT-4/ILK functions as an adaptor protein within integrin adhesion complexes. Curr Biol 12, 787-797.
38. Moes, M., Rodius, S., Coleman, S. J., Monkley, S. J., Goormaghtigh, E., Tremuth, L., Kox, C., van der Holst, P. P., Critchley, D. R., and Kieffer, N. (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.
39. Montanez, E., Ussar, S., Schifferer, M., Bösl, M., Zent, R., Moser, M., and Fässler, R. (2008). Kindlin-2 controls bidirectional signaling of integrins. Genes Dev 22, 1325-1330.
40. Mory, A., Feigelson, S. W., Yarali, N., Kilic, S. S., Bayhan, G. I., Gershoni-Baruch, R., Etzioni, A., and Alon, R. (2008). Kindlin-3: a new gene involved in the pathogenesis of LAD-III. Blood 112, 2591.
41. Moser, M., Nieswandt, B., Ussar, S., Pozgajova, M., and Fässler, R. (2008). Kindlin-3 is essential for integrin activation and platelet aggregation. Nat Med 14, 325-330.
42. Moser, M., Bauer, M., Schmid, S., Ruppert, R., Schmidt, S., Sixt, M., Wang, H. V., Sperandio, M., and Fässler, R. (2009). Kindlin-3 is required for beta2 integrin-mediated leukocyte adhesion to endothelial cells. Nat Med 15, 300-305.
43. Nurden, A. T. (2006). Glanzmann thrombasthenia. Orphanet J Rare Dis 1, 10-20.
44. Pasvolsky, R., Feigelson, S. W., Kilic, S. S., Simon, A. J., Tal-Lapidot, G., Grabovsky, V., Crittenden, J. R., Amariglio, N., Safran, M., Graybiel, A. M., et al. (2007). A LAD-III syndrome is associated with defective expression of the Rap-1 activator CalDAG-GEFI in lymphocytes, neutrophils, and platelets. J Exp Med 204, 1571-1582.
45. Rivera, J., Lozano, M. L., Navarro-Núñez, L., and Vicente, V. (2009). Platelet receptors and signaling in the dynamics of thrombus formation. Haematologica 94, 700-711.
46. Rodius, S., Chaloin, O., Moes, M., Schaffner-Reckinger, E., Landrieu, I., Lippens, G., Lin, M., Zhang, J., and Kieffer, N. (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.
47. Rogalski, T. M., Mullen, G. P., Gilbert, M. M., Williams, B. D., and Moerman, D. G. (2000). The UNC-112 gene in Caenorhabditis elegans encodes a novel component of cell-matrix adhesion structures required for integrin localization in the muscle cell membrane. J Cell Biol 150, 253-264.
48. Saltel, F., Mortier, E., Hytönen, 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 beta3-integrin clustering. J Cell Biol 187, 715-731.
49. Savage, B., Almus-Jacobs, F., and Ruggeri, Z. M. (1998). Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell 94, 657-666.
50. Shattil, S. J., Cunningham, M., and Hoxie, J. A. (1987). Detection of activated platelets in whole blood using activation-dependent monoclonal antibodies and flow cytometry. Blood 70, 307-315.
51. Shi, X., Ma, Y. Q., Tu, Y., Chen, K., Wu, S., Fukuda, K., Qin, J., Plow, E. F., and Wu, C. (2007). The MIG-2/integrin interaction strengthens cell-matrix adhesion and modulates cell motility. J Biol Chem 282, 20455-20466.
52. Shimaoka, M., Takagi, J., and Springer, T. A. (2002). Conformational regulation of integrin structure and function. Annu Rev Biophys Biomol Struct 31, 485-516.
53. Siegel, D. H., Ashton, G. H., Penagos, H. G., Lee, J. V., Feiler, H. S., Wilhelmsen, K. C., South, A. P., Smith, F. J., Prescott, A. R., Wessagowit, V., et al. (2003). Loss of kindlin-1, a human homolog of the Caenorhabditis elegans actin-extracellular-matrix linker protein UNC-112, causes Kindler syndrome. Am J Hum Genet 73, 174-187.
54. Su, X., Mi, J., Yan, J., Flevaris, P., Lu, Y., Liu, H., Ruan, Z., Wang, X., Kieffer, N., Chen, S., et al. (2008). RGT, a synthetic peptide corresponding to the integrin beta 3 cytoplasmic C-terminal sequence, selectively inhibits outside-in signaling in human platelets by disrupting the interaction of integrin alpha IIb beta 3 with Src kinase. Blood 112, 592-602.
55. Svensson, L., Howarth, K., McDowall, A., Patzak, I., Evans, R., Ussar, S., Moser, M., Metin, A., Fried, M., Tomlinson, I., et al. (2009). Leukocyte adhesion deficiency-III is caused by mutations in KINDLIN3 affecting integrin activation. Nat Med 15, 306-312.
56. 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 beta tails: a final common step in integrin activation. Science 302, 103-106.
57. Tanentzapf, G., and Brown, N. H. (2006). An interaction between integrin and the talin FERM domain mediates integrin activation but not linkage to the cytoskeleton. Nat Cell Biol 8, 601-606.
58. Tremuth, L., Kreis, S., Melchior, C., Hoebeke, J., Rondé, P., Plançon, S., Takeda, K., and Kieffer, N. (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.
59. 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.
60. Ussar, S., Wang, H. V., Linder, S., Fässler, R., and Moser, M. (2006). The Kindlins: subcellular localization and expression during murine development. Exp Cell Res 312, 3142-3151.
61. Ussar, S., Moser, M., Widmaier, M., Rognoni, E., Harrer, C., Genzel-Boroviczeny, O., Fässler, R., and van Heyningen, V. (2008). Loss of Kindlin-1 causes skin atrophy and lethal neonatal intestinal epithelial dysfunction. PLoS Genet 4, e1000289.
62. Vinogradova, O., Velyvis, A., Velyviene, A., Hu, B., Haas, T., Plow, E., and Qin, J. (2002). A structural mechanism of integrin alpha(IIb) beta(3) "inside-out" activation as regulated by its cytoplasmic face. Cell 110, 587-597.
63. Watanabe, N., Bodin, L., Pandey, M., Krause, M., Coughlin, S., Boussiotis, V. A., Ginsberg, M. H., and Shattil, S. J. (2008). Mechanisms and consequences of agonist-induced talin recruitment to platelet integrin alphaIIbbeta3. J Cell Biol 181, 1211-1222.
64. Wegener, K. L., Partridge, A. W., Han, J., Pickford, A. R., Liddington, R. C., Ginsberg, M. H., and Campbell, I. D. (2007). Structural basis of integrin activation by talin. Cell 128, 171-182.
65. Weinstein, E. J., Bourner, M., Head, R., Zakeri, H., Bauer, C., and Mazzarella, R. (2003). URP1: a member of a novel family of PH and FERM domain-containing membrane-associated proteins is significantly over-expressed in lung and colon carcinomas. Biochim Biophys Acta 1637, 207-216.
66. Wu, C. (2005). Migfilin and its binding partners: from cell biology to human diseases. J Cell Sci 118, 659-664.
67. Xiong, J. P., Stehle, T., Diefenbach, B., Zhang, R., Dunker, R., Scott, D. L., Joachimiak, A., Goodman, S. L., and Arnaout, M. A. (2001). Crystal structure of the extracellular segment of integrin alpha Vbeta3. Science 294, 339-345.
68. Xiong, J. P., Stehle, T., Goodman, S. L., and Arnaout, M. A. (2003). New insights into the structural basis of integrin activation. Blood 102, 1155-1159.
69. 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.
70. Zhu, J., Luo, B. H., Barth, P., Schonbrun, J., Baker, D., and Springer, T. A. (2009). The structure of a receptor with two associating transmembrane domains on the cell surface: integrin alphaIIbbeta3. Mol Cell 34, 234-249.