The extracellular matrix metalloproteinase inducer EMMPRIN is a target of nitric oxide in myocardial ischemia/reperfusion

Free Radical Biology and Medicine

Volumn 51, Issue 2, 2011, Pages 387-395

  Tarin, Carlos ^a   Lavin, Begoña ^a   Gomez, Monica ^a   Saura, Marta ^b   Diez Juan, Antonio ^c   Zaragoza, Carlos ^a  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b UNIVERSITY OF ALCALÁ   (Spain)

^c CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

EMMPRIN; Free radicals; Ischemia reperfusion; Mice; MMP; Nitric oxide

Indexed keywords

CD147 ANTIGEN; CYCLIC GMP DEPENDENT PROTEIN KINASE; EMMPRIN ANTIBODY; IMMUNOGLOBULIN G; INDUCIBLE NITRIC OXIDE SYNTHASE; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; NEUTRALIZING ANTIBODY; NITRIC OXIDE; NITROPRUSSIDE SODIUM; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; EXTRACELLULAR MATRIX; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; TRANSCRIPTION INITIATION;

ANIMALS; ANTIGENS, CD147; BASE SEQUENCE; CELLS, CULTURED; DNA PRIMERS; MICE; MICE, KNOCKOUT; MYOCARDIAL REPERFUSION INJURY; NITRIC OXIDE; PROMOTER REGIONS, GENETIC;

MUS;

EID: 79959343142     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.04.021     Document Type: Article

References (36)

1. H. Takano, S. Manchikalapudi, X.L. Tang, Y. Qiu, A. Rizvi, and A.K. Jadoon Nitric oxide synthase is the mediator of late preconditioning against myocardial infarction in conscious rabbits Circulation 98 1998 441 449 (Pubitemid 28357947)
2. Q. Li, Y. Guo, Q. Ou, C. Cui, W.J. Wu, and W. Tan Gene transfer of inducible nitric oxide synthase affords cardioprotection by upregulating heme oxygenase-1 via a nuclear factor-κB-dependent pathway Circulation 120 2009 1222 1230
3. Y. Wang, E. Kodani, J. Wang, S.X. Zhang, H. Takano, and X.L. Tang Cardioprotection during the final stage of the late phase of ischemic preconditioning is mediated by neuronal NO synthase in concert with cyclooxygenase-2 Circ. Res. 95 2004 84 91 (Pubitemid 38931839)
4. Q. Li, Y. Guo, W. Tan, Q. Ou, W.J. Wu, and D. Sturza Cardioprotection afforded by inducible nitric oxide synthase gene therapy is mediated by cyclooxygenase-2 via a nuclear factor-kappaB dependent pathway Circulation 116 2007 1577 1584 (Pubitemid 47511421)
5. N. Harada, T. Miura, Y. Dairaku, R. Kametani, M. Shibuya, and R. Wang NO donor-activated PKC-delta plays a pivotal role in ischemic myocardial protection through accelerated opening of mitochondrial K-ATP channels J. Cardiovasc. Pharmacol. 44 2004 35 41 (Pubitemid 38857126)
6. Z. Balafanova, R. Bolli, J. Zhang, Y. Zheng, J.M. Pass, and A. Bhatnagar Nitric oxide (NO) induces nitration of protein kinase Cepsilon (PKCepsilon), facilitating PKCepsilon translocation via enhanced PKCepsilon-RACK2 interactions: a novel mechanism of NO-triggered activation of PKCepsilon J. Biol. Chem. 277 2002 15021 15027 (Pubitemid 34952578)
7. M.B. West, G. Rokosh, D. Obal, M. Velayutham, Y.T. Xuan, and B.G. Hill Cardiac myocyte-specific expression of inducible nitric oxide synthase protects against ischemia/reperfusion injury by preventing mitochondrial permeability transition Circulation 118 2008 1970 1978
8. D. Rodriguez, C.J. Morrison, and C.M. Overall Matrix metalloproteinases: what do they not do? New substrates and biological roles identified by murine models and proteomics Biochim. Biophys. Acta 1803 2010 39 54
9. F.J. Villarreal, M. Griffin, J. Omens, W. Dillmann, J. Nguyen, and J. Covell Early short-term treatment with doxycycline modulates postinfarction left ventricular remodeling Circulation 108 2003 1487 1492 (Pubitemid 37176456)
10. R. Schmidt, A. Bultmann, M. Ungerer, N. Joghetaei, O. Bulbul, and S. Thieme Extracellular matrix metalloproteinase inducer regulates matrix metalloproteinase activity in cardiovascular cells: implications in acute myocardial infarction Circulation 113 2006 834 841
11. D.A. Siwik, G.M. Kuster, J.V. Brahmbhatt, Z. Zaidi, J. Malik, and H. Ooi EMMPRIN mediates beta-adrenergic receptor-stimulated matrix metalloproteinase activity in cardiac myocytes J. Mol. Cell. Cardiol. 44 2008 210 217
12. 2+ uptake during simulated ischemia does not affect permeability transition pore opening upon simulated reperfusion Cardiovasc. Res. 71 2006 715 724 (Pubitemid 44848013)
13. C. Tarin, M. Gomez, E. Calvo, J.A. Lopez, and C. Zaragoza Endothelial nitric oxide deficiency reduces MMP-13-mediated cleavage of ICAM-1 in vascular endothelium: a role in atherosclerosis Arterioscler. Thromb. Vasc. Biol. 29 2009 27 32
14. C. Zaragoza, C.J. Ocampo, M. Saura, A. McMillan, and C.J. Lowenstein Nitric oxide inhibition of coxsackievirus replication in vitro J. Clin. Invest. 100 1997 1760 1767 (Pubitemid 27431333)
15. E. Lopez-Rivera, T.R. Lizarbe, M. Martinez-Moreno, J.M. Lopez-Novoa, A. Rodriguez-Barbero, and J. Rodrigo Matrix metalloproteinase 13 mediates nitric oxide activation of endothelial cell migration Proc. Natl. Acad. Sci. U. S. A. 102 2005 3685 3690 (Pubitemid 40354672)
16. C. Zaragoza, E. Soria, E. Lopez, D. Browning, M. Balbin, and C. Lopez-Otin Activation of the mitogen activated protein kinase extracellular signal-regulated kinase 1 and 2 by the nitric oxide-cGMP-cGMP-dependent protein kinase axis regulates the expression of matrix metalloproteinase 13 in vascular endothelial cells Mol. Pharmacol. 62 2002 927 935
17. R. Nie, S. Xie, B. Du, X. Liu, B. Deng, and J. Wang Extracellular matrix metalloproteinase inducer (EMMPRIN) is increased in human left ventricle after acute myocardial infarction Arch. Med. Res. 40 2009 605 611
18. W. Tang, and M.E. Hemler Caveolin-1 regulates matrix metalloproteinase-1 induction and CD147/EMMPRIN cell surface clustering J. Biol. Chem. 279 2004 11112 11118 (Pubitemid 38401604)
19. M. Agromayor, E. Wloga, B. Naglieri, J. Abrashkin, K. Verma, and L. Yamasaki Visualizing dynamic E2F-mediated repression in vivo Mol. Cell. Biol. 26 2006 4448 4461 (Pubitemid 43877566)
20. S.P. Jones, and R. Bolli The ubiquitous role of nitric oxide in cardioprotection J. Mol. Cell. Cardiol. 40 2006 16 23 (Pubitemid 43012113)
21. M.C. de Waard, R. van Haperen, T. Soullie, D. Tempel, R. de Crom, and D.J. Duncker Beneficial effects of exercise training after myocardial infarction require full eNOS expression J. Mol. Cell. Cardiol. 48 2010 1041 1049
22. Y.T. Xuan, Y. Guo, Y. Zhu, O.L. Wang, G. Rokosh, and R. Bolli Endothelial nitric oxide synthase plays an obligatory role in the late phase of ischemic preconditioning by activating the protein kinase C epsilon p44/42 mitogen-activated protein kinase pSer-signal transducers and activators of transcription 1/3 pathway Circulation 116 2007 535 544 (Pubitemid 47450262)
23. Q. Qin, X.M. Yang, L. Cui, S.D. Critz, M.V. Cohen, and N.C. Browner Exogenous NO triggers preconditioning via a cGMP- and mitoKATP-dependent mechanism Am. J. Physiol. Heart Circ. Physiol. 287 2004 H712 718
24. J. Venugopal, K. Hanashiro, Z.Z. Yang, and Y. Nagamine Identification and modulation of a caveolae-dependent signal pathway that regulates plasminogen activator inhibitor-1 in insulin-resistant adipocytes Proc. Natl. Acad. Sci. U. S. A. 101 2004 17120 17125 (Pubitemid 39627784)
25. I.V. Turko, and F. Murad Protein nitration in cardiovascular diseases Pharmacol. Rev. 54 2002 619 634 (Pubitemid 35351199)
26. T.R. Lizarbe, C. Garcia-Rama, C. Tarin, M. Saura, E. Calvo, and J.A. Lopez Nitric oxide elicits functional MMP-13 protein-tyrosine nitration during wound repair FASEB J. 22 2008 3207 3215
27. Z. Gu, M. Kaul, B. Yan, S.J. Kridel, J. Cui, and A. Strongin S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death Science 297 2002 1186 1190 (Pubitemid 36193354)
28. P.J. Leary, S. Rajasekaran, R.R. Morrison, E.I. Tuomanen, T.K. Chin, and P.A. Hofmann A cardioprotective role for platelet-activating factor through NOS-dependent S-nitrosylation Am. J. Physiol. Heart Circ. Physiol. 294 2008 H2775 2784
29. 2+ channel alpha1 subunit and reduced ischemia/reperfusion injury Circ. Res. 98 2006 403 411
30. J.A. Zavadzkas, R.A. Plyler, S. Bouges, C.N. Koval, W.T. Rivers, and C.U. Beck Cardiac-restricted overexpression of extracellular matrix metalloproteinase inducer causes myocardial remodeling and dysfunction in aging mice Am. J. Physiol. Heart Circ. Physiol. 295 2008 H1394 1402
31. F.G. Spinale Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function Physiol. Rev. 87 2007 1285 1342 (Pubitemid 350041472)
32. B. Ibanez, S. Prat-Gonzalez, W.S. Speidl, G. Vilahur, A. Pinero, and G. Cimmino Early metoprolol administration before coronary reperfusion results in increased myocardial salvage: analysis of ischemic myocardium at risk using cardiac magnetic resonance Circulation 115 2007 2909 2916 (Pubitemid 46915384)
33. D.J. Hausenloy, S.B. Ong, and D.M. Yellon The mitochondrial permeability transition pore as a target for preconditioning and postconditioning Basic Res. Cardiol. 104 2009 189 202
34. C. Piot, P. Croisille, P. Staat, H. Thibault, G. Rioufol, and N. Mewton Effect of cyclosporine on reperfusion injury in acute myocardial infarction N. Engl. J. Med. 359 2008 473 481
35. P. Seizer, T. Schonberger, M. Schott, M.R. Lang, H.F. Langer, and B. Bigalke EMMPRIN and its ligand cyclophilin A regulate MT1-MMP, MMP-9 and M-CSF during foam cell formation Atherosclerosis 209 2010 51 57
36. J. Navarro-Antolin, M. Redondo-Horcajo, C. Zaragoza, A. Alvarez-Barrientos, A.P. Fernandez, and E. Leon-Gomez Role of peroxynitrite in endothelial damage mediated by cyclosporine A Free Radic. Biol. Med. 42 2007 394 403 (Pubitemid 46038047)