Differences in binding to the ILK complex determines kindlin isoform adhesion localization and integrin activation

Journal of Cell Science

Volumn 127, Issue 19, 2014, Pages 4308-4321

  Huet Calderwood, Clotilde ^a   Brahme, Nina N ^a   Kumar, Nikit ^a   Stiegler, Amy L ^a   Raghavan, Srikala ^a,b   Boggon, Titus J ^a   Calderwood, David A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Institute for Stem Cell Biology and Regenerative Medicine   (India)

Author keywords

Focal adhesion; Integrin; Integrin activation; Integrin linked kinase; Kindlin

Indexed keywords

FOCAL ADHESION KINASE; INTEGRIN; INTEGRIN LINKED KINASE; KINDLIN; KINDLIN 1; KINDLIN 2; KINDLIN 3; LEUCINE; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5; VINCULIN; INTEGRIN-LINKED KINASE; ISOPROTEIN; MEMBRANE PROTEIN; MIG2B PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; TUMOR PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CHO CELL LINE; FEMALE; FIBROBLAST; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; 3T3 CELL LINE; AMINO ACID SEQUENCE; ANIMAL; CRICETULUS; FOCAL ADHESION; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CHO CELLS; CRICETULUS; FOCAL ADHESIONS; HEK293 CELLS; HUMANS; INTEGRINS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; NIH 3T3 CELLS; PROTEIN ISOFORMS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 84913604423     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.155879     Document Type: Article

References (64)

1. Bandyopadhyay, A., Rothschild, G., Kim, S., Calderwood, D. A. and Raghavan, S. (2012). Functional differences between kindlin-1 and kindlin-2 in keratinocytes. J. Cell Sci. 125, 2172-2184.
2. Bialkowska, K., Ma, Y. Q., Bledzka, K., Sossey-Alaoui, K., Izem, L., Zhang, X., Malinin, N., Qin, J., Byzova, T. and Plow, E. F. (2010). The integrin co-activator Kindlin-3 is expressed and functional in a non-hematopoietic cell, the endothelial cell. J. Biol. Chem. 285, 18640-18649.
3. Bouaouina, M., Goult, B. T., Huet-Calderwood, C., Bate, N., Brahme, N. N., Barsukov, I. L., Critchley, D. R. and Calderwood, D. A. (2012a). A conserved lipid-binding loop in the kindlin FERM F1 domain is required for kindlin-mediated aIIbb3 integrin coactivation. J. Biol. Chem. 287, 6979-6990.
4. Bouaouina, M., Harburger, D. S. and Calderwood, D. A. (2012b). Talin and signaling through integrins. Methods Mol. Biol. 757, 325-347.
5. Brahme, N. N., Harburger, D. S., Kemp-O'Brien, K., Stewart, R., Raghavan, S., Parsons, M. and Calderwood, D. A. (2013). Kindlin binds migfilin tandem LIM domains and regulates migfilin focal adhesion localization and recruitment dynamics. J. Biol. Chem. 288, 35604-35616.
6. Calderwood, D. A. (2004a). Integrin activation. J. Cell Sci. 117, 657-666. Calderwood, D. A. (2004b). Talin controls integrin activation. Biochem. Soc. Trans. 32, 434-437.
7. Calderwood, D. A. (2004b). Talin controls integrin activation. Biochem. Soc. Trans. 32, 434-437.
8. Calderwood, D. A., Campbell, I. D. and Critchley, D. R. (2013). Talins and kindlins: partners in integrin-mediated adhesion. Nat. Rev. Mol. Cell Biol. 14, 503-517.
9. Chiswell, B. P., Zhang, R., Murphy, J. W., Boggon, T. J. and Calderwood, D. A. (2008). The structural basis of integrin-linked kinase-PINCH interactions. Proc. Natl. Acad. Sci. USA 105, 20677-20682.
10. Chiswell, B. P., Stiegler, A. L., Razinia, Z., Nalibotski, E., Boggon, T. J. and Calderwood, D. A. (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.
11. 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.
12. Elad, N., Volberg, T., Patla, I., Hirschfeld-Warneken, V., Grashoff, C., Spatz, J. P., Fässler, R., Geiger, B. and Medalia, O. (2013). The role of integrin-linked kinase in the molecular architecture of focal adhesions. J. Cell Sci. 126, 4099-4107.
13. Feigelson, S. W., Grabovsky, V., Manevich-Mendelson, E., Pasvolsky, R., Shulman, Z., Shinder, V., Klein, E., Etzioni, A., Aker, M. and Alon, R. (2011). Kindlin-3 is required for the stabilization of TCR-stimulated LFA-1:ICAM-1 bonds critical for lymphocyte arrest and spreading on dendritic cells. Blood 117, 7042-7052.
14. Friedrich, E. B., Liu, E., Sinha, S., Cook, S., Milstone, D. S., MacRae, C. A., Mariotti, M., Kuhlencordt, P. J., Force, T., Rosenzweig, A. et al. (2004). Integrin-linked kinase regulates endothelial cell survival and vascular development. Mol. Cell. Biol. 24, 8134-8144.
15. Fukuda, T., Chen, K., Shi, X. and Wu, C. (2003). PINCH-1 is an obligate partner of integrin-linked kinase (ILK) functioning in cell shape modulation, motility, and survival. J. Biol. Chem. 278, 51324-51333.
16. Fukuda, K., Gupta, S., Chen, K., Wu, C. and Qin, J. (2009). The pseudoactive site of ILK is essential for its binding to α-Parvin and localization to focal adhesions. Mol. Cell 36, 819-830.
17. Geiger, T. and Zaidel-Bar, R. (2012). Opening the floodgates: proteomics and the integrin adhesome. Curr. Opin. Cell Biol. 24, 562-568.
18. Ghatak, S., Morgner, J. and Wickström, S. A. (2013). ILK: a pseudokinase with a unique function in the integrin-actin linkage. Biochem. Soc. Trans. 41, 995-1001.
19. Gkretsi, V., Mars, W. M., Bowen, W. C., Barua, L., Yang, Y., Guo, L., St-Arnaud, R., Dedhar, S., Wu, C. and Michalopoulos, G. K. (2007). Loss of integrin linked kinase from mouse hepatocytes in vitro and in vivo results in apoptosis and hepatitis. Hepatology 45, 1025-1034.
20. 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. et al. (2009). The structure of the N-terminus of kindlin-1: a domain important for alphaiibbeta3 integrin activation. J. Mol. Biol. 394, 944-956.
21. Hannigan, G. E., Leung-Hagesteijn, C., Fitz-Gibbon, L., Coppolino, M. G., Radeva, G., Filmus, J., Bell, J. C. and Dedhar, S. (1996). Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 379, 91-96.
22. Harburger, D. S. and Calderwood, D. A. (2009). Integrin signalling at a glance. J. Cell Sci. 122, 159-163.
23. Harburger, D. S., Bouaouina, M. and Calderwood, D. A. (2009). Kindlin-1 and-2 directly bind the C-terminal region of β integrin cytoplasmic tails and exert integrin-specific activation effects. J. Biol. Chem. 284, 11485-11497.
24. Honda, S., Shirotani-Ikejima, H., Tadokoro, S., Maeda, Y., Kinoshita, T., Tomiyama, Y. and Miyata, T. (2009). Integrin-linked kinase associated with integrin activation. Blood 113, 5304-5313.
25. Karaköse, E., Schiller, H. B. and Fässler, R. (2010). The kindlins at a glance. J. Cell Sci. 123, 2353-2356.
26. Kogata, N., Tribe, R. M., Fässler, R., Way, M. and Adams, R. H. (2009). Integrinlinked kinase controls vascular wall formation by negatively regulating Rho/ ROCK-mediated vascular smooth muscle cell contraction. Genes Dev. 23, 2278-2283.
27. Kuijpers, T. W., van de Vijver, E., Weterman, M. A., de Boer, M., Tool, A. T., Den Berg, T. K., Moser, M., Jakobs, M. E., Seeger, K., Sanal, ö. et al. (2009). LAD-1/variant syndrome is caused by mutations in FERMT3. Blood 113, 4740-4746.
28. Lad, Y., Harburger, D. S. and Calderwood, D. A. (2007). Integrin cytoskeletal interactions. Methods Enzymol. 426, 69-84.
29. Lai-Cheong, J. E., Ussar, S., Arita, K., Hart, I. R. and McGrath, J. A. (2008). Colocalization of kindlin-1, kindlin-2, and migfilin at keratinocyte focal adhesion and relevance to the pathophysiology of Kindler syndrome. J. Invest. Dermatol. 128, 2156-2165.
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. Liu, J., Fukuda, K., Xu, Z., Ma, Y. Q., Hirbawi, J., Mao, X., Wu, C., Plow, E. F. and Qin, J. (2011). Structural basis of phosphoinositide binding to kindlin-2 protein pleckstrin homology domain in regulating integrin activation. J. Biol. Chem. 286, 43334-43342.
32. Liu, W., Draheim, K. M., Zhang, R., Calderwood, D. A. and Boggon, T. J. (2013). Mechanism for KRIT1 release of ICAP1-mediated suppression of integrin activation. Mol. Cell 49, 719-729.
33. Ma, Y. Q., Qin, J., Wu, C. and Plow, E. F. (2008). Kindlin-2 (Mig-2): a co-activator of b3 integrins. J. Cell Biol. 181, 439-446.
34. 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.
35. Malinin, N. L., Zhang, L., Choi, J., Ciocea, A., Razorenova, O., Ma, Y. Q., Podrez, E. A., Tosi, M., Lennon, D. P., Caplan, A. I. et al. (2009). A point mutation in KINDLIN3 ablates activation of three integrin subfamilies in humans. Nat. Med. 15, 313-318.
36. 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.
37. 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.
38. 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 β2 integrinmediated leukocyte adhesion to endothelial cells. Nat. Med. 15, 300-305.
39. Nakazawa, T., Tadokoro, S., Kamae, T., Kiyomizu, K., Kashiwagi, H., Honda, S., Kanakura, Y. and Tomiyama, Y. (2013). Agonist stimulation, talin-1, and kindlin-3 are crucial for α(IIb)β(3) activation in a human megakaryoblastic cell line, CMK. Exp. Hematol. 41, 79, e1.
40. Perera, H. D., Ma, Y. Q., Yang, J., Hirbawi, J., Plow, E. F. and Qin, J. (2011). Membrane binding of the N-terminal ubiquitin-like domain of kindlin-2 is crucial for its regulation of integrin activation. Structure 19, 1664-1671.
41. Pluskota, E., Dowling, J. J., Gordon, N., Golden, J. A., Szpak, D., West, X. Z., Nestor, C., Ma, Y. Q., Bialkowska, K., Byzova, T. et al. (2011). The integrin coactivator kindlin-2 plays a critical role in angiogenesis in mice and zebrafish. Blood 117, 4978-4987.
42. Qadota, H., Moerman, D. G. and Benian, G. M. (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.
43. Qin, J. and Wu, C. (2012). ILK: a pseudokinase in the center stage of cell-matrix adhesion and signaling. Curr. Opin. Cell Biol. 24, 607-613.
44. Qu, H., Tu, Y., Shi, X., Larjava, H., Saleem, M. A., Shattil, S. J., Fukuda, K., Qin, J., Kretzler, M. and Wu, C. (2011). Kindlin-2 regulates podocyte adhesion and fibronectin matrix deposition through interactions with phosphoinositides and integrins. J. Cell Sci. 124, 879-891.
45. Sakai, T., Li, S., Docheva, D., Grashoff, C., Sakai, K., Kostka, G., Braun, A., Pfeifer, A., Yurchenco, P. D. and Fässler, R. (2003). Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion, and controlling actin accumulation. Genes Dev. 17, 926-940.
46. Shattil, S. J., Kim, C. and Ginsberg, M. H. (2010). The final steps of integrin activation: the end game. Nat. Rev. Mol. Cell Biol. 11, 288-300.
47. 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.
48. 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.
49. Stanchi, F., Grashoff, C., Nguemeni Yonga, C. F., Grall, D., Fässler, R. and Van Obberghen-Schilling, E. (2009). Molecular dissection of the ILK-PINCH-parvin triad reveals a fundamental role for the ILK kinase domain in the late stages of focal-adhesion maturation. J. Cell Sci. 122, 1800-1811.
50. Stiegler, A. L., Draheim, K. M., Li, X., Chayen, N. E., Calderwood, D. A. and Boggon, T. J. (2012). Structural basis for paxillin binding and focal adhesion targeting of β-parvin. J. Biol. Chem. 287, 32566-32577.
51. Stiegler, A. L., Grant, T. D., Luft, J. R., Calderwood, D. A., Snell, E. H. and Boggon, T. J. (2013). Purification and SAXS analysis of the integrin linked kinase, PINCH, parvin (IPP) heterotrimeric complex. PLoS ONE 8, e55591.
52. 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.
53. Terpstra, L., Prud'homme, J., Arabian, A., Takeda, S., Karsenty, G., Dedhar, S. and St-Arnaud, R. (2003). Reduced chondrocyte proliferation and chondrodysplasia in mice lacking the integrin-linked kinase in chondrocytes. J. Cell Biol. 162, 139-148.
54. Tucker, K. L., Sage, T., Stevens, J. M., Jordan, P. A., Jones, S., Barrett, N. E., St-Arnaud, R., Frampton, J., Dedhar, S. and Gibbins, J. M. (2008). A dual role for integrin-linked kinase in platelets: regulating integrin function and alphagranule secretion. Blood 112, 4523-4531.
55. 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.
56. Ussar, S., Moser, M., Widmaier, M., Rognoni, E., Harrer, C., Genzel-Boroviczeny, O. and Fässler, R. (2008). Loss of Kindlin-1 causes skin atrophy and lethal neonatal intestinal epithelial dysfunction. PLoS Genet. 4, e1000289.
57. Wang, H. V., Chang, L. W., Brixius, K., Wickström, S. A., Montanez, E., Thievessen, I., Schwander, M., Müller, U., Bloch, W., Mayer, U. et al. (2008). Integrin-linked kinase stabilizes myotendinous junctions and protects muscle from stress-induced damage. J. Cell Biol. 180, 1037-1049.
58. Wehrle-Haller, B. (2012). Assembly and disassembly of cell matrix adhesions. Curr. Opin. Cell Biol. 24, 569-581.
59. Wickström, S. A., Lange, A., Montanez, E. and Fässler, R. (2010). The ILK/ PINCH/parvin complex: the kinase is dead, long live the pseudokinase! EMBO J. 29, 281-291.
60. Xu, Z., Gao, J., Hong, J. and Ma, Y. Q. (2013). Integrity of kindlin-2 FERM subdomains is required for supporting integrin activation. Biochem. Biophys. Res. Commun. 434, 382-387.
61. Yang, Y., Wang, X., Hawkins, C. A., Chen, K., Vaynberg, J., Mao, X., Tu, Y., Zuo, X., Wang, J., Wang, Y. X. et al. (2009). Structural basis of focal adhesion localization of LIM-only adaptor PINCH by integrin-linked kinase. J. Biol. Chem. 284, 5836-5844.
62. Yates, L. A., Lumb, C. N., Brahme, N. N., Zalyte, R., Bird, L. E., De Colibus, L., Owens, R. J., Calderwood, D. A., Sansom, M. S. and Gilbert, R. J. (2012). Structural and functional characterization of the kindlin-1 pleckstrin homology domain. J. Biol. Chem. 287, 43246-43261.
63. Ye, F., Kim, C. and Ginsberg, M. H. (2012). Reconstruction of integrin activation. Blood 119, 26-33.
64. Ye, F., Petrich, B. G., Anekal, P., Lefort, C. T., Kasirer-Friede, A., Shattil, S. J., Ruppert, R., Moser, M., Fässler, R. and Ginsberg, M. H. (2013). The mechanism of kindlin-mediated activation of integrin αIIbβ3. Curr. Biol. 23, 2288-2295.