Hydrogen peroxide causes cardiac dysfunction independent from its effects on matrix metalloproteinase-2 activation

Canadian Journal of Physiology and Pharmacology

Volumn 85, Issue 3-4, 2007, Pages 341-348

  León, Hernando ^a   Bautista López, Norma ^a   Sawicka, Jolanta ^a   Schulz, Richard ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cardiac function; Matrix metalloproteinases; Oxidative stress

Indexed keywords

DOXYCYCLINE; GELATINASE A; HYDROGEN PEROXIDE; N1 [2,2 DIMETHYL 1 [(METHYLAMINO)CARBONYL]PROPYL] N4 HYDROXY 2 (2 METHYLPROPYL)BUTANEDIAMIDE; PYRUVIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; HEART CONTRACTION; HEART DISEASE; HEART PERFUSION; HEART PROTECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; ZYMOGRAPHY;

ANIMALS; ANTIOXIDANTS; CORONARY CIRCULATION; DOXYCYCLINE; HEART; HYDROGEN PEROXIDE; HYDROXAMIC ACIDS; MALE; MATRIX METALLOPROTEINASE 2; PHOSPHATES; PYRUVIC ACID; RATS; RATS, SPRAGUE-DAWLEY;

EID: 34547916157     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/Y07-003     Document Type: Article

References (43)

1. Becker, B.F., Reinholz, N., Ozcelik, T., Leipert, B., and Gerlach, E. 1989. Uric acid as radical scavenger and antioxidant in the heart. Pflugers Arch. 415: 127-135. doi:10.1007/BF00370582. PMID:2556684.
2. 2 exposure. Lab. Invest. 77: 533-539. PMID:9389796.
3. Beresewicz, A., and Horackova, M. 1991. Alterations in electrical and contractile behavior of isolated cardiomyocytes by hydrogen peroxide: possible ionic mechanisms. J. Mol. Cell. Cardiol. 23: 899-918. doi:10.1016/0022-2828(91)90133-7. PMID:1942091.
4. 2) increases the steady-state mRNA levels of collagenase/MMP-1 in human dermal fibroblasts. Free Radic. Biol. Med. 22: 515-524. doi:10.1016/S0891- 5849(96)00404-2. PMID:8981044.
5. Byler, R.M., Sherman, N.A., Wallner, J.S., and Horwitz, L.D. 1994. Hydrogen peroxide cytotoxicity in cultured cardiac myocytes is iron dependent. Am. J. Physiol. 266: H121-H127. PMID:8304492.
6. Cai, H., and Harrison, D.G. 2000. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ. Res. 87: 840-844. PMID:11073878.
7. Canton, M., Neverova, I., Menabo, R., Van Eyk, J., and Di Lisa, F. 2004. Evidence of myofibrillar protein oxidation induced by postischemic reperfusion in isolated rat hearts. Am. J. Physiol. Heart Circ. Physiol. 286: H870-H877. PMID:14766672.
8. Cheung, P.Y., Sawicki, G., Wozniak, M., Wang, W., Radomski, M.W., and Schulz, R. 2000. Matrix metalloproteinase-2 contributes to ischemia-reperfusion injury in the heart. Circulation, 101: 1833-1839. PMID:10769285.
9. Crestanello, J.A., Lingle, D.M., Millili, J., and Whitman, G.J. 1998. Pyruvate improves myocardial tolerance to reperfusion injury by acting as an antioxidant: a chemiluminescence study. Surgery, 124: 92-99. PMID:9663257.
10. Cuzzocrea, S., Riley, O.P., Caputi, A.P., and Salvemini, D. 2001. Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacol. Rev. 53: 135-159. PMID:11171943.
11. DeBoer, L.W., Bekx, P.A., Han, L., and Steinke, L. 1993. Pyruvate enhances recovery of rat hearts after ischemia and reperfusion by preventing free radical generation. Am. J. Physiol. 265: H1571-H1576. PMID:8238569.
12. Desagher, S., Glowinski, J., and Premont, J. 1997. Pyruvate protects neurons against hydrogen peroxide-induced toxicity. J. Neurosci. 17: 9060-9067. PMID:9364052.
13. Dobsak, P., Courderot-Masuyer, C., Zeller, M., Vergely, C., Laubriet, A., Assem, M., et al. 1999. Antioxidative properties of pyruvate and protection of the ischemic rat heart during cardioplegia. J. Cardiovasc. Pharmacol. 34: 651-659. doi: 10.1097/00005344-199911000-00005. PMID:10547080.
14. Duan, J., and Moffat, M.P. 1992. Potential cellular mechanisms of hydrogen peroxide-induced cardiac arrhythmias. J. Cardiovasc. Pharmacol. 19: 593-601. PMID:1380603.
15. Gao, C.Q., Sawicki, G., Suarez-Pinzon, W.L., Csont, T., Wozniak, M., Ferdinandy, P., and Schulz, R. 2003. Matrix metalloproteinase-2 mediates cytokine-induced myocardial contractile dysfunction. Cardiovasc. Res. 57: 426-433. PMID: 12566115.
16. 2 in quiescent isolated rat cardiomyocytes. Basic Res. Cardiol. 96: 623-629. doi:10.1007/s003950170014. PMID: 11770081.
17. 2+ exchange in ventricular myocytes. Am. J. Physiol. 271: H823-H833. PMID:8853314.
18. Hegstad, A.C., Antonsen, O.K., and Ytrehus, K. 1997. Low concentrations of hydrogen peroxide improve post-ischaemic metabolic and functional recovery in isolated perfused rat hearts. J. Mol. Cell. Cardiol. 29: 2779-2787. doi:10.1006/jmcc.l997. 0513. PMID:9344772.
19. 2+ channel alpha 1C subunits but does not mediate their sensitivity to acute hypoxia. Biochem. Biophys. Res. Commun. 318: 135-141. doi:10.1016/j.bbrc.2004.04.011. PMID:15110764.
20. Janero, D.R., Hreniuk, D., and Sharif, H.M. 1994. Hydroperoxide-induced oxidative stress impairs heart muscle cell carbohydrate metabolism. Am. J. Physiol. 266: C179-C188. PMID:8304415.
21. Leon, H., Atkinson, L.L., Sawicka, J., Strynadka, K., Lopaschuk, G.D., and Schulz, R. 2004. Pyruvate prevents cardiac dysfunction and AMP-activated protein kinase activation by hydrogen peroxide in isolated rat hearts. Can. J. Physiol. Pharmacol. 82: 409-416. doi:10.1139/y04-050. PMID:15381965.
22. Maeda, H., Okamoto, T., and Akaike, T. 1998. Human matrix metalloprotease activation by insults of bacterial infection involving proteases and free radicals. Biol. Chem. 379:193-200. PMID:9524071.
23. Mallet, R.T. 2000. Pyruvate: metabolic protector of cardiac performance. Proc. Soc. Exp. Biol. Med. 223: 136-148. doi:10.1046/j. 1525-1373.2000.22319.x. PMID:10654616.
24. McDonough, K.H., Henry, J.J.. and Spitzer, J.J. 1987. Effects of oxygen radicals on substrate oxidation by cardiac myocytes. Biochim. Biophys. Acta, 926: 127-131. PMID:2822138.
25. Murray, C.J., and Lopez, A.D. 1997. Alternative projections of mortality and disability by cause 1990-2020: Global Burden of Disease Study. Lancet, 349: 1498-1504. doi:10.1016/S01406736(96)07492-2. PMID:9167458.
26. Peters, S.L., Pfaffendorf, M., and van Zwieten, P.A. 1997. The influence of oxidative stress on various inotropic responses in isolated rat left atria. Naunyn Schmiedebergs Arch. Pharmacol. 355: 390-397. doi:10.1007/ PL00004959. PMID: 9089671.
27. Purdom, S., and Chen, Q.M. 2005. Epidermal growth factor receptor-dependent and -independent pathways in hydrogen peroxide-induced mitogen-activated protein kinase activation in cardiomyocytes and heart fibroblasts. J. Pharmacol. Exp. Ther. 312: 1179-1186. PMID:15574683.
28. Rajagopalan, S., Meng, X.P., Ramasamy, S., Harrison, D.G., and Galis, Z.S. 1996. Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J. Clin. Invest. 98: 2572-2579. PMID:8958220.
29. Saddik, M., Gamble, J., Witters, L.A., and Lopaschuk, G.D. 1993. Acetyl-CoA carboxylase regulation of fatty acid oxidation in the heart. J. Biol. Chem. 268: 25836-25845. PMID:7902355.
30. Saurin, A.T., Neubert, H., Brennan, J.P., and Eaton, P. 2004. Widespread sulfenic acid formation in tissues in response to hydrogen peroxide. Proc. Natl. Acad. Sci. U.S.A. 101: 17982-17987. doi:10.1073/pnas.0404762101. PMID:15604151.
31. Sawicki, G., Leon, H., Sawicka, J., Sariahmetoglu, M., Schulze, C.J., Scott, P.G., Szczesna-Cordary, D., and Schulz, R. 2005. Degradation of myosin light chain in isolated rat hearts subjected to ischemia-reperfusion injury: a new intracellular target for matrix metalloproteinase-2. Circulation, 112: 544-552. doi:10. 1161/CIRCULATIONAHA.104.531616. PMID:16027249.
32. Schulz, R., Dodge, K.L., Lopaschuk, G.D., and Clanachan, A.S. 1997. Peroxynitrite impairs cardiac contractile function by decreasing cardiac efficiency. Am. J. Physiol. 272: H1212-H1219. PMID:9087595.
33. Schulz, R., Panas, D.L., Catena, R., Moncada, S., Olley, P.M., and Lopaschuk, G.D. 1995. The role of nitric oxide in cardiac depression induced by interleukin-1 β and tumour necrosis factor-α. Br. J. Pharmacol. 114: 27-34. PMID:7536096.
34. Siwik, D.A., Pagano, P.J., and Colucci, W.S. 2001. Oxidative stress regulates collagen synthesis and matrix metalloproteinase activity in cardiac fibroblasts. Am. J. Physiol. Cell Physiol. 280: C53-C60. PMID:11121376.
35. Skjelbakken, T., Valen, G., and Vaage, J. 1996. Perfusing isolated rat hearts with hydrogen peroxide: an experimental model of cardiac dysfunction caused by reactive oxygen species. Scand. J. Clin. Lab. Invest. 56: 431-439. PMID:8869666.
36. Tejero-Taldo, M.I., Caffrey, I.L., Sun, J., and Mallet, R.T. 1999. Antioxidant properties of pyruvate mediate its potentiation of β-adrenergic inotropism in stunned myocardium. J. Mol. Cell. Cardiol. 31: 1863-1872. doi:10.1006/jmcc.1999.1020. PMID: 10525424.
37. Tokube, K., Kiyosue, T., and Arita, M. 1998. Effects of hydroxyl radicals on KATP channels in guinea-pig ventricular myocytes. Pflugers Arch. 437: 155-157. doi:10.1007/s004240050760. PMID:9817800.
38. Wang, P., and Zweier, J.L. 1996. Measurement of nitric oxide and peroxynitrite generation in the postischemic heart. Evidence for peroxynitrite-mediated reperfusion injury. J. Biol. Chem. 271: 29223-29230. PMID:8910581.
39. Wang, W., Sawicki, G., and Schulz, R. 2002a. Peroxynitrite-induced myocardial injury is mediated through matrix metalloproteinase-2. Cardiovasc. Res. 53: 165-174. doi:10. 1016/S0008-6363(01)00445-X. PMID: 11744025.
40. Wang, W., Schulze, C.J., Suarez-Pinzon, W.L., Dyck, J.R., Sawicki, G., and Schulz, R. 2002b. Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation, 106: 1543-1549. doi:10.1161/01. CIR.0000028818.33488.7B. PMID:12234962.
41. Ward, C.A., and Giles, W.R. 1997. Ionic mechanism of the effects of hydrogen peroxide in rat ventricular myocytes. J. Physiol. 500: 631-642. PMID:9161981.
42. Ward, C.A., and Moffat, M.P. 1995. Role of protein kinase C in mediating effects of hydrogen peroxide in guinea-pig ventricular myocytes. J. Mol. Cell. Cardiol. 27: 1089-1097. doi: 10.1016/0022-2828(95)90077-2. PMID:7563105.
43. Yasmin, W., Strynadka, K.D., and Schulz, R. 1997. Generation of peroxynitrite contributes to ischemia-reperfusion injury in isolated rat hearts. Cardiovasc. Res. 33: 422-432. doi:10.1016/80008-6363(96)00254-4. PMID:9074708.