Endothelial-specific deletion of connexin40 promotes atherosclerosis by increasing CD73-dependent leukocyte adhesion

Circulation

Volumn 121, Issue 1, 2010, Pages 123-131

  Chadjichristos, C E ^a   Scheckenbach, K E L ^b   Van Veen, T A B ^c   Richani Sarieddine, M Z ^b   De Wit, C ^d   Yang, Z ^e   Roth, I ^a   Bacchetta, M ^b   Viswambharan, H ^e   Foglia, B ^a,b   Dudez, T ^b   Van Kempen, M J A ^c   Coenjaerts, F E J ^c   Miquerol, L ^f   Deutsch, U ^g   Jongsma, H J ^c   Chanson, M ^b   Kwak, B R ^a  

^a Division of Cardiology   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF LÜBECK   (Germany)

^e UNIVERSITY OF FRIBOURG   (Switzerland)

^f AIX MARSEILLE UNIVERSITÉ   (France)

^g UNIVERSITY OF BERN   (Switzerland)

Author keywords

Atherosclerosis; Connexins; Endothelium; Gap junctions; Inflammation

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; CONNEXIN 40; SMALL INTERFERING RNA; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; CHOLESTEROL DIET; CONTROLLED STUDY; GENE DELETION; HEART RATE; LEUKOCYTE ADHERENCE; LUNG CIRCULATION; MEAN ARTERIAL PRESSURE; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

5'-NUCLEOTIDASE; ANIMALS; ATHEROSCLEROSIS; CELL ADHESION; CELLS, CULTURED; CONNEXINS; ENDOTHELIAL CELLS; GAP JUNCTIONS; GREEN FLUORESCENT PROTEINS; MICE; MICE, TRANSGENIC; MONOCYTES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VASCULITIS;

EID: 74549136229     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.109.867176     Document Type: Article

References (47)

1. Murray CJ, Lopez AD. Global mortality, disability, and the contribution of risk factors: Global Burden of Disease Study. Lancet. 1997;349: 1436-1442
2. Ross R. Atherosclerosis: an inflammatory disease N Engl J Med. 1999; 340:115-126.
3. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-1695.
4. Davies PF. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med. 2009;6:16-26.
5. Tedgui A, Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev. 2006;86:515-581.
6. Weber C, Zernecke A, Libby P. The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat Rev Immunol. 2008;8:802-815.
7. Harris AL. Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys. 2001;34:325-472.
8. Sáez 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.
9. 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.
10. Kwak BR, Veillard N, Pelli G, Mulhaupt F, James RW, Chanson M, Mach F. Reduced connexin43 expression inhibits atherosclerotic lesion formation in low-density lipoprotein receptor-deficient mice. Circulation. 2003;107:1033-1039.
11. 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. Nature Med. 2006;12:950-954.
12. De Maio A, Vega VL, Contreras JE. Gap junctions, homeostasis, and injury. J Cell Physiol. 2002;191:269-282.
13. Chanson M, Derouette JP, Roth I, Foglia B, Scerri I, Dudez T, Kwak BR. Gap junctional communication in tissue inflammation and repair. Biochim Biophys Acta. 2005;1711:197-207.
14. Galkina E, Ley K. Vascular adhesion molecules in atherosclerosis. Arterioscler Thromb Vasc Biol. 2007;27:2292-2301.
15. Gabriels JE, Paul DL. Connexin43 is highly localized to sites of disturbed flow in rat aortic endothelium but connexin37 and connexin40 are more uniformly distributed. Circ Res. 1998;83:636-643.
16. van Kempen MJ, Jongsma HJ. Distribution of Connexin37, Connexin40 and Connexin43 in the aorta and coronary artery of several mammals. Histochem Cell Biol. 1999;112:479-486.
17. de Wit C, Roos F, Bolz SS, Kirchhoff S, Krüger O, Willecke K, Pohl U. Impaired conduction of vasodilation along arterioles in connexin40-deficient mice. Circ Res. 2000;86:649-655.
18. de Wit C, Roos F, Bolz SS, Pohl U. Lack of vascular connexin 40 is associated with hypertension and irregular arteriolar vasomotion. Physiol Genomics. 2003;13:169-177.
19. Morabito L, Montesinos MC, Schreibmann DM, Balter L, Thomson LF, Resta R, Carlin G, Huie MA, Cronstein BN. Methotrexate and sulfasalazine promote adenosine release by a mechanism that requires ecto-5'-nucleotidase-mediated conversion of adenine nucleotides. J Clin Invest. 1998;101:295-300.
20. Simon AM, McWhorter AR. Decreased intercellular dye-transfer and downregulation of non-ablated connexins in aortic endothelium deficient in connexin37 or connexin40. J Cell Sci. 2003;116:2223-2236.
21. Veillard NR, Steffens S, Burger F, Pelli G, Mach F. Differential expression patterns of proinflammatory and anti-inflammatory mediators during atherogenesis in mice. Arterioscler Thromb Vasc Biol. 2004;24: 2339-2344.
22. Zernecke A, Bidzhekov K, Ozüyaman B, Fraemohs L, Liehn EA, Lüscher-Firzlaff JM, Lüscher B, Schrader J, Weber C. CD73/ecto-5'-nucleotidase protects against vascular inflammation and neointima formation. Circulation. 2006;113:2120-2127.
23. Koni PA, Joshi SK, Temann UA, Olson D, Burkly L, Flavell RA. Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J Exp Med. 2001;193:741-754.
24. Lennon PF, Taylor CT, Stahl GL, Colgan SP. Neutrophil-derived 5'-adenosine monophosphate promotes endothelial barrier function via CD73-mediated conversion to adenosine and endothelial A2B receptor activation. J Exp Med. 1998;188:1433-1443.
25. Narravula S, Lennon PF, Mueller BU, Colgan CP. Regulation of endothelial CD73 by adenosine: paracrine pathway for enhanced endothelial barrier function. J Immunol. 2000;165:5262-5268.
26. van Rijen H, van Kempen MJ, Analbers LJ, Rook MB, van Ginneken AC, Gros D, Jongsma HJ. Gap junctions in human umbilical cord endothelial cells contain multiple connexins. Am J Physiol. 1997;272:C117-C130.
27. Haseqawa T, Bouïs D, Liao H, Visovatti SH, Pinsky DJ. Ecto-5' nucleotidase (CD73)-mediated adenosine generation and signaling in murine cardiac allograft vasculopathy. Circ Res. 2008;103:1410-1421.
28. Kwak BR, MS Pepper, DB Gros, Meda P. Inhibition of endothelial wound repair by dominant negative connexin inhibitors. Mol Biol Cell. 2001;12:831-845.
29. Montesinos MC, Takedachi M, Thompson LF, Wilder TF, Fernández P, Cronstein BN. The antiinflammatory mechanism of methotrexate depends on extracellular conversion of adenine nucleotides to adenosine by ecto-5'-nucleotidase: findings in a study of ecto-5'-nucleotidase gene-deficient mice. Arthritis Rheum. 2007;56:1440-1445.
30. Krattinger N, Capponi A, Mazzolai L, Aubert JF, Caille D, Nicod P, Waeber G, Meda P, Haefliger JA. Connexin40 regulates renin production and blood pressure. Kidney Int. 2007;72:814-822.
31. Wagner C, de Wit C, Kurtz L, Grunberger C, Kurtz A, Schweda F. Connexin40 is essential for the pressure control of renin synthesis and secretion. Circ Res. 2007;100:556-563.
32. Helderman F, Segers D, de Crom R, Hierck BP, Poelmann RE, Evans PC, Krams R. Effect of shear stress on vascular inflammation and plaque development. Curr Opin Lipidol. 2007;18:527-533.
33. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7:678-689.
34. Cybulsky MI, Iiyama K, Li H, Zhu S, Chen M, Iiyama M, Davis V, Gutierrez-Ramos J-C, Connelly PW, Milstone DS. A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest. 2001; 107:1255-1262.
35. Koszalka P, Ozuyaman B, Huo Y, Zemecke A, Flogel U, Braun N, Buchheiser A, Decking UK, Smith ML, Sévigny J, Gear A, Weber AA, Molojavyi A, Ding Z, Weber C, Ley K, Zimmermann H, Gödecke A, Schrader J. Targeted disruption of cd73/ecto-5'-nucleotidase alters throm-boregulation and augments vascular inflammatory response. Circ Res. 2004;95:814-821.
36. Thomson LF, Eltzschig HK, Ibla JC, Van de Wiele CJ, Resta R, Morote-Garcia JC, Colgan SP. Crucial role for ecto-5'-nucleotidase (CD73) in vascular leakage during hypoxia. J Exp Med. 2004;200:1395-1405.
37. Buchheiser A, Emde B, Fischer JW, Schrader J. Role of CD73-derived adenosine in atherosclerosis. Circulation. 2007;116:II-114. Abstract 623.
38. Bouis D, McCubbrey AL, Hyman MC, Thompson LF, Pinsky DJ. Bimodal atherogenic effects of CD73 in apolipoprotein E deficient mice. Arterioscler Thromb Vasc Biol. 2008;28:e115. Abstract P452.
39. Stelzner TJ, Weil JV, O'Brian RF. Role of cyclic adenosine monophosphate in the induction of endothelial barrier properties. J Cell Physiol. 1989;139:157-166.
40. Hansen KR, Resta R, Webb CF, Thompson LF. Isolation and characterization of the promoter of the human 5'-nucleotidase (CD73)-encoding gene. Gene. 1995;167:307-312.
41. Eltzschig HK, Eckle T, Mager A, Küper N, Karcher C, Weismüller T, Boengler K, Schulz R, Robson SC, Colgan SP. ATP release form activated macrophages occurs via connexin 43 and modulates adenosine-dependent endothelial cell function. Circ Res. 2006;99:1100-1108.
42. Kanaporis G, Mese G, Valiuniene L, White TW, Brink PR, Valiunas V. Gap junction channels exhibit connexin-specific permeability to cyclic nucleotides. J Gen Physiol. 2008;131:293-305.
43. van Rijen HV, van Veen TA, Hermans MM, Jongsma HJ. Human con-nexin40 gap junction channels are modulated by cAMP. Cardiovasc Res. 2000;45:941-951.
44. Lewis BM, Pexa A, Francic K, Verma V, McNicol AM, Scanlon M, Deussen A, Evans WH, Rees DA, Ham J. Adenosine stimulates con-nexin43 expression and gap junctional communication in pituitary fol-liculostellate cells. FASEB J. 2006;20:2585-2587.
45. Volmer JB, Thompson LF, Blackburn MR. Ecto-5'-nucleotidase (CD73)-mediated adenosine production is tissue protective in a model of bleomycin-induced lung injury. J Immunol. 2006;6:4449-4458.
46. Eckle T, Füllbier L, Wehrmann M, Khoury J, Mittelbronn M, Ibla J, Rosenberger P, Eltzschig HK. Identification of ectonucleotidases CD39 and CD73 in innate protection during acute lung injury. J Immunol. 2007;178:8127-8137.
47. Firouzi M, Kok B, Spiering W, Busjahn A, Bezzina CR, Ruijter JM, Koeleman BP, Schipper M, Groenewegen WA, Jongsma HJ, de Leeuw PW. Polymorphisms in human connexin40 gene promoter are associated with increased risk of hypertension in men. J Hypertens. 2006;24: 325-330.