Kindlin-3 is essential for the resting α4β1 integrin-mediated firm cell adhesion under shear flow conditions

Journal of Biological Chemistry

Volumn 291, Issue 19, 2016, Pages 10363-10371

  Lu, Ling ^a   Lin, ChangDong ^a   Yan, ZhanJun ^b   Wang, Shu ^a   Zhang, YouHua ^a   Wang, ShiHui ^a   Wang, JunLei ^a   Liu, Cui ^a   Chen, JianFeng ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CELL ADHESION; CHEMICAL ACTIVATION; CONFORMATIONS; SHEAR FLOW;

BINDING AFFINITIES; CELL ROLLING; CRITICAL STEPS; FLOW CONDITION; INTEGRIN ACTIVATION; RESTING STATE; ROLLING ADHESION; VASCULAR CELL ADHESION MOLECULE-1;

CELLS;

BINDING PROTEIN; KINDLIN 3; MANGANESE; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 4; MEMBRANE PROTEIN; MIG2B PROTEIN, HUMAN; PROTEIN BINDING; TUMOR PROTEIN;

ARTICLE; BINDING AFFINITY; CELL ADHESION; CONTROLLED STUDY; FIRM CELL ADHESION; GENE SILENCING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; ROLLING CELL ADHESION; SHEAR FLOW; VELOCITY; GENETICS; HUMAN; K-562 CELL LINE; METABOLISM; PHYSIOLOGY; SHEAR STRENGTH; SIGNAL TRANSDUCTION;

CELL ADHESION; HUMANS; INTEGRIN ALPHA4BETA1; K562 CELLS; MANGANESE; MEMBRANE PROTEINS; NEOPLASM PROTEINS; PROTEIN BINDING; SHEAR STRENGTH; SIGNAL TRANSDUCTION; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84966333663     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.717694     Document Type: Article

References (60)

1. Hynes, R. O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687
2. Berlin, C., Bargatze, R. F., Campbell, J. J., von Andrian, U. H., Szabo, M. C., Hasslen, S. R., Nelson, R. D., Berg, E. L., Erlandsen, S. L., and Butcher, E. C. (1995) α4 integrins mediate lymphocyte attachment and rolling under physiological flow. Cell 80, 413- 422
3. Chen, C., Mobley, J. L., Dwir, O., Shimron, F., Grabovsky, V., Lobb, R. R., Shimizu, Y., and Alon, R. (1999) High affinity very late antigen-4 subsets expressed on T cells are mandatory for spontaneous adhesion strengthening but not for rolling on VCAM-1 in shear flow. J. Immunol. 162, 1084-1095
4. Lim, Y. C., Wakelin, M. W., Henault, L., Goetz, D. J., Yednock, T., Cabañas, C., Sánchez-Madrid, F., Lichtman, A. H., and Luscinskas, F. W. (2000) α4 β1 -Integrin activation is necessary for high-efficiency T-cell subset interactions with VCAM-1 under flow. Microcirculation 7, 201-214
5. Hyduk, S. J., Rullo, J., Cano, A. P., Xiao, H., Chen, M., Moser, M., and Cybulsky, M. I. (2011) Talin-1 and kindlin-3 regulate α4 β1 integrin-mediated adhesion stabilization, but not G protein-coupled receptor-induced affinity upregulation. J. Immunol. 187, 4360- 4368
6. Luo, B. H., Carman, C. V., and Springer, T. A. (2007) Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25, 619-647
7. Takagi, J., Petre, B. M., Walz, T., and Springer, T. A. (2002) Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 110, 599-611
8. Shimaoka, M., and Springer, T. A. (2004) Therapeutic antagonists and the conformational regulation of the β2 integrins. Curr. Top. Med. Chem. 4, 1485-1495
9. Arnaout, M. A., Mahalingam, B., and Xiong, J. P. (2005) Integrin structure, allostery, and bidirectional signaling. Annu. Rev. Cell Dev. Biol. 21, 381- 410
10. Liu, S., Calderwood, D. A., and Ginsberg, M. H. (2000) Integrin cytoplasmic domain-binding proteins. J. Cell Sci. 113, 3563-3571
11. Moser, M., Legate, K. R., Zent, R., and Fässler, R. (2009) The tail of integrins, talin, and kindlins. Science 324, 895- 899
12. Banno, A., and Ginsberg, M. H. (2008) Integrin activation. Biochem. Soc. Trans. 36, 229-234
13. Calderwood, D. A. (2004) Talin controls integrin activation. Biochem. Soc. Trans. 32, 434-437
14. 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 β tails: a final common step in integrin activation. Science 302, 103-106
15. Kahner, B. N., Kato, H., Banno, A., Ginsberg, M. H., Shattil, S. J., and Ye, F. (2012) Kindlins, integrin activation and the regulation of talin recruitment to αIIbβ3. PLos One 7, e34056
16. Ye, F., and Petrich, B. G. (2011) Kindlin: helper, co-activator, or booster of talin in integrin activation? Curr. Opin. Hematol. 18, 356-360
17. 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
18. Sun, H., Liu, J., Zheng, Y., Pan, Y., Zhang, K., and Chen, J. (2014) Distinct chemokine signaling regulates integrin ligand specificity to dictate tissuespecific lymphocyte homing. Dev. Cell 30, 61-70
19. Zhang, K., and Chen, J. (2012) The regulation of integrin function by divalent cations. Cell Adh. Migr. 6, 20-29
20. Leitinger, B., McDowall, A., Stanley, P., and Hogg, N. (2000) The regulation of integrin function by Ca 2+ . Biochim. Biophys. Acta 1498, 91-98
21. Chen, J., Salas, A., and Springer, T. A. (2003) Bistable regulation of integrin adhesiveness by a bipolar metal ion cluster. Nat. Struct. Biol. 10, 995-1001
22. Mould, A. P., Akiyama, S. K., and Humphries, M. J. (1995) Regulation of integrinα5β1-fibronectin interactions by divalent cations-evidence for distinct classes of binding sites for Mn 2+ ,Mg 2+ , and Ca 2+ . J. Biol. Chem. 270, 26270-26277
23. Karaköse, E., Schiller, H. B., and Fässler, R. (2010) The kindlins at a glance. J. Cell Sci. 123, 2353-2356
24. Malinin, N. L., Plow, E. F., and Byzova, T. V. (2010) Kindlins in FERM adhesion. Blood 115, 4011-4017
25. Moretti, F., Schmidt, S., Ruppert, R., Fassler, R., and Moser, M. (2010) A critical kindlin-3 level is required for efficient integrin activation in hematopoietic cells. Eur. J. Cell Biol. 89, 51
26. 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., Shurin, S. B., Plow, E. F., and Byzova, T. V. (2009) A point mutation in KINDLIN3 ablates activation of three integrin subfamilies in humans. Nat. Med. 15, 313-318
27. 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
28. McDowall, A., Svensson, L., Stanley, P., Patzak, I., Chakravarty, P., Howarth, K., Sabnis, H., Briones, M., and Hogg, N. (2010) Two mutations in the KINDLIN3 gene of a new leukocyte adhesion deficiency III patient reveal distinct effects on leukocyte function in vitro. Blood 115, 4834-4842
29. Meller, J., Malinin, N. L., Panigrahi, S., Kerr, B. A., Patil, A., Ma, Y., Venkateswaran, L., Rogozin, I. B., Mohandas, N., Ehlayel, M. S., Podrez, E. A., Chinen, J., and Byzova, T. V. (2012) Novel aspects of kindlin-3 function in humans based on a new case of leukocyte adhesion deficiency III. J. Thromb. Haemost. 10, 1397-1408
30. Svensson, L., Howarth, K., McDowall, A., Patzak, I., Evans, R., Ussar, S., Moser, M., Metin, A., Fried, M., Tomlinson, I., and Hogg, N. (2009) Leukocyte adhesion deficiency-III is caused by mutations in KINDLIN3 affecting integrin activation. Nat. Med. 15, 306-312
31. Manevich-Mendelson, E., Feigelson, S. W., Pasvolsky, R., Aker, M., Grabovsky, V., Shulman, Z., Kilic, S. S., Rosenthal-Allieri, M. A., Ben-Dor, S., Mory, A., Bernard, A., Moser, M., Etzioni, A., and Alon, R. (2009) Loss of kindlin-3 in LAD-III eliminates LFA-1 but not VLA-4 adhesiveness developed under shear flow conditions. Blood 114, 2344-2353
32. Kassner, P. D., and Hemler, M. E. (1993) Interchangeable α-chain cytoplasmic domains play a positive role in control of cell adhesion mediated by Vla-4, a β1 integrin. J. Exp. Med. 178, 649-660
33. Yue, J., Pan, Y., Sun, L., Zhang, K., Liu, J., Lu, L., and Chen, J. (2013) The unique disulfide bond-stabilized W1 α4-β1 loop in the α4 β-propeller domain regulates integrin α4 β7 affinity and signaling. J. Biol. Chem. 288, 14228-14237
34. Askari, J. A., Tynan, C. J., Webb, S. E., Martin-Fernandez, M. L., Ballestrem, C., and Humphries, M. J. (2010) Focal adhesions are sites of integrin extension. J. Cell Biol. 188, 891-903
35. Rose, D. M., Cardarelli, P. M., Cobb, R. R., and Ginsberg, M. H. (2000) Soluble VCAM-1 binding to α4 integrins is cell-type specific and activation dependent and is disrupted during apoptosis in T cells. Blood 95, 602- 609
36. Liao, Z., Kato, H., Pandey, M., Cantor, J. M., Ablooglu, A. J., Ginsberg, M. H., and Shattil, S. J. (2015) Interaction of kindlin-2 with integrin β3 promotes outside-in signaling responses by the αVβ3 vitronectin receptor. Blood 125, 1995-2004
37. Chen, J., Yang, W., Kim, M., Carman, C. V., and Springer, T. A. (2006) Regulation of outside-in signaling and affinity by the β2 I domain of integrin αL β2 . Proc. Natl. Acad. Sci. U.S.A. 103, 13062-13067
38. Salas, A., Shimaoka, M., Chen, S., Carman, C. V., and Springer, T. (2002) Transition from rolling to firm adhesion is regulated by the conformation of the I domain of the integrin lymphocyte function-associated antigen-1. J. Biol. Chem. 277, 50255-50262
39. Pan, Y., Zhang, K., Qi, J., Yue, J., Springer, T. A., and Chen, J. (2010) Cation-π interaction regulates ligand-binding affinity and signaling of integrin α4β7 . Proc. Natl. Acad. Sci. U.S.A. 107, 21388-21393
40. 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
41. Harburger, D. S., Bouaouina, M., and Calderwood, D. A. (2009) Kindlin-1 and-2 directly bind the C-terminal region of βintegrin cytoplasmic tails and exert integrin-specific activation effects. J. Biol. Chem. 284, 11485-11497
42. de Château, M., Chen, S., Salas, A., and Springer, T. A. (2001) Kinetic and mechanical basis of rolling through an integrin and novel Ca 2+ -dependent rolling and Mg 2+ -dependent firm adhesion modalities for the α4β7-MAdCAM-1 interaction. Biochemistry 40, 13972-13979
43. Chen, X., Xie, C., Nishida, N., Li, Z., Walz, T., and Springer, T. A. (2010) Requirement of open headpiece conformation for activation of leukocyte integrin αX β2 . Proc. Natl. Acad. Sci. U.S.A. 107, 14727-14732
44. Takada, Y., and Puzon, W. (1993) Identification of a regulatory region of integrin-β1 subunit using activating and inhibiting antibodies. J. Biol. Chem. 268, 17597-17601
45. 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 integrin-mediated leukocyte adhesion to endothelial cells. Nat. Med. 15, 300-305
46. Dixit, N., Kim, M. H., Rossaint, J., Yamayoshi, I., Zarbock, A., and Simon, S. I. (2012) Leukocyte function antigen-1, kindlin-3, and calcium flux orchestrate neutrophil recruitment during inflammation. J. Immunol. 189, 5954-5964
47. Moretti, F. A., Moser, M., Lyck, R., Abadier, M., Ruppert, R., Engelhardt, B., and Fässler, R. (2013) Kindlin-3 regulates integrin activation and adhesion reinforcement of effector T cells. Proc. Natl. Acad. Sci. U.S.A. 110, 17005-17010
48. Tidswell, M., Pachynski, R., Wu, S. W., Qiu, S. Q., Dunham, E., Cochran, N., Briskin, M. J., Kilshaw, P. J., Lazarovits, A. I., Andrew, D. P., Butcher, E. C., Yednock, T. A., and Erle, D. J. (1997) Structure-function analysis of the integrin β7 subunit-identification of domains involved in adhesion to MAdCAM-1. J. Immunol. 159, 1497-1505
49. Ma, Y. Q., Qin, J., Wu, C., and Plow, E. F. (2008) Kindlin-2 (Mig-2): a co-activator of β3 integrins. J. Cell Biol. 181, 439-446
50. Cohen, S. J., Gurevich, I., Feigelson, S. W., Petrovich, E., Moser, M., Shakhar, G., Fassler, R., and Alon, R. (2013) The integrin coactivator kindlin-3 is not required for lymphocyte diapedesis. Blood 122, 2609-2617
51. O'Toole, T. E., Katagiri, Y., Faull, R. J., Peter, K., Tamura, R., Quaranta, V., Loftus, J. C., Shattil, S. J., and Ginsberg, M. H. (1994) Integrin cytoplasmic domains mediate inside-out signal transduction. J. Cell Biol. 124, 1047-1059
52. Vinogradova, O., Velyvis, A., Velyviene, A., Hu, B., Haas, T., Plow, E., and Qin, J. (2002) A structural mechanism of integrin αIIb β3 inside-out activation as regulated by its cytoplasmic face. Cell 110, 587-597
53. Kinashi, T. (2005) Intracellular signalling controlling integrin activation in lymphocytes. Nat. Rev. Immunol. 5, 546-559
54. 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
55. Theodosiou, M., Widmaier, M., Böttcher, R. T., Rognoni, E., Veelders, M., Bharadwaj, M., Lambacher, A., Austen, K., Müller, D. J., Zent, R., and Fässler, R. (2016) Kindlin-2 cooperates with talin to activate integrins and induces cell spreading by directly binding paxillin. Elife 5, e10130
56. Hato, T., Pampori, N., and Shattil, S. J. (1998) Complementary roles for receptor clustering and conformational change in the adhesive and signaling functions of integrin αIIb β3 . J. Cell Biol. 141, 1685-1695
57. Carman, C. V., and Springer, T. A. (2003) Integrin avidity regulation: are changes in affinity and conformation underemphasized? Curr. Opin. Cell Biol. 15, 547-556
58. Chigaev, A., Zwartz, G., Graves, S. W., Dwyer, D. C., Tsuji, H., Foutz, T. D., Edwards, B. S., Prossnitz, E. R., Larson, R. S., and Sklar, L. A. (2003) α4 β1 integrin affinity changes govern cell adhesion. J. Biol. Chem. 278, 38174-38182
59. Lefort, C. T., Rossaint, J., Moser, M., Petrich, B. G., Zarbock, A., Monkley, S. J., Critchley, D. R., Ginsberg, M. H., Fässler, R., and Ley, K. (2012) Distinct roles for talin-1 and kindlin-3 in LFA-1 extension and affinity regulation. Blood 119, 4275-4282
60. 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