Time-dependent and ethanol-induced cardiac protection from ischemia mediated by mitochondrial translocation of e{open}PKC and activation of aldehyde dehydrogenase 2

Journal of Molecular and Cellular Cardiology

Volumn 46, Issue 2, 2009, Pages 278-284

  Churchill, Eric N ^a   Disatnik, Marie Hélène ^a   Mochly Rosen, Daria ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acute myocardial infarction; ALDH2; Ethanol preconditioning; HNE; In vivo; Ischemia reperfusion; Ischemic preconditioning; Mitochondria; Oxidative stress; PKC; Stress signaling

Indexed keywords

4 HYDROXYNONENAL; ALCOHOL; ALDEHYDE DEHYDROGENASE ISOENZYME 2; CREATINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DETOXIFICATION; ENZYME ACTIVATION; ENZYME RELEASE; HEART INFARCTION; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN TRANSPORT; RAT; REPERFUSION INJURY;

ALDEHYDE DEHYDROGENASE; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; ETHANOL; IMMUNOPRECIPITATION; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MITOCHONDRIA, HEART; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY; OXIDATIVE STRESS; PROTEIN KINASE C-EPSILON;

ANIMALIA; RATTUS;

EID: 58149302706     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2008.09.713     Document Type: Article

References (67)

1. Gaziano J.M., Gaziano T.A., Glynn R.J., Sesso H.D., Ajani U.A., Stampfer M.J., et al. Light-to-moderate alcohol consumption and mortality in the Physicians' Health Study enrollment cohort. J. Am. Coll. Cardiol. 35 1 (2000 Jan) 96-105
2. Renaud S.C., Gueguen R., Schenker J., and d'Houtaud A. Alcohol and mortality in middle-aged men from eastern France. Epidemiology (Camb. Mass.) 9 2 (1998 Mar) 184-188
3. Rimm E.B., Giovannucci E.L., Willett W.C., Colditz G.A., Ascherio A., Rosner B., et al. Prospective study of alcohol consumption and risk of coronary disease in men. Lancet 338 8765 (1991 Aug 24) 464-468
4. Stampfer M.J., Colditz G.A., Willett W.C., Speizer F.E., and Hennekens C.H. A prospective study of moderate alcohol consumption and the risk of coronary disease and stroke in women. N. Engl. J. Med. 319 5 (1988 Aug 4) 267-273
5. Thun M.J., Peto R., Lopez A.D., Monaco J.H., Henley S.J., Heath Jr. C.W., et al. Alcohol consumption and mortality among middle-aged and elderly U.S. adults. N. Engl. J. Med. 337 24 (1997 Dec 11) 1705-1714
6. Mukamal K.J., Maclure M., Muller J.E., Sherwood J.B., and Mittleman M.A. Prior alcohol consumption and mortality following acute myocardial infarction. JAMA 285 15 (2001 Apr 18) 1965-1970
7. Muntwyler J., Hennekens C.H., Buring J.E., and Gaziano J.M. Mortality and light to moderate alcohol consumption after myocardial infarction. Lancet 352 9144 (1998 Dec 12) 1882-1885
8. Chen C.H., Gray M.O., and Mochly-Rosen D. Cardioprotection from ischemia by a brief exposure to physiological levels of ethanol: role of epsilon protein kinase C. Proc. Natl. Acad. Sci. U. S. A. 96 22 (1999 Oct 26) 12784-12789
9. Krenz M., Baines C.P., Heusch G., Downey J.M., and Cohen M.V. Acute alcohol-induced protection against infarction in rabbit hearts: differences from and similarities to ischemic preconditioning. J. Mol. Cell. Cardiol. 33 11 (2001 Nov) 2015-2022
10. Renaud S., and de Lorgeril M. Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet 339 8808 (1992 Jun 20) 1523-1526
11. Rimm E.B., Williams P., Fosher K., Criqui M., and Stampfer M.J. Moderate alcohol intake and lower risk of coronary heart disease: meta-analysis of effects on lipids and haemostatic factors. BMJ (Clin. Res. Ed.) 319 7224 (1999 Dec 11) 1523-1528
12. Guiraud A., de Lorgeril M., Boucher F., Berthonneche C., Rakotovao A., and de Leiris J. Cardioprotective effect of chronic low dose ethanol drinking: insights into the concept of ethanol preconditioning. J. Mol. Cell. Cardiol. 36 4 (2004 Apr) 561-566
13. Miyamae M., Diamond I., Weiner M.W., Camacho S.A., and Figueredo V.M. Regular alcohol consumption mimics cardiac preconditioning by protecting against ischemia-reperfusion injury. Proc. Natl. Acad. Sci. U. S. A. 94 7 (1997 Apr 1) 3235-3239
14. Chen C., and Mochly-Rosen D. Opposing effects of delta and xi PKC in ethanol-induced cardioprotection. J. Mol. Cell. Cardiol. 33 3 (2001 Mar) 581-585
15. Bellows S.D., Hale S.L., and Kloner R.A. Acute ethanol does not protect against ischemic/reperfusion injury in rabbit myocardium. J. Thromb. Thrombolysis 3 3 (1996) 181-184
16. Hale S.L., and Kloner R.A. Ethanol does not exert myocardial preconditioning in an intact rabbit model of ischemia/reperfusion. Heart Dis. (Hagerst. Md.) 3 5 (2001 Sep-Oct) 293-296
17. Itoya M., Morrison J.D., and Downey H.F. Effect of ethanol on myocardial infarct size in a canine model of coronary artery occlusion-reperfusion. Mol. Cell. Biochem. 186 1-2 (1998 Sep) 35-41
18. Krenz M., Baines C.P., Yang X.M., Heusch G., Cohen M.V., and Downey J.M. Acute ethanol exposure fails to elicit preconditioning-like protection in in situ rabbit hearts because of its continued presence during ischemia. J. Am. Coll. Cardiol. 37 2 (2001 Feb) 601-607
19. Krenz M., Cohen M.V., and Downey J.M. The protective and anti-protective effects of ethanol in a myocardial infarct model. Ann. N.Y. Acad. Sci. 957 (2002 May) 103-114
20. Krenz M., Yang X.M., Qin Q., Downey J.M., and Cohen M.V. Dose-response relationships of the protective and antiprotective effects of acute ethanol exposure in isolated rabbit hearts. Heart Dis. (Hagerst. Md.) 4 5 (2002 Sep-Oct) 276-281
21. Niccoli G., Altamura L., Fabretti A., Lanza G.A., Biasucci L.M., Rebuzzi A.G., et al. Ethanol abolishes ischemic preconditioning in humans. J. Am. Coll. Cardiol. 51 3 (2008 Jan 22) 271-275
22. Inagaki K., and Mochly-Rosen D. DeltaPKC-mediated activation of epsilonPKC in ethanol-induced cardiac protection from ischemia. J. Mol. Cell. Cardiol. 39 2 (2005 Aug) 203-211
23. Miyamae M., Rodriguez M.M., Camacho S.A., Diamond I., Mochly-Rosen D., and Figueredo V.M. Activation of epsilon protein kinase C correlates with a cardioprotective effect of regular ethanol consumption. Proc. Natl. Acad. Sci. U. S. A. 95 14 (1998 Jul 7) 8262-8267
24. Zhou H.Z., Karliner J.S., and Gray M.O. Moderate alcohol consumption induces sustained cardiac protection by activating PKC-epsilon and Akt. Am. J. Physiol. 283 1 (2002 Jul) H165-174
25. Costa A.D., Garlid K.D., West I.C., Lincoln T.M., Downey J.M., Cohen M.V., et al. Protein kinase G transmits the cardioprotective signal from cytosol to mitochondria. Circ. Res. 97 4 (2005 Aug 19) 329-336
26. Jaburek M., Costa A.D., Burton J.R., Costa C.L., and Garlid K.D. Mitochondrial PKC epsilon and mitochondrial ATP-sensitive K+ channel copurify and coreconstitute to form a functioning signaling module in proteoliposomes. Circ. Res. 99 8 (2006 Oct 13) 878-883
27. Guo D., Nguyen T., Ogbi M., Tawfik H., Ma G., Yu Q., et al. Protein kinase C-epsilon coimmunoprecipitates with cytochrome oxidase subunit IV and is associated with improved cytochrome-c oxidase activity and cardioprotection. Am. J. Physiol. 293 4 (2007 Oct) H2219-2230
28. Juhaszova M., Zorov D.B., Kim S.H., Pepe S., Fu Q., Fishbein K.W., et al. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J. Clin. Invest. 113 11 (2004 Jun) 1535-1549
29. Chen C.H., Budas G., Churchill E., Disatnik M.H., Hurley T.D., and Mochly-Rosen D. Activation of aldehyde dehydrogenase 2 reduces ischemic damage to the heart. Science 12 (2008 September) 1493-1495
30. Powers S.K., Demirel H.A., Vincent H.K., Coombes J.S., Naito H., Hamilton K.L., et al. Exercise training improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. Am. J. Physiol. 275 5 Pt 2 (1998 Nov) R1468-1477
31. Mukamal K.J., and Mittleman M.A. Acute ethanol exposure fails to elicit preconditioning-like protection in in situ rabbit hearts because of its continued presence during ischemia. J. Am. Coll. Cardiol. 38 4 (2001 Oct) 1271
32. Baines C.P., Zhang J., Wang G.W., Zheng Y.T., Xiu J.X., Cardwell E.M., et al. Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon-MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection. Circ. Res. 90 4 (2002 Mar 8) 390-397
33. Ohnuma Y., Miura T., Miki T., Tanno M., Kuno A., Tsuchida A., et al. Opening of mitochondrial K(ATP) channel occurs downstream of PKC-epsilon activation in the mechanism of preconditioning. Am. J. Physiol. 283 1 (2002 Jul) H440-447
34. Kaneda K., Miyamae M., Sugioka S., Okusa C., Inamura Y., Domae N., et al. Sevoflurane enhances ethanol-induced cardiac preconditioning through modulation of protein kinase C, mitochondrial KATP channels, and nitric oxide synthase, in guinea pig hearts. Anesth. Analg. 106 1 (2008 Jan) 9-16 table of contents
35. Bulteau A.L., Lundberg K.C., Humphries K.M., Sadek H.A., Szweda P.A., Friguet B., et al. Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J. Biol. Chem. 276 32 (2001 Aug 10) 30057-30063
36. Chen J., Henderson G.I., and Freeman G.L. Role of 4-hydroxynonenal in modification of cytochrome c oxidase in ischemia/reperfused rat heart. J. Mol. Cell. Cardiol. 33 11 (2001 Nov) 1919-1927
37. Eaton P., Li J.M., Hearse D.J., and Shattock M.J. Formation of 4-hydroxy-2-nonenal-modified proteins in ischemic rat heart. Am. J. Physiol. 276 3 Pt 2 (1999 Mar) H935-943
38. Kristal B.S., Park B.K., and Yu B.P. 4-Hydroxyhexenal is a potent inducer of the mitochondrial permeability transition. J. Biol. Chem. 271 11 (1996 Mar 15) 6033-6038
39. Lucas D.T., and Szweda L.I. Cardiac reperfusion injury: aging, lipid peroxidation, and mitochondrial dysfunction. Proc. Natl. Acad. Sci. U. S. A. 95 2 (1998 Jan 20) 510-514
40. Blasig I.E., Grune T., Schonheit K., Rohde E., Jakstadt M., Haseloff R.F., et al. 4-Hydroxynonenal, a novel indicator of lipid peroxidation for reperfusion injury of the myocardium. Am. J. Physiol. 269 1 Pt 2 (1995 Jul) H14-22
41. Kwon S.H., Pimentel D.R., Remondino A., Sawyer D.B., and Colucci W.S. H(2)O(2) regulates cardiac myocyte phenotype via concentration-dependent activation of distinct kinase pathways. J. Mol. Cell. Cardiol. 35 6 (2003 Jun) 615-621
42. Parola M., Robino G., Marra F., Pinzani M., Bellomo G., Leonarduzzi G., et al. HNE interacts directly with JNK isoforms in human hepatic stellate cells. J. Clin. Invest. 102 11 (1998 Dec 1) 1942-1950
43. Soh Y., Jeong K.S., Lee I.J., Bae M.A., Kim Y.C., and Song B.J. Selective activation of the c-Jun N-terminal protein kinase pathway during 4-hydroxynonenal-induced apoptosis of PC12 cells. Mol. Pharmacol. 58 3 (2000 Sep) 535-541
44. Miyamae M., Camacho S.A., Zhou H.Z., Diamond I., and Figueredo V.M. Alcohol consumption reduces ischemia-reperfusion injury by species-specific signaling in guinea pigs and rats. Am. J. Physiol. 275 1 Pt 2 (1998 Jul) H50-56
45. Armstrong S.C., Hoover D.B., Delacey M.H., and Ganote C.E. Translocation of PKC, protein phosphatase inhibition and preconditioning of rabbit cardiomyocytes. J. M. Cell. Cardiol. 28 7 (1996 Jul) 1479-1492
46. Kawamura S., Yoshida K., Miura T., Mizukami Y., and Matsuzaki M. Ischemic preconditioning translocates PKC-delta and -epsilon, which mediate functional protection in isolated rat heart. Am. J. Physiol. 275 6 Pt 2 (1998 Dec) H2266-2271
47. Liu H., McPherson B.C., and Yao Z. Preconditioning attenuates apoptosis and necrosis: role of protein kinase C epsilon and -delta isoforms. Am. J. Physiol 281 1 (2001 Jul) H404-410
48. Ytrehus K., Liu Y., and Downey J.M. Preconditioning protects ischemic rabbit heart by protein kinase C activation. Am. J. Physiol. 266 3 Pt 2 (1994 Mar) H1145-1152
49. Saurin A.T., Pennington D.J., Raat N.J., Latchman D.S., Owen M.J., and Marber M.S. Targeted disruption of the protein kinase C epsilon gene abolishes the infarct size reduction that follows ischaemic preconditioning of isolated buffer-perfused mouse hearts. Cardiovasc. Res. 55 3 (2002 Aug 15) 672-680
50. Ehrig T., Bosron W.F., and Li T.K. Alcohol and aldehyde dehydrogenase. Alcohol Alcohol. (Oxford, Oxfordshire). 25 2-3 (1990) 105-116
51. Kabir A.M., Clark J.E., Tanno M., Cao X., Hothersall J.S., Dashnyam S., et al. Cardioprotection initiated by reactive oxygen species is dependent on activation of PKCepsilon. Am. J. Physiol. 291 4 (2006 Oct) H1893-1899
52. Chen Q., Moghaddas S., Hoppel C.L., and Lesnefsky E.J. Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am. J. Physiol., Cell Physiol. 294 2 (2008 Feb) C460-466
53. Gopalakrishna R., and Jaken S. Protein kinase C signaling and oxidative stress. Free radic. Biol. Med. 28 9 (2000 May 1) 1349-1361
54. Ambrosio G., Zweier J.L., Duilio C., Kuppusamy P., Santoro G., Elia P.P., et al. Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J. Biol. Chem. 268 25 (1993 Sep 5) 18532-18541
55. Churchill E.N., Murriel C.L., Chen C.H., Mochly-Rosen D., and Szweda L.I. Reperfusion-induced translocation of deltaPKC to cardiac mitochondria prevents pyruvate dehydrogenase reactivation. Circ. Res. 97 1 (2005 Jul 8) 78-85
56. Murriel C.L., Churchill E., Inagaki K., Szweda L.I., and Mochly-Rosen D. Protein kinase Cdelta activation induces apoptosis in response to cardiac ischemia and reperfusion damage: a mechanism involving BAD and the mitochondria. J. Biol. Chem. 279 46 (2004 Nov 12) 47985-47991
57. Lewandowski E.D., and White L.T. Pyruvate dehydrogenase influences postischemic heart function. Circulation 91 7 (1995 Apr 1) 2071-2079
58. Churchill E.N., and Szweda L.I. Translocation of deltaPKC to mitochondria during cardiac reperfusion enhances superoxide anion production and induces loss in mitochondrial function. Archives of biochemistry and biophysics. Arch. Biochem. Biophys. 439 2 (2005 Jul 15) 194-199
59. Andrukhiv A., Costa A.D., West I.C., and Garlid K.D. Opening mitoKATP increases superoxide generation from complex I of the electron transport chain. Am. J. Physiol. 291 5 (2006 Nov) H2067-2074
60. Baines C.P., Goto M., and Downey J.M. Oxygen radicals released during ischemic preconditioning contribute to cardioprotection in the rabbit myocardium. J. Mol. Cell. Cardiol. 29 1 (1997 Jan) 207-216
61. Halestrap A.P., Clarke S.J., and Javadov S.A. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc. Res. 61 3 (2004 Feb 15) 372-385
62. Hausenloy D., Wynne A., Duchen M., and Yellon D. Transient mitochondrial permeability transition pore opening mediates preconditioning-induced protection. Circulation 109 14 (2004 Apr 13) 1714-1717
63. Baines C.P., Cohen M.V., and Downey J.M. Signal transduction in ischemic preconditioning: the role of kinases and mitochondrial K(ATP) channels. J. Cardiovasc. Electrophysiol. 10 5 (1999 May) 741-754
64. Cohen M.V., Baines C.P., and Downey J.M. Ischemic preconditioning: from adenosine receptor to KATP channel. Ann. Rev. Physiol. 62 (2000) 79-109
65. Awasthi Y.C., Ansari G.A., and Awasthi S. Regulation of 4-hydroxynonenal mediated signaling by glutathione S-transferases. Methods Enzymol. 401 (2005) 379-407
66. Raza H., John A., Brown E.M., Benedict S., and Kambal A. Alterations in mitochondrial respiratory functions, redox metabolism and apoptosis by oxidant 4-hydroxynonenal and antioxidants curcumin and melatonin in PC12 cells. Toxicol. Appl. Pharmacol. 226 2 (2008 Jan 15) 161-168
67. Li S.Y., Li Q., Shen J.J., Dong F., Sigmon V.K., Liu Y., et al. Attenuation of acetaldehyde-induced cell injury by overexpression of aldehyde dehydrogenase-2 (ALDH2) transgene in human cardiac myocytes: role of MAP kinase signaling. J. Mol. Cell. Cardiol. 40 2 (2006 Feb) 283-294