The integrin-linked kinase-PINCH-parvin complex supports integrin αIIbβ3 activation

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Honda, Shigenori ^a   Shirotani Ikejima, Hiroko ^a   Tadokoro, Seiji ^b   Tomiyama, Yoshiaki ^b,c   Miyata, Toshiyuki ^a  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c OSAKA UNIVERSITY HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; FLOW CYTOMETRY; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LIM DOMAIN PROTEINS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; MULTIPROTEIN COMPLEXES; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84893238618     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085498     Document Type: Article

References (51)

1. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687. doi:10.1016/S0092-8674(02)00971-6. PubMed: 12297042.
2. Shattil SJ, Newman PJ (2004) Integrins: dynamic scaffolds for adhesion and signaling in platelets. Blood 104: 1606-1615. doi:10.1182/blood-2004-04- 1257. PubMed: 15205259. (Pubitemid 39202265)
3. 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. doi:10.1126/science.1086652. PubMed: 14526080. (Pubitemid 37210697)
4. Shattil SJ, Kim C, Ginsberg MH (2010) The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol 11: 288-300. doi:10.1038/nrm2871. PubMed: 20308986.
5. Calderwood DA, Yan B, de Pereda JM, Alvarez BG, Fujioka Y et al. (2002) The phosphotyrosine binding-like domain of talin activates integrins. J Biol Chem 277: 21749-21758. doi:10.1074/jbc.M111996200. PubMed: 11932255. (Pubitemid 34952326)
6. Anthis NJ, Wegener KL, Ye F, Kim C, Goult BT et al. (2009) The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J 28: 3623-3632. doi:10.1038/emboj.2009.287. PubMed: 19798053.
7. Elliott PR, Goult BT, Kopp PM, Bate N, Grossmann JG et al. (2010) The Structure of the talin head reveals a novel extended conformation of the FERM domain. Structure 18: 1289-1299. doi:10.1016/j.str.2010.07.011. PubMed: 20947018.
8. Goult BT, Bouaouina M, Elliott PR, Bate N, Patel B et al. (2010) Structure of a double ubiquitin-like domain in the talin head: a role in integrin activation. EMBO J 29: 1069-1080. doi:10.1038/emboj.2010.4. PubMed: 20150896.
9. Moser M, Nieswandt B, Ussar S, Pozgajova M, Fässler R (2008) Kindlin-3 is essential for integrin activation and platelet aggregation. Nat Med 14: 325-330. doi:10.1038/nm1722. PubMed: 18278053. (Pubitemid 351347914)
10. Harburger DS, Bouaouina M, Calderwood DA (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. PubMed: 19240021.
11. Malinin NL, Plow EF, Byzova TV (2010) Kindlins in FERM adhesion. Blood 115: 4011-4017. doi:10.1182/blood-2009-10-239269. PubMed: 20228270.
12. Ma YQ, Qin J, Wu C, Plow EF (2008) Kindlin-2 (Mig-2): a co-activator of beta3 integrins. J Cell Biol 181: 439-446. doi:10.1083/jcb.200710196. PubMed: 18458155. (Pubitemid 351645034)
13. Moser M, Legate KR, Zent R, Fässler R (2009) The tail of integrins, talin, and kindlins. Science 324: 895-899. doi:10.1126/science.1163865. PubMed: 19443776.
14. 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. PubMed: 19098287.
15. Calderwood DA, Tai V, Di Paolo G, De Camilli P, Ginsberg MH (2004) Competition for talin results in trans-dominant inhibition of integrin activation. J Biol Chem 279: 28889-28895. doi:10.1074/jbc.M402161200. PubMed: 15143061. (Pubitemid 38915756)
16. Hughes PE, Renshaw MW, Pfaff M, Forsyth J, Keivens VM et al. (1997) Suppression of integrin activation: a novel function of a Ras/Raf-initiated MAP kinase pathway. Cell 88: 521-530. doi:10.1016/S0092-8674(00)81892-9. PubMed: 9038343. (Pubitemid 27154417)
17. Ramos JW, Kojima TK, Hughes PE, Fenczik CA, Ginsberg MH (1998) The death effector domain of PEA-15 is involved in its regulation of integrin activation. J Biol Chem 273: 33897-33900. doi:10.1074/jbc.273.51.33897. PubMed: 9852038. (Pubitemid 29008850)
18. Zent R, Fenczik CA, Calderwood DA, Liu S, Dellos M et al. (2000) Class- and splice variant-specific association of CD98 with integrin beta cytoplasmic domains. J Biol Chem 275: 5059-5064. doi:10.1074/jbc.275.7.5059. PubMed: 10671548. (Pubitemid 30108905)
19. Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L, Coppolino MG, Radeva G et al. (1996) Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 379: 91-96. doi:10.1038/379091a0. PubMed: 8538749. (Pubitemid 26008142)
20. Sakai T, Li S, Docheva D, Grashoff C, Sakai K et al. (2003) Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion, and controlling actin accumulation. Genes Dev 17: 926-940. doi:10.1101/gad.255603. PubMed: 12670870. (Pubitemid 36397379)
21. Hannigan GE, McDonald PC, Walsh MP, Dedhar S (2011) Integrin-linked kinase: not so 'pseudo' after all. Oncogene 30: 4375-4385. doi:10.1038/onc.2011. 177. PubMed: 21602880.
22. Qin J, Wu C (2012) ILK: a pseudokinase in the center stage of cell-matrix adhesion and signaling. Curr Opin Cell Biol 24: 607-613. doi:10.1016/j.ceb. 2012.06.003. PubMed: 22763012.
23. Li F, Zhang Y, Wu C (1999) Integrin-linked kinase is localized to cell-matrix focal adhesions but not cell-cell adhesion sites and the focal adhesion localization of integrin-linked kinase is regulated by the PINCH-binding ANK repeats. J Cell Sci 112 (24): 4589-4599. (Pubitemid 30034808)
24. Tu Y, Li F, Goicoechea S, Wu C (1999) The LIM-only protein PINCH directly interacts with integrin-linked kinase and is recruited to integrin-rich sites in spreading cells. Mol Cell Biol 19: 2425-2434. PubMed: 10022929. (Pubitemid 29098300)
25. Tu Y, Huang Y, Zhang Y, Hua Y, Wu C (2001) A new focal adhesion protein that interacts with integrin-linked kinase and regulates cell adhesion and spreading. J Cell Biol 153: 585-598. doi:10.1083/jcb.153.3.585. PubMed: 11331308. (Pubitemid 34280144)
26. Yamaji S, Suzuki A, Sugiyama Y, Koide Y, Yoshida M et al. (2001) A novel integrin-linked kinase-binding protein, affixin, is involved in the early stage of cell-substrate interaction. J Cell Biol 153: 1251-1264. doi:10.1083/jcb.153. 6.1251. PubMed: 11402068. (Pubitemid 34289263)
27. Braun A, Bordoy R, Stanchi F, Moser M, Kostka GG et al. (2003) PINCH2 is a new five LIM domain protein, homologous to PINCHand localized to focal adhesions. Exp Cell Res 284: 239-250. PubMed: 12651156. (Pubitemid 36324531)
28. Chu H, Thievessen I, Sixt M, Lämmermann T, Waisman A et al. (2006) gamma-Parvin is dispensable for hematopoiesis, leukocyte trafficking, and T-cell-dependent antibody response. Mol Cell Biol 26: 1817-1825. doi:10.1128/MCB.26.5.1817-1825.2006. PubMed: 16479001.
29. Tu Y, Li F, Wu C (1998) Nck-2, a novel Src homology2/3-containing adaptor protein that interacts with the LIM-only protein PINCH and components of growth factor receptor kinase-signaling pathways. Mol Biol Cell 9: 3367-3382. doi:10.1091/mbc.9.12.3367. PubMed: 9843575. (Pubitemid 28551035)
30. Widmaier M, Rognoni E, Radovanac K, Azimifar SB, Fässler R (2012) Integrin-linked kinase at a glance. J Cell Sci 125: 1839-1843. doi:10.1242/jcs.093864. PubMed: 22637643.
31. Honda S, Shirotani-Ikejima H, Tadokoro S, Maeda Y, Kinoshita T et al. (2009) Integrin-linked kinase associated with integrin activation. Blood 113: 5304-5313. doi:10.1182/blood-2008-07-169136. PubMed: 19299337.
32. Friedrich EB, Liu E, Sinha S, Cook S, Milstone DS et al. (2004) Integrin-linked kinase regulates endothelial cell survival and vascular development. Mol Cell Biol 24: 8134-8144. doi:10.1128/MCB. 24.18.8134-8144.2004. PubMed: 15340074.
33. Tucker KL, Sage T, Stevens JM, Jordan PA, Jones S et al. (2008) A dual role for integrin-linked kinase in platelets: regulating integrin function and alpha-granule secretion. Blood 112: 4523-4531. doi:10.1182/blood-2008-03-148502. PubMed: 18772455.
34. Chiswell BP, Stiegler AL, Razinia Z, Nalibotski E, Boggon TJ et al. (2010) Structural basis of competition between PINCH1 and PINCH2 for binding to the ankyrin repeat domain of integrin-linked kinase. J Struct Biol 170: 157-163. doi:10.1016/j.jsb.2009.12.002. PubMed: 19963065.
35. Fukuda K, Gupta S, Chen K, Wu C, Qin J (2009) The pseudoactive site of ILK is essential for its binding to alpha-Parvin and localization to focal adhesions. Mol Cell 36: 819-830. doi:10.1016/j.molcel.2009.11.028. PubMed: 20005845.
36. Calderwood DA, Zent R, Grant R, Rees DJ, Hynes RO et al. (1999) The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J Biol Chem 274: 28071-28074. doi:10.1074/jbc.274.40.28071. PubMed: 10497155.
37. Montanez E, Ussar S, Schifferer M, Bösl M, Zent R et al. (2008) Kindlin-2 controls bidirectional signaling of integrins. Genes Dev 22: 1325-1330. doi:10.1101/gad.469408. PubMed: 18483218. (Pubitemid 351717522)
38. Legate KR, Montañez E, Kudlacek O, Fässler R (2006) ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol 7: 20-31. doi:10.1038/nrm1789. PubMed: 16493410. (Pubitemid 43361569)
39. McDonald PC, Fielding AB, Dedhar S (2008) Integrin-linked kinase - essential roles in physiology and cancer biology. J Cell Sci 121: 3121-3132. doi:10.1242/jcs.017996. PubMed: 18799788.
40. Zhang Y, Guo L, Chen K, Wu C (2002) A critical role of the PINCH-integrin-linked kinase interaction in the regulation of cell shape change and migration. J Biol Chem 277: 318-326. PubMed: 11694512. (Pubitemid 34952061)
41. Qadota H, Moerman DG, Benian GM (2012) A molecular mechanism for the requirement of PAT-4 (integrin-linked kinase (ILK)) for the localization of UNC-112 (Kindlin) to integrin adhesion sites. J Biol Chem 287: 28537-28551. doi:10.1074/jbc.M112.354852. PubMed: 22761445.
42. Zhang Y, Chen K, Guo L, Wu C (2002) Characterization of PINCH-2, a new focal adhesion protein that regulates the PINCH-1-ILK interaction, cell spreading, and migration. J Biol Chem 277: 38328-38338. doi:10.1074/jbc. M205576200. PubMed: 12167643. (Pubitemid 35154687)
43. Yamaji S, Suzuki A, Kanamori H, Mishima W, Takabayashi M et al. (2002) Possible role of ILK-affixin complex in integrin-cytoskeleton linkage during platelet aggregation. Biochem Biophys Res Commun 297: 1324-1331. doi:10.1016/S0006-291X(02)02381-1. PubMed: 12372433.
44. Dittrich M, Birschmann I, Mietner S, Sickmann A, Walter U et al. (2008) Platelet protein interactions: map, signaling components, and phosphorylation groundstate. Arterioscler Thromb Vasc Biol 28: 1326-1331. doi:10.1161/ATVBAHA. 107.161000. PubMed: 18451328.
45. Pasquet JM, Noury M, Nurden AT (2002) Evidence that the platelet integrin alphaIIb beta3 is regulated by the integrin-linked kinase, ILK, in a PI3-kinase dependent pathway. Thromb Haemost 88: 115-122. PubMed: 12152651. (Pubitemid 34752276)
46. Stevens JM, Jordan PA, Sage T, Gibbins JM (2004) The regulation of integrin-linked kinase in human platelets: evidence for involvement in the regulation of integrin alpha 2 beta 1. J Thromb Haemost 2: 1443-1452. doi:10.1111/j.1538-7836.2004.00870.x. PubMed: 15304053. (Pubitemid 40186144)
47. Attwell S, Mills J, Troussard A, Wu C, Dedhar S (2003) Integration of cell attachment, cytoskeletal localization, and signaling by integrin-linked kinase (ILK), CH-ILKBP, and the tumor suppressor PTEN. Mol Biol Cell 14: 4813-4825. doi:10.1091/mbc.E03-05-0308. PubMed: 12960424. (Pubitemid 37484798)
48. Grashoff C, Aszódi A, Sakai T, Hunziker EB, Fässler R (2003) Integrin-linked kinase regulates chondrocyte shape and proliferation. EMBO Rep 4: 432-438. doi:10.1038/sj.embor.embor801. PubMed: 12671688. (Pubitemid 36622011)
49. Terpstra L, Prud'homme J, Arabian A, Takeda S, Karsenty G et al. (2003) Reduced chondrocyte proliferation and chondrodysplasia in mice lacking the integrin-linked kinase in chondrocytes. J Cell Biol 162: 139-148. doi:10.1083/jcb.200302066. PubMed: 12835312. (Pubitemid 36859541)
50. Vouret-Craviari V, Boulter E, Grall D, Matthews C, Van Obberghen-Schilling E (2004) ILK is required for the assembly of matrix-forming adhesions and capillary morphogenesis in endothelial cells. J Cell Sci 117: 4559-4569. doi:10.1242/jcs.01331. PubMed: 15316070. (Pubitemid 39360081)
51. Chen K, Tu Y, Zhang Y, Blair HC, Zhang L et al. (2008) PINCH-1 regulates the ERK-Bim pathway and contributes to apoptosis resistance in cancer cells. J Biol Chem 283: 2508-2517. PubMed: 18063582.