JAM-A protects from thrombosis by suppressing integrin α IIbβ3-dependent outside-in signaling in platelets

Blood

Volumn 119, Issue 14, 2012, Pages 3352-3360

  Naik, Meghna U ^a   Stalker, Timothy J ^b   Brass, Lawrence F ^b   Naik, Ulhas P ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRINOGEN RECEPTOR; INTEGRIN; JUNCTIONAL ADHESION MOLECULE A; PROTEIN INTEGRIN ALPHA2BBETA3; THROMBOXANE A2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CLOT RETRACTION; CONTROLLED STUDY; EX VIVO STUDY; HUMAN; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBOSIS;

EID: 84859583115     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-12-397398     Document Type: Article

References (50)

1. Broos K, Feys HB, De Meyer SF, Vanhoorelbeke K, Deckmyn H. Platelets at work in primary hemostasis. Blood Rev. 2011;25(4):155-167.
2. Hughes PE, Pfaff M. Integrin affinity modulation. Trends Cell Biol. 1998;8(9):359-364. (Pubitemid 28398427)
3. Shattil SJ. Signaling through platelet integrin alpha IIb beta 3: inside-out, outside-in, and sideways. Thromb Haemost. 1999;82(2):318-325.
4. Rivera J, Lozano ML, Navarro-Nunez L, Vicente V. Platelet receptors and signaling in the dynamics of thrombus formation. Haematologica. 2009;94(5):700-711.
5. Li Z, Delaney MK, O'Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol. 2010;30(12):2341-2349.
6. Kornecki E, Walkowiak B, Naik UP, Ehrlich YH. Activation of human platelets by a stimulatory monoclonal antibody. J Biol Chem. 1990;265(17):10042-10048.
7. Naik UP, Ehrlich YH, Kornecki E. Mechanisms of platelet activation by a stimulatory antibody: cross-linking of a novel platelet receptor for monoclonal antibody F11 with the Fc gamma RII receptor. Biochem J. 1995;310(pt 1):155-162.
8. Babinska A, Kedees MH,Athar H, et al. F11-receptor (F11R/JAM) mediates platelet adhesion to endothelial cells: role in inflammatory thrombosis. Thromb Haemost. 2002;88(5):843-850. (Pubitemid 35350778)
9. Babinska A, Kedees MH, Athar H, et al. Two regions of the human platelet F11-receptor (F11R) are critical for platelet aggregation, potentiation and adhesion. Thromb Haemost. 2002;87(4):712-721. (Pubitemid 34308431)
10. Sobocka MB, Sobocki T, Babinska A, et al. Signaling pathways of the F11 receptor (F11R; a.k.a. JAM-1, JAM-A) in human platelets: F11R dimerization, phosphorylation and complex formation with the integrin GPIIIa. J Recept Signal Transduct Res. 2004;24(1-2):85-105. (Pubitemid 39011291)
11. Sobocka MB, Sobocki T, Banerjee P, et al. Cloning of the human platelet F11 receptor: a cell adhesion molecule member of the immunoglobulin superfamily involved in platelet aggregation. Blood. 2000;95(8):2600-2609. (Pubitemid 30210539)
12. Ozaki H, Ishii K, Arai H, et al. Junctional adhesion molecule (JAM) is phosphorylated by protein kinase C upon platelet activation. Biochem Biophys Res Commun. 2000;276(3):873-878.
13. Aurrand-Lions M, Johnson-Leger C, Wong C, Du Pasquier L, Imhof BA. Heterogeneity of endothelial junctions is reflected by differential expression and specific subcellular localization of the three JAM family members. Blood. 2001;98(13):3699-3707.
14. Naik UP, Eckfeld K. Junctional adhesion molecule 1 (JAM-1). J Biol Regul Homeost Agents. 2003;17(4):341-347. (Pubitemid 38443667)
15. Mandell KJ, Babbin BA, Nusrat A, Parkos CA. Junctional adhesion molecule 1 regulates epithelial cell morphology through effects on beta1 integrins and Rap1 activity. J Biol Chem. 2005;280(12):11665-11674. (Pubitemid 40418481)
16. Naik MU, Mousa SA, Parkos CA, Naik UP. Signaling through JAM-1 and alphavbeta3 is required for the angiogenic action of bFGF: dissociation of the JAM-1 and alphavbeta3 complex. Blood. 2003;102(6):2108-2114. (Pubitemid 37122387)
17. Cooke VG, Naik MU, Naik UP. Fibroblast growth factor-2 failed to induce angiogenesis in junctional adhesion molecule-A-deficient mice. Arterioscler Thromb Vasc Biol. 2006;26(9):2005-2011. (Pubitemid 44253781)
18. Parris JJ, Cooke VG, Skarnes WC, Duncan MK, Naik UP. JAM-A expression during embryonic development. Dev Dyn. 2005;233(4):1517-1524. (Pubitemid 40995149)
19. Naik UP, Naik MU. Association of CIB with GPIIb/IIIa during outside-in signaling is required for platelet spreading on fibrinogen. Blood. 2003;102(4):1355-1362. (Pubitemid 36988043)
20. Naik MU, Nigam A, Manrai P, et al. CIB1 deficiency results in impaired thrombosis: the potential role of CIB1 in outside-in signaling through integrin alpha IIb beta 3. J Thromb Haemost. 2009;7(11):1906-1914.
21. Naik MU, Naik UP. Contra-regulation of calcium-and integrin-binding protein 1-induced cell migration on fibronectin by PAK1 and MAP kinase signaling. J Cell Biochem. 2011;112(11):3289-3299.
22. Goodman SL. Sheep, pig, and human platelet-material interactions with model cardiovascular biomaterials. J Biomed Mater Res. 1999;45(3):240-250. (Pubitemid 29165940)
23. Falati S, Gross P, Merrill-Skoloff G, Furie BC, Furie B. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat Med. 2002;8(10):1175-1181.
24. Stalker TJ, Wu J, Morgans A, et al. Endothelial cell specific adhesion molecule (ESAM) localizes to platelet-platelet contacts and regulates thrombus formation in vivo. J Thromb Haemost. 2009;7(11):1886-1896.
25. Weiss EJ, Hamilton JR, Lease KE, Coughlin SR. Protection against thrombosis in mice lacking PAR3. Blood. 2002;100(9):3240-3244. (Pubitemid 35217073)
26. Suzuki-Inoue K, Hughes CE, Inoue O, et al. Involvement of Src kinases and PLCgamma2 in clot retraction. Thromb Res. 2007;120(2):251-258. (Pubitemid 46778747)
27. Kang LI, Wang Y, Suckow AT, et al. Deletion of JAM-A causes morphological defects in the corneal epithelium. Int J Biochem Cell Biol. 2007;39(3):576-585. (Pubitemid 46096795)
28. Shao M, Ghosh A, Cooke VG, Naik UP, Martin-DeLeon PA. JAM-A is present in mammalian spermatozoa where it is essential for normal motility. Dev Biol. 2008;313(1):246-255. (Pubitemid 350298312)
29. Chen C, Li Q, Darrow AL, et al. Mer receptor tyrosine kinase signaling participates in platelet function. Arterioscler Thromb Vasc Biol. 2004;24(6):1118-1123. (Pubitemid 38737840)
30. Ling Q, Jacovina AT, Deora A, et al. Annexin II regulates fibrin homeostasis and neoangiogenesis in vivo. J Clin Invest. 2004;113(1):38-48. (Pubitemid 38541630)
31. Angelillo-Scherrer A, de Frutos P, Aparicio C, et al. Deficiency or inhibition of Gas6 causes platelet dysfunction and protects mice against thrombosis. Nat Med. 2001;7(2):215-221. (Pubitemid 32148489)
32. Bergmeier W, Schulte V, Brockhoff G, Bier U, Zirngibl H, Nieswandt B. Flow cytometric detection of activated mouse integrin alphaIIbbeta3 with a novel monoclonal antibody. Cytometry. 2002;48(2):80-86. (Pubitemid 34591919)
33. Patil S, Newman DK, Newman PJ. Platelet endothelial cell adhesion molecule-1 serves as an inhibitory receptor that modulates platelet responses to collagen. Blood. 2001;97(6):1727-1732. (Pubitemid 32217240)
34. Flevaris P, Stojanovic A, Gong H, Chishti A, Welch E, Du X. A molecular switch that controls cell spreading and retraction. J Cell Biol. 2007;179(3):553-565. (Pubitemid 350074797)
35. Gong H, Shen B, Flevaris P, et al. G protein subunit Galpha13 binds to integrin alphaIIbbeta3 and mediates integrin "outside-in" signaling. Science. 2010;327(5963):340-343.
36. Boylan B, Gao C, Rathore V, Gill JC, Newman DK, Newman PJ. Identification of FcgammaRIIa as the ITAM-bearing receptor mediating alphaIIbbeta3 outside-in integrin signaling in human platelets. Blood. 2008;112(7):2780-2786.
37. Obergfell A, Eto K, Mocsai A, et al. Coordinate interactions of Csk, Src, and Syk kinases with [alpha]IIb[beta]3 initiate integrin signaling to the cytoskeleton. J Cell Biol. 2002;157(2):265-275. (Pubitemid 34839823)
38. Jackson DE, Ward CM, Wang R, Newman PJ. The protein-tyrosine phosphatase SHP-2 binds platelet/endothelial cell adhesion molecule-1 (PECAM-1) and forms a distinct signaling complex during platelet aggregation. Evidence for a mechanistic link between PECAM-1- and integrin-mediated cellular signaling. J Biol Chem. 1997;272(11):6986-6993. (Pubitemid 27166399)
39. Gibbins JM. The negative regulation of platelet function: extending the role of the ITIM. Trends Cardiovasc Med. 2002;12(5):213-219. (Pubitemid 34823631)
40. Hirata K, Ishida T, Penta K, et al. Cloning of an immunoglobulin family adhesion molecule selectively expressed by endothelial cells. J Biol Chem. 2001;276(19):16223-16231.
41. Muller MM, Klaile E, Vorontsova O, Singer BB, Obrink B. Homophilic adhesion and CEACAM1-S regulate dimerization of CEACAM1-L and recruitment of SHP-2 and c-Src. J Cell Biol. 2009;187(4):569-581.
42. Sun J, Williams J, Yan HC, Amin KM, Albelda SM, DeLisser HM. Platelet endothelial cell adhesion molecule-1 (PECAM-1) homophilic adhesion is mediated by immunoglobulin-like domains 1 and 2 and depends on the cytoplasmic domain and the level of surface expression. J Biol Chem. 1996;271(31):18561-18570. (Pubitemid 26322717)
43. Falati S, Patil S, Gross PL, et al. Platelet PECAM-1 inhibits thrombus formation in vivo. Blood. 2006;107(2):535-541. (Pubitemid 43076376)
44. Wong C, Liu Y, Yip J, et al. CEACAM1 negatively regulates platelet-collagen interactions and thrombus growth in vitro and in vivo. Blood. 2009;113(8):1818-1828.
45. Henshall TL, Jones KL, Wilkinson R, Jackson DE. Src homology 2 domain-containing proteintyrosine phosphatases, SHP-1 and SHP-2, are required for platelet endothelial cell adhesion molecule-1/CD31-mediated inhibitory signaling. J Immunol. 2001;166(5):3098-3106. (Pubitemid 33117306)
46. Huber M, Izzi L, Grondin P, et al. The carboxylterminal region of biliary glycoprotein controls its tyrosine phosphorylation and association with protein-tyrosine phosphatases SHP-1 and SHP-2 in epithelial cells. J Biol Chem. 1999;274(1):335-344. (Pubitemid 29035067)
47. Jones KL, Hughan SC, Dopheide SM, Farndale RW, Jackson SP, Jackson DE. Platelet endothelial cell adhesion molecule-1 is a negative regulator of platelet-collagen interactions. Blood. 2001;98(5):1456-1463.
48. Ostermann G,Weber KS, Zernecke A, Schroder A, Weber C. JAM-1 is a ligand of the beta(2) integrin LFA-1 involved in transendothelial migration of leukocytes. Nat Immunol. 2002;3(2):151-158. (Pubitemid 34141445)
49. Ablooglu AJ, Kang J, Petrich BG, Ginsberg MH, Shattil SJ. Antithrombotic effects of targeting alphaIIbbeta3 signaling in platelets. Blood. 2009;113(15):3585-3592.
50. Su X, Mi J, Yan J, et al. 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. 2008;112(3):592-602.