Interaction of kindlin-2 with integrin β3 promotes outside-in signaling responses by the αVβ3 vitronectin receptor

Blood

Volumn 125, Issue 12, 2015, Pages 1995-2004

  Liao, Zhongji ^a   Kato, Hisashi ^a   Pandey, Manjula ^a   Cantor, Joseph M ^a   Ablooglu, Ararat J ^a   Ginsberg, Mark H ^a   Shattil, Sanford J ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; CELL PROTEIN; KINDLIN 2; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2; VITRONECTIN; VITRONECTIN RECEPTOR; CYTOSKELETON PROTEIN; KINDLIN-2 PROTEIN, MOUSE; MEMBRANE PROTEIN; MIG2B PROTEIN, HUMAN; MUSCLE PROTEIN; PROTEIN BINDING; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; CANCER GROWTH; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; IN VITRO STUDY; LIGAND BINDING; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RETINA BLOOD VESSEL; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION; WESTERN BLOTTING; WILD TYPE; ANIMAL; CANCER TRANSPLANTATION; CELL MOTION; CYTOPLASM; EXPERIMENTAL MELANOMA; HUMAN; METABOLISM; MUTATION; NEOVASCULARIZATION (PATHOLOGY); PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; THROMBOCYTE;

ANIMALS; BLOOD PLATELETS; BONE MARROW TRANSPLANTATION; CELL MOVEMENT; CYTOPLASM; CYTOSKELETAL PROTEINS; ENDOTHELIAL CELLS; HUMANS; INTEGRIN ALPHAVBETA3; INTEGRIN BETA3; MELANOMA, EXPERIMENTAL; MEMBRANE PROTEINS; MICE; MUSCLE PROTEINS; MUTATION; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84925379438     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-09-603035     Document Type: Article

References (65)

1. Bennett JS. Structure and function of the platelet integrin alphaIIbbeta3. J Clin Invest. 2005;115(12):3363-3369.
2. Coller BS, Shattil SJ. The GPIIb/IIIa (integrin alphaIIbbeta3) odyssey: a technology-driven saga of a receptor with twists, turns, and even a bend. Blood. 2008;112(8):3011-3025.
3. Felding-Habermann B, Cheresh DA. Vitronectin and its receptors. Curr Opin Cell Biol. 1993;5(5):864-868.
4. Brooks PC, Montgomery AM, Rosenfeld M, et al. Integrin α v β 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell. 1994;79(7):1157-1164.
5. Reynolds LE, Wyder L, Lively JC, et al. Enhanced pathological angiogenesis in mice lacking β3 integrin or β3 and β5 integrins. Nat Med. 2002;8(1):27-34.
6. Steri V, Ellison TS, Gontarczyk AM, et al. Acute depletion of endothelial β3-integrin transiently inhibits tumor growth and angiogenesis in mice. Circ Res. 2014;114(1):79-91.
7. Mahabeleshwar GH, Feng W, Phillips DR, Byzova TV. Integrin signaling is critical for pathological angiogenesis. J Exp Med. 2006;203(11):2495-2507.
8. Shattil SJ, Kim C, Ginsberg MH. The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol. 2010;11(4):288-300.
9. Bouvard D, Pouwels J, De Franceschi N, Ivaska J. Integrin inactivators: balancing cellular functions in vitro and in vivo. Nat Rev Mol Cell Biol. 2013;14(7):430-442.
10. Calderwood DA, Fujioka Y, de Pereda JM, et al. Integrin β cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc Natl Acad Sci USA. 2003;100(5):2272-2277.
11. Ma YQ, Qin J, Wu C, Plow EF. Kindlin-2 (Mig-2): a co-activator of β3 integrins. J Cell Biol. 2008;181(3):439-446.
12. Bledzka K, Bialkowska K, Nie H, et al. Tyrosine phosphorylation of integrin β3 regulates kindlin-2 binding and integrin activation. J Biol Chem. 2010;285(40):30370-30374.
13. Ablooglu AJ, Kang J, Petrich BG, Ginsberg MH, Shattil SJ. Antithrombotic effects of targeting alphaIIbbeta3 signaling in platelets. Blood. 2009;113(15):3585-3592.
14. Desgrosellier JS, Lesperance J, Seguin L, et al. Integrin αvβ3 drives slug activation and stemness in the pregnant and neoplastic mammary gland. Dev Cell. 2014;30(3):295-308.
15. Desgrosellier JS, Barnes LA, Shields DJ, et al. An integrin α(v)β(3)-c-Src oncogenic unit promotes anchorage-independence and tumor progression. Nat Med. 2009;15(10):1163-1169.
16. Cowan KJ, Law DA, Phillips DR. Identification of shc as the primary protein binding to the tyrosinephosphorylated β 3 subunit of α IIbbeta 3 during outside-in integrin platelet signaling. J Biol Chem. 2000;275(46):36423-36429.
17. Bandyopadhyay A, Rothschild G, Kim S, Calderwood DA, Raghavan S. Functional differences between kindlin-1 and kindlin-2 in keratinocytes. J Cell Sci. 2012;125(Pt 9):2172-2184.
18. Harburger DS, Bouaouina M, Calderwood DA. Kindlin-1 and -2 directly bind the C-terminal region of β integrin cytoplasmic tails and exert integrinspecific activation effects. J Biol Chem. 2009;284(17):11485-11497.
19. Montanez E, Ussar S, Schifferer M, et al. Kindlin-2 controls bidirectional signaling of integrins. Genes Dev. 2008;22(10):1325-1330.
20. Plow EF, Qin J, Byzova T. Kindling the flame of integrin activation and function with kindlins. Curr Opin Hematol. 2009;16(5):323-328.
21. Karaköse E, Schiller HB, Fässler R. The kindlins at a glance. J Cell Sci. 2010;123(Pt 14):2353-2356.
22. Lefort CT, Rossaint J, Moser M, et al. Distinct roles for talin-1 and kindlin-3 in LFA-1 extension and affinity regulation. Blood. 2012;119(18):4275-4282.
23. Moser M, Nieswandt B, Ussar S, Pozgajova M, Fässler R. Kindlin-3 is essential for integrin activation and platelet aggregation. Nat Med. 2008;14(3):325-330.
24. Morrison VL, MacPherson M, Savinko T, Lek HS, Prescott A, Fagerholm SC. The β2 integrin-kindlin-3 interaction is essential for T-cell homing but dispensable for T-cell activation in vivo. Blood. 2013;122(8):1428-1436.
25. Pluskota E, Dowling JJ, Gordon N, et al. The integrin coactivator kindlin-2 plays a critical role in angiogenesis in mice and zebrafish. Blood. 2011;117(18):4978-4987.
26. Pluskota E, Ma Y, Bledzka KM, et al. Kindlin-2 regulates hemostasis by controlling endothelial cell surface expression of ADP/AMP catabolic enzymes via a clathrin-dependent mechanism. Blood. 2013;122(14):2491-2499.
27. Arias-Salgado EG, Lizano S, Sarkar S, Brugge JS, Ginsberg MH, Shattil SJ. Src kinase activation by direct interaction with the integrin βcytoplasmic domain. Proc Natl Acad Sci USA. 2003;100(23):13298-13302.
28. Arias-Salgado EG, Lizano S, Shattil SJ, Ginsberg MH. Specification of the direction of adhesive signaling by the integrin β cytoplasmic domain. J Biol Chem. 2005;280(33):29699-29707.
29. Fitzpatrick P, Shattil SJ, Ablooglu AJ. C-terminal COOH of integrin β1 is necessary for β1 association with the kindlin-2 adapter protein. J Biol Chem. 2014;289(16):11183-11193.
30. Kato H, Liao Z, Mitsios JV, et al. The primacy of β1 integrin activation in the metastatic cascade. PLoS ONE. 2012;7(10):e46576.
31. Calderwood DA, Zent R, Grant R, Rees DJ, Hynes RO, Ginsberg MH. The Talin head domain binds to integrin β subunit cytoplasmic tails and regulates integrin activation. J Biol Chem. 1999;274(40):28071-28074.
32. Pampori N, Hato T, Stupack DG, et al. Mechanisms and consequences of affinity modulation of integrin α(V)β(3) detected with a novel patch-engineered monovalent ligand. J Biol Chem. 1999;274(31):21609-21616.
33. Kiosses WB, Shattil SJ, Pampori N, Schwartz MA. Rac recruits high-affinity integrin alphavbeta3 to lamellipodia in endothelial cell migration. Nat Cell Biol. 2001;3(3):316-320.
34. Nakatsu MN, Davis J, Hughes CC. Optimized fibrin gel bead assay for the study of angiogenesis. J Vis Exp. 2007;(3):186.
35. Newman AC, Nakatsu MN, Chou W, Gershon PD, Hughes CC. The requirement for fibroblasts in angiogenesis: fibroblast-derived matrix proteins are essential for endothelial cell lumen formation. Mol Biol Cell. 2011;22(20):3791-3800.
36. Scheppke L, Aguilar E, Gariano RF, et al. Retinal vascular permeability suppression by topical application of a novel VEGFR2/Src kinase inhibitor in mice and rabbits. J Clin Invest. 2008;118(6):2337-2346.
37. Pitulescu ME, Schmidt I, Benedito R, Adams RH. Inducible gene targeting in the neonatal vasculature and analysis of retinal angiogenesis in mice. Nat Protoc. 2010;5(9):1518-1534.
38. Liu S, Calderwood DA, Ginsberg MH. Integrin cytoplasmic domain-binding proteins. J Cell Sci. 2000;113(Pt 20):3563-3571.
39. Leisner TM, Yuan W, DeNofrio JC, Liu J, Parise LV. Tickling the tails: cytoplasmic domain proteins that regulate integrin alphaIIbbeta3 activation. Curr Opin Hematol. 2007;14(3):255-261.
40. Morse EM, Brahme NN, Calderwood DA. Integrin cytoplasmic tail interactions. Biochemistry. 2014;53(5):810-820.
41. Greenwood J, Pryce G, Devine L, et al. SV40 large T immortalised cell lines of the rat bloodbrain and blood-retinal barriers retain their phenotypic and immunological characteristics. J Neuroimmunol. 1996;71(1-2):51-63.
42. Eliceiri BP, Cheresh DA. The role of alphav integrins during angiogenesis. Mol Med. 1998;4(12):741-750.
43. De Smet F, Segura I, De Bock K, Hohensinner PJ, Carmeliet P. Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler Thromb Vasc Biol. 2009;29(5):639-649.
44. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer. 2010;10(1):9-22.
45. Chen J, Zheng XF, Brown EJ, Schreiber SL. Identification of an 11-kDa FKBP12-rapamycinbinding domain within the 289-kDa FKBP12-rapamycin-associated protein and characterization of a critical serine residue. Proc Natl Acad Sci USA. 1995;92(11):4947-4951.
46. Castellano F, Montcourrier P, Guillemot JC, et al. Inducible recruitment of Cdc42 or WASP to a cell-surface receptor triggers actin polymerization and filopodium formation. Curr Biol. 1999;9(7):351-360.
47. Shi X, Ma YQ, Tu Y, et al. The MIG-2/integrin interaction strengthens cell-matrix adhesion and modulates cell motility. J Biol Chem. 2007;282(28):20455-20466.
48. Byzova TV, Goldman CK, Pampori N, et al. A mechanism for modulation of cellular responses to VEGF: activation of the integrins. Mol Cell. 2000;6(4):851-860.
49. Uemura A, Kusuhara S, Katsuta H, Nishikawa S. Angiogenesis in the mouse retina: a model system for experimental manipulation. Exp Cell Res. 2006;312(5):676-683.
50. Gerhardt H, Golding M, Fruttiger M, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161(6):1163-1177.
51. Herzig M, Christofori G. Recent advances in cancer research: mouse models of tumorigenesis. Biochim Biophys Acta. 2002;1602(2):97-113.
52. Okamoto R, Ueno M, Yamada Y, et al. Hematopoietic cells regulate the angiogenic switch during tumorigenesis. Blood. 2005;105(7):2757-2763.
53. Takakura N, Watanabe T, Suenobu S, et al. A role for hematopoietic stem cells in promoting angiogenesis. Cell. 2000;102(2):199-209.
54. Feng W, McCabe NP, Mahabeleshwar GH, Somanath PR, Phillips DR, Byzova TV. The angiogenic response is dictated by β3 integrin on bone marrow-derived cells. J Cell Biol. 2008;183(6):1145-1157.
55. Monkley SJ, Zhou XH, Kinston SJ, et al. Disruption of the talin gene arrests mouse development at the gastrulation stage. Dev Dyn. 2000;219(4):560-574.
56. Criscuoli ML, Nguyen M, Eliceiri BP. Tumor metastasis but not tumor growth is dependent on Src-mediated vascular permeability. Blood. 2005;105(4):1508-1514.
57. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell. 1999;4(6):915-924.
58. Malinin NL, Zhang L, Choi J, et al. A point mutation in KINDLIN3 ablates activation of three integrin subfamilies in humans. Nat Med. 2009;15(3):313-318.
59. Xu Z, Chen X, Zhi H, et al. Direct interaction of kindlin-3 with integrin αIIbß3 in platelets is required for supporting arterial thrombosis in mice. Arterioscler Thromb Vasc Biol. 2014;34(9):1961-1967.
60. Werdich XQ, Penn JS. Src, Fyn and Yes play differential roles in VEGF-mediated endothelial cell events. Angiogenesis. 2005;8(4):315-326.
61. Bialkowska K, Ma YQ, Bledzka K, et al. The integrin co-activator Kindlin-3 is expressed and functional in a non-hematopoietic cell, the endothelial cell. J Biol Chem. 2010;285(24):18640-18649.
62. Danhier F, Le Breton A, Préat V. RGD-based strategies to target α(v) β(3) integrin in cancer therapy and diagnosis. Mol Pharm. 2012;9(11):2961-2973.
63. Goodman SL, Picard M. Integrins as therapeutic targets. Trends Pharmacol Sci. 2012;33(7):405-412.
64. Su X, Mi J, Yan J, et al. RGT, a synthetic peptide corresponding to the integrin β 3 cytoplasmic C-terminal sequence, selectively inhibits outsidein signaling in human platelets by disrupting the interaction of integrin α IIb β 3 with Src kinase. Blood. 2008;112(3):592-602.
65. Xiao R, Xi XD, Chen Z, Chen SJ, Meng G. Structural framework of c-Src activation by integrin β3. Blood. 2013;121(4):700-706.