Connexin 37 limits thrombus propensity by downregulating platelet reactivity

Circulation

Volumn 124, Issue 8, 2011, Pages 930-939

  Angelillo Scherrer, Anne ^a   Fontana, Pierre ^b   Burnier, Laurent ^a,b,c   Roth, Isabelle ^c   Sugamele, Rocco ^a   Brisset, Anne ^a   Morel, Sandrine ^c   Nolli, Séverine ^b   Sutter, Esther ^c   Chassot, Alexandra ^c   Capron, Claude ^e   Borgel, Delphine ^e   Saller, François ^a   Chanson, Marc ^d   Kwak, Brenda R ^c  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d UNIVERSITY HOSPITAL   (Switzerland)

^e HÔPITAL AMBROISE PARÉ   (France)

Author keywords

connexin 37; gap junction; platelets; thrombosis

Indexed keywords

CONNEXIN 37; NEUROBIOTIN; TRACER; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ARTICLE; ATHEROSCLEROSIS; BLEEDING TIME; DNA POLYMORPHISM; DOWN REGULATION; GAP JUNCTION; GENE DELETION; HUMAN; HUMAN CELL; MALE; MEGAKARYOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; THROMBOCYTE; THROMBOCYTE AGGREGATION; THROMBUS;

ADOLESCENT; ADULT; ANIMALS; BIOTIN; BLEEDING TIME; BLOOD PLATELETS; CONNEXINS; DOWN-REGULATION; GAP JUNCTIONS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MEGAKARYOCYTES; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PLATELET AGGREGATION; POLYMORPHISM, GENETIC; THROMBOSIS; YOUNG ADULT;

EID: 80052176112     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.110.015479     Document Type: Article

References (51)

1. Saez JC, Berthoud VM, Branes MC, Martinez AD, Beyer EC. Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev. 2003;83:1359-1400. (Pubitemid 37222275)
2. Dobrowolski R, Willecke K. Connexin-caused genetic diseases and corresponding mouse models. Antioxid Redox Signal. 2009;11:283-295.
3. Chanson M, Kwak BR. Connexin37: a potential modifier gene of inflammatory disease. J Mol Med. 2007;85:787-795. (Pubitemid 47077108)
4. Derouette JP, Wong C, Burnier L, Morel S, Sutter E, Galan K, Brisset AC, Roth I, Chadjichristos CE, Kwak BR. Molecular role of Cx37 in advanced atherosclerosis: a micro-array study. Atherosclerosis. 2009;206: 69-76.
5. Wong CW, Christen T, Roth I, Chadjichristos CE, Derouette JP, Foglia BF, Chanson M, Goodenough DA, Kwak BR. Connexin37 protects against atherosclerosis by regulating monocyte adhesion. Nat Med. 2006; 12:950-954. (Pubitemid 44175148)
6. Listi F, Candore G, Lio D, Russo M, Colonna-Romano G, Caruso M, Hoffmann E, Caruso C. Association between c1019t polymorphism of connexin37 and acute myocardial infarction: a study in patients from Sicily. Int J Cardiol. 2005;102:269-271. (Pubitemid 40854041)
7. Yamada Y, Izawa H, Ichihara S, Takatsu F, Ishihara H, Hirayama H, Sone T, Tanaka M, Yokota M. Prediction of the risk of myocardial infarction from polymorphisms in candidate genes. N Engl J Med. 2002; 347:1916-1923. (Pubitemid 35429921)
8. Lanfear DE, Jones PG, Marsh S, Cresci S, Spertus JA, McLeod HL. Connexin37 (GJA4) genotype predicts survival after an acute coronary syndrome. Am Heart J. 2007;154:561-566. (Pubitemid 47268243)
9. Wong CW, Christen T, Pfenniger A, James RW, Kwak BR. Do allelic variants of the connexin37 1019 gene polymorphism differentially predict for coronary artery disease and myocardial infarction? Atherosclerosis. 2007;191:355-361. (Pubitemid 46400696)
10. Yeh HI, Chou Y, Liu HF, Chang SC, Tsai CH. Connexin37 gene polymorphism and coronary artery disease in Taiwan. Int J Cardiol. 2001; 81:251-255. (Pubitemid 34017445)
11. Boerma M, Forsberg L, Van Zeijl L, Morgenstern R, De Faire U, Lemne C, Erlinge D, Thulin T, Hong Y, Cotgreave IA. A genetic polymorphism in connexin 37 as a prognostic marker for atherosclerotic plaque development. J Intern Med. 1999;246:211-218. (Pubitemid 29378926)
12. Simon AM, Goodenough DA, Li E, Paul DL. Female infertility in mice lacking connexin 37. Nature. 1997;385:525-529. (Pubitemid 27074669)
13. Cazenave JP, Ohlmann P, Cassel D, Eckly A, Hechler B, Gachet C. Preparation of washed platelet suspensions from human and rodent blood. Methods Mol Biol. 2004;272:13-28.
14. Fontana P, Nolli S, Reber G, de Moerloose P. Biological effects of aspirin and clopidogrel in a randomized cross-over study in 96 healthy volunteers. J Thromb Haemost. 2006;4:813-819.
15. Kwak BR, Pepper MS, Gros DB, Meda P. Inhibition of endothelial wound repair by dominant negative connexin inhibitors. Mol Biol Cell. 2001;12:831-845. (Pubitemid 33051982)
16. Angelillo-Scherrer A, Burnier L, Flores N, Savi P, DeMol M, Schaeffer P, Herbert JM, Lemke G, Goff SP, Matsushima GK, Earp HS, Vesin C, Hoylaerts MF, Plaisance S, Collen D, Conway EM, Wehrle-Haller B, Carmeliet P. Role of gas6 receptors in platelet signaling during thrombus stabilization and implications for antithrombotic therapy. J Clin Invest. 2005;115:237-246. (Pubitemid 40385466)
17. Derouette JP, Desplantez T, Wong CW, Roth I, Kwak BR, Weingart R. Functional differences between human Cx37 polymorphic hemichannels. J Mol Cell Cardiol. 2009;46:499-507.
18. Brass LF, Zhu L, Stalker TJ. Novel therapeutic targets at the platelet vascular interface. Arterioscler Thromb Vasc Biol. 2008;28:s43-s50.
19. Nanda N, Andre P, Bao M, Clauser K, Deguzman F, Howie D, Conley PB, Terhorst C, Phillips DR. Platelet aggregation induces platelet aggregate stability via slam family receptor signaling. Blood. 2005;106: 3028-3034. (Pubitemid 41565895)
20. Prevost N, Woulfe D, Tanaka T, Brass LF. Interactions between eph kinases and ephrins provide a mechanism to support platelet aggregation once cell-to-cell contact has occurred. Proc Natl Acad Sci USA. 2002; 99:9219-9224. (Pubitemid 34764594)
21. Prevost N, Woulfe DS, Jiang H, Stalker TJ, Marchese P, Ruggeri ZM, Brass LF. Eph kinases and ephrins support thrombus growth and stability by regulating integrin outside-in signaling in platelets. Proc Natl Acad Sci USA. 2005;102:9820-9825. (Pubitemid 40993651)
22. Angelillo-Scherrer A, de Frutos P, Aparicio C, Melis E, Savi P, Lupu F, Arnout J, Dewerchin M, Hoylaerts M, Herbert J, Collen D, Dahlback B, Carmeliet P. Deficiency or inhibition of gas6 causes platelet dysfunction and protects mice against thrombosis. Nat Med. 2001;7:215-221. (Pubitemid 32148489)
23. Andre P, Prasad KS, Denis CV, He M, Papalia JM, Hynes RO, Phillips DR, Wagner DD. Cd40l stabilizes arterial thrombi by a beta3 integrin-dependent mechanism. Nat Med. 2002;8:247-252. (Pubitemid 34250102)
24. Zhu L, Bergmeier W, Wu J, Jiang H, Stalker TJ, Cieslak M, Fan R, Boumsell L, Kumanogoh A, Kikutani H, Tamagnone L, Wagner DD, Milla ME, Brass LF. Regulated surface expression and shedding support a dual role for semaphorin 4d in platelet responses to vascular injury. Proc Natl Acad Sci USA. 2007;104:1621-1626. (Pubitemid 46214640)
25. Falati S, Patil S, Gross PL, Stapleton M, Merrill-Skoloff G, Barrett NE, Pixton KL, Weiler H, Cooley B, Newman DK, Newman PJ, Furie BC, Furie B, Gibbins JM. Platelet PECAM-1 inhibits thrombus formation in vivo. Blood. 2006;107:535-541. (Pubitemid 43076376)
26. 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;98:1456-1463.
27. 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;97:1727-1732. (Pubitemid 32217240)
28. Stalker TJ, Wu J, Morgans A, Traxler EA, Wang L, Chatterjee MS, Lee D, Quertermous T, Hall RA, Hammer DA, Diamond SL, Brass LF. Endothelial cell specific adhesion molecule (ESAM) localizes to platelet-platelet contacts and regulates thrombus formation in vivo. J Thromb Haemost. 2009;7:1886-1896.
29. Goodenough DA, Paul DL. Beyond the gap: functions of unpaired connexon channels. Nat Rev Mol Cell Biol. 2003;4:285-294. (Pubitemid 36383955)
30. Bruzzone R, Haefliger JA, Gimlich RL, Paul DL. Connexin40, a component of gap junctions in vascular endothelium, is restricted in its ability to interact with other connexins. Mol Biol Cell. 1993;4:7-20. (Pubitemid 23071299)
31. Larson DM, Haudenschild CC, Beyer EC. Gap junction messenger RNA expression by vascular wall cells. Circ Res. 1990;66:1074-1080. (Pubitemid 20126437)
32. Reed KE, Westphale EM, Larson DM, Wang HZ, Veenstra RD, Beyer EC. Molecular cloning and functional expression of human connexin37, an endothelial cell gap junction protein. J Clin Invest. 1993;91:997-1004. (Pubitemid 23095274)
33. Yeh HI, Dupont E, Coppen S, Rothery S, Severs NJ. Gap junction localization and connexin expression in cytochemically identified endothelial cells of arterial tissue. J Histochem Cytochem. 1997;45:539-550. (Pubitemid 27175798)
34. Kwak BR, Mulhaupt F, Veillard N, Gros DB, Mach F. Altered pattern of vascular connexin expression in atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 2002;22:225-230. (Pubitemid 34127031)
35. Nesbitt WS, Giuliano S, Kulkarni S, Dopheide SM, Harper IS, Jackson SP. Intercellular calcium communication regulates platelet aggregation and thrombus growth. J Cell Biol. 2003;160:1151-1161. (Pubitemid 36443882)
36. Fox JE, Berndt MC. Cyclic AMP-dependent phosphorylation of glycoprotein Ib inhibits collagen-induced polymerization of actin in platelets. J Biol Chem. 1989;264:9520-9526. (Pubitemid 19157595)
37. Hauser W, Knobeloch KP, Eigenthaler M, Gambaryan S, Krenn V, Geiger J, Glazova M, Rohde E, Horak I, Walter U, Zimmer M. Megakaryocyte hyperplasia and enhanced agonist-induced platelet activation in vasodilator-stimulated phosphoprotein knockout mice. Proc Natl Acad Sci USA. 1999;96:8120-8125. (Pubitemid 29328418)
38. Wardell MR, Reynolds CC, Berndt MC, Wallace RW, Fox JE. Platelet glycoprotein Ib beta is phosphorylated on serine 166 by cyclic AMPdependent protein kinase. J Biol Chem. 1989;264:15656-15661. (Pubitemid 19242947)
39. Mazzucato M, Pradella P, Cozzi MR, De Marco L, Ruggeri ZM. Sequential cytoplasmic calcium signals in a 2-stage platelet activation process induced by the glycoprotein Ibalpha mechanoreceptor. Blood. 2002;100:2793-2800.
40. Polanowska-Grabowska R, Gear AR. Role of cyclic nucleotides in rapid platelet adhesion to collagen. Blood. 1994;83:2508-2515. (Pubitemid 24135842)
41. Sim DS, Merrill-Skoloff G, Furie BC, Furie B, Flaumenhaft R. Initial accumulation of platelets during arterial thrombus formation in vivo is inhibited by elevation of basal cAMP levels. Blood. 2004;103: 2127-2134. (Pubitemid 38326229)
42. Lawrence TS, Beers WH, Gilula NB. Transmission of hormonal stimulation by cell-to-cell communication. Nature. 1978;272:501-506. (Pubitemid 8312298)
43. Tsien RW, Weingart R. Cyclic AMP: cell-to-cell movement and inotropic effect in ventricular muscle, studied by a cut-end method. J Physiol. 1974;242:95P-96P.
44. Veitch GI, Gittens JE, Shao Q, Laird DW, Kidder GM. Selective assembly of connexin37 into heterocellular gap junctions at the oocyte/granulosa cell interface. J Cell Sci. 2004;117:2699-2707. (Pubitemid 38997253)
45. Carabatsos MJ, Sellitto C, Goodenough DA, Albertini DF. Oocytegranulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence. Dev Biol. 2000; 226:167-179.
46. Dekel N. Regulation of oocyte maturation: the role of cAMP. Ann N Y Acad Sci. 1988;541:211-216. (Pubitemid 19025501)
47. Downs SM, Daniel SA, Bornslaeger EA, Hoppe PC, Eppig JJ. Maintenance of meiotic arrest in mouse oocytes by purines: modulation of cAMP levels and cAMP phosphodiesterase activity. Gamete Res. 1989; 23:323-334. (Pubitemid 19189447)
48. Eppig JJ. The participation of cyclic adenosine monophosphate (cAMP) in the regulation of meiotic maturation of oocytes in the laboratory mouse. J Reprod Fertil Suppl. 1989;38:3-8.
49. Chadjichristos CE, Scheckenbach KE, van Veen TA, Richani Sarieddine MZ, de Wit C, Yang Z, Roth I, Bacchetta M, Viswambharan H, Foglia B, Dudez T, van Kempen MJ, Coenjaerts FE, Miquerol L, Deutsch U, Jongsma HJ, Chanson M, Kwak BR. Endothelial-specific deletion of connexin40 promotes atherosclerosis by increasing CD73-dependent leukocyte adhesion. Circulation. 2010;121:123-131.
50. Chandrasekar B, Tanguay JF. Platelets and restenosis. J Am Coll Cardiol. 2000;35:555-562. (Pubitemid 30167011)
51. Rudez G, Pons D, Leebeek F, Monraats P, Schrevel M, Zwinderman A, de Winter R, Tio R, Doevendans P, Jukema W, de Maat M. Platelet receptor p2ry12 haplotypes predict restenosis after percutaneous coronary interventions. Hum Mutat. 2008;29:375-380. (Pubitemid 351364939)