Pyruvate prevents cardiac dysfunction and AMP-activated protein kinase activation by hydrogen peroxide in isolated rat hearts

Canadian Journal of Physiology and Pharmacology

Volumn 82, Issue 6, 2004, Pages 409-416

  Leon, Hernando ^a   Atkinson, Laura L ^a   Sawicka, Jolanta ^a   Strynadka, Ken ^a   Lopaschuk, Gary D ^a   Schulz, Richard ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

AMPK; Antioxidant; Isolated rat heart; Oxidative stress; Pyruvate

Indexed keywords

CREATINE; CREATINE PHOSPHATE; DIMETHYL SULFOXIDE; HYDROGEN PEROXIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PHOSPHOTRANSFERASE INHIBITOR; PYRUVIC ACID;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXPERIMENTAL RAT; HEART FUNCTION; HEART MUSCLE ISCHEMIA; ISOLATED HEART; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REDUCTION; REPERFUSION INJURY; STATISTICAL SIGNIFICANCE; UREA CYCLE;

ADENOSINE MONOPHOSPHATE; ANIMALS; ENZYME ACTIVATION; ENZYME INHIBITORS; HYDROGEN PEROXIDE; MALE; MULTIENZYME COMPLEXES; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; PROTEIN-SERINE-THREONINE KINASES; PYRUVIC ACID; RATS; RATS, SPRAGUE-DAWLEY;

EID: 4544347659     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/y04-050     Document Type: Article

References (48)

1. Altarejos, J.Y., Tanaguchi, M., and Lopaschuk, G.D. 2000. 5′ AMP-activated protein kinase kinase (AMPKK) is expressed in the heart and is activated during ischemia. Circulation, 102(Suppl. S): 1694. [Abstr. 503505].
2. Arad, M., Benson, D.W., Perez-Atayde, A.R., McKenna, W.J., Sparks, E.A., Kanter, R.J., McGarry, K., Seidman, J.G., and Seidman, C.E. 2002. Constitutively active AMP kinase mutations cause glycogen storage disease mimicking hypertrophic cardiomyopathy. J. Clin. Invest. 109: 357-362.
3. Azumi, H., Inoue, N., Ohashi, Y., Terashima, M., Mori, T., Fujita, H., Awano, K., Kobayashi, K., Maeda, K., Hata, K., Shinke, T., Kobayashi, S., Hirata, K., Kawashima, S., Itabe, H., Hayashi, Y., Imajoh-Ohmi, S., Itoh, H., and Yokoyama, M. 2002. Superoxide generation in directional coronary atherectomy specimens of patients with angina pectoris: important role of NAD(P)H oxidase. Arterioscler. Thromb. Vasc. Biol. 22: 1838-1844.
4. 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.
5. 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.
6. Blair, E., Redwood, C., Ashrafian, H., Oliveira, M., Broxholme, J., Kerr, B., Salmon, A., Ostman-Smith, I., and Watkins, H. 2001. Mutations in the gamma(2) subunit of AMP-activated protein kinase cause familial hypertrophic cardiomyopathy: evidence for the central role of energy compromise in disease pathogenesis. Hum. Mol. Genet. 10: 1215-1220.
7. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
8. Bunger, R., Mallet, R.T., and Hartman, D.A. 1989. Pyruvate-enhanced phosphorylation potential and inotropism in normoxic and postischemic isolated working heart. Near-complete prevention of reperfusion contractile failure. Eur. J. Biochem. 180: 221-233.
9. 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.
10. 2, Biochem. Biophys. Res. Commun. 287: 92-97.
11. 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.
12. Cuzzocrea, S., Riley, D.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.
13. 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.
14. Dobsak, P., Courderot-Masuyer, C., Zeller, M., Vergely, C., Laubriet, A., Assem, M., Eicher, J. C., Teyssier, J.R., Wolf, J.E., and Rochette, L. 1999. Antioxidative properties of pyruvate and protection of the ischemic rat heart during cardioplegia. J. Cardiovasc. Pharmacol. 34: 651-659.
15. Duan, J., and Moffat, M.P. 1992. Potential cellular mechanisms of hydrogen peroxide-induced cardiac arrhythmias. J. Cardiovasc. Pharmacol. 19: 593-601.
16. Gollob, M.H., Seger, J.J., Gollob, T.N., Tapscott, T., Gonzales, O., Bachinski, L., and Roberts, R. 2001. Novel PRKAG2 mutation responsible for the genetic syndrome of ventricular preexcitation and conduction system disease with childhood onset and absence of cardiac hypertrophy. Circulation, 104: 3030-3033.
17. Hardie, D.G., and Carling, D. 1997. The AMP-activated protein kinase - fuel gauge of the mammalian cell? Eur. J. Biochem. 246: 259-273.
18. Hardie, D.G., and Hawley, S.A. 2001. AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays, 23: 1112-1119.
19. Hasenfuss, G., Maier, L.S., Hermann, H.P., Luers, C., Hunlich, M., Zeitz, O., Janssen, P.M., and Pieske, B. 2002. Influence of pyruvate on contractile performance and Ca(2+) cycling in isolated failing human myocardium. Circulation, 105: 194-199.
20. Hawley, S.A., Davison, M., Woods, A., Davies, S.P., Beri, R.K., Carling, D., and Hardie, D.G. 1996. Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J. Biol. Chem. 271: 27 879-27 887.
21. Hermann, H.P., Zeitz, O., Lehnart, S.E., Keweloh, B., Datz, N., Hasenfuss, G., and Janssen, P.M. 2002. Potentiation of beta-adrenergic inotropic response by pyruvate in failing human myocardium. Cardiovasc. Res. 53: 116-123.
22. Ide, T., Tsutsui, H., Kinugawa, S., Suematsu, N., Hayashidani, S., Ichikawa, K., Utsumi, H., Machida, Y., Egashira, K., and Takeshita, A. 2000. Direct evidence for increased hydroxyl radicals originating from superoxide in the failing myocardium. Circ. Res. 86: 152-157.
23. 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.
24. Kudo, N., Gillespie, J.G., Kung, L., Witters, L.A., Schulz, R., Clanachan, A.S., and Lopaschuk, G.D. 1996. Characterization of 5′ AMP-activated protein kinase activity in the heart and its role in inhibiting acetyl-CoA carboxylase during reperfusion following ischemia. Biochim. Biophys. Acta, 1301: 67-75.
25. 2) causes transient cardiac dysfunction in rat hearts with activation of matrix metalloproteinase-2. Can. J. Cardiol. 18(Suppl. B): 419. [Abstr.]
26. Light, P.E., Wallace, C.H., and Dyck, J.R. 2003. Constitutively active adenosine monophosphate-activated protein kinase regulates voltage-gated sodium channels in ventricular myocytes. Circulation, 107: 1962-1965.
27. 2 on intracellular pH (pHi) in isolated working rat hearts. Can. J. Cardiol. 16(Suppl. F): 346. [Abstr.]
28. Maier, L.S., Braunhalter, J., Horn, W., Weichert, S., and Pieske, B. 2002. The role of SR Ca(2+)-content in blunted inotropic responsiveness of failing human myocardium. J. Mol. Cell. Cardiol. 34: 455-467.
29. Mallet, R.T. 2000. Pyruvate: metabolic protector of cardiac performance. Proc. Soc. Exp. Biol. Med. 223: 136-148.
30. Mallet, R.T., Squires, J.E., Bhatia, S., and Sun, J. 2002. Pyruvate restores contractile function and antioxidant defenses of hydrogen peroxide-challenged myocardium. J. Mol. Cell. Cardiol. 34: 1173-1184.
31. Marsin, A.S., Bertrand, L., Rider, M.H., Deprez, J., Beauloye, C., Vincent, M.F., Van den Berghe, G., Carling, D., and Hue, L. 2000. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol. 10: 1247-1255.
32. 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.
33. Mekhfi, H., Veksler, V., Mateo, P., Maupoil, V., Rochette, L., and Ventura-Clapier, R. 1996. Creatine kinase is the main target of reactive oxygen species in cardiac myofibrils. Circ. Res. 78: 1016-1027.
34. Moore, F., Weekes, J., and Hardie, D.G. 1991. Evidence that AMP triggers phosphorylation as well as direct allosteric activation of rat liver AMP-activated protein kinase. A sensitive mechanism to protect the cell against ATP depletion. Eur. J. Biochem. 199: 691-697.
35. Muoio, D.M., Seefeld, K., Witters, L.A., and Coleman, R.A. 1999. AMP-activated kinase reciprocally regulates triacylglycerol synthesis and fatty acid oxidation in liver and muscle: evidence that sn-glycerol-3-phosphate acyltransferase is a novel target. Biochem. J. 338: 783-791.
36. Orie, N.N., Zidek, W., and Tepel, M. 1999. Reactive oxygen species in essential hypertension and non-insulin-dependent diabetes mellitus. Am. J. Hypertens. 12: 1169-1174.
37. 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.
38. Ponticos, M., Lu, Q.L., Morgan, J.E., Hardie, D.G., Partridge, T.A., and Carling, D. 1998. Dual regulation of the AMP-activated protein kinase provides a novel mechanism for the control of creatine kinase in skeletal muscle. EMBO (Eur. Mol. Biol. Org.) J. 17: 1688-1699.
39. Russell, R.R. III, Bergeron, R., Shulman, G.I., and Young, L.H. 1999. Translocation of myocardial GLUT-4 and increased glucose uptake through activation of AMPK by AICAR. Am. J. Physiol. 277: H643-H649.
40. 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: 25 836-25 845.
41. Tejero-Taldo, M.I., Caffrey, J.L., Sun, J., and Mallet, R.T. 1999. Antioxidant properties of pyruvate mediate its potentiation of beta-adrenergic inotropism in stunned myocardium. J. Mol. Cell. Cardiol. 31: 1863-1872.
42. van Bilsen, M., van der Vusse, G.J., Snoeckx, L.H., Arts, T., Coumans, W.A., Willemsen, P.H., and Reneman, R.S. 1988. Effects of pyruvate on post-ischemic myocardial recovery at various workloads. Pflugers Arch. 413: 167-173.
43. 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.
44. 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.
45. 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.
46. 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.
47. Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., Musi, N., Hirshman, M.F., Goodyear, L.J., and Moller, D.E. 2001. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 108: 1167-1174.
48. Zou, M.H., Hou, X.Y., Shi, C.M., Nagata, D., Walsh, K., and Cohen, R.A. 2002. Modulation by peroxynitrite of Akt- and AMP-activated kinase-dependent Ser1179 phosphorylation of endothelial nitric oxide synthase. J. Biol. Chem. 277: 32 552-32 557.