Activation of aldehyde dehydrogenase 2 (ALDH2) confers cardioprotection in protein kinase C epsilon (PKCe{open}) knockout mice

Journal of Molecular and Cellular Cardiology

Volumn 48, Issue 4, 2010, Pages 757-764

  Budas, Grant R ^a   Disatnik, Marie Hélène ^a   Chen, Che Hong ^a   Mochly Rosen, Daria ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aldehyde dehydrogenase 2; Cardiac ischemia; Preconditioning; Protein kinase C; Signaling

Indexed keywords

4 HYDROXYNONENAL; ALCOHOL; ALDA 44; ALDEHYDE; ALDEHYDE DEHYDROGENASE ISOENZYME 2; ENZYME ACTIVATOR; PROTEIN KINASE C EPSILON; UNCLASSIFIED DRUG;

ALCOHOL CONSUMPTION; ANIMAL TISSUE; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVATION; EX VIVO STUDY; HEART INFARCTION SIZE; HEART MUSCLE ISCHEMIA; HEART PROTECTION; ISOLATED HEART; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; WILD TYPE;

ALDEHYDE DEHYDROGENASE; ANIMALS; ENZYME ACTIVATION; ETHANOL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEART; HUMANS; MICE; MICE, KNOCKOUT; MUTATION; MYOCARDIAL ISCHEMIA; PROTEIN KINASE C; PROTEIN KINASE C-EPSILON; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

MUS;

EID: 77649273950     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.10.030     Document Type: Article

References (52)

1. Kloner R.A., and Rezkalla S.H. To drink or not to drink? That is the question. Circulation 116 11 (2007) 1306-1317
2. Renaud S., and de Lorgeril M. Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet 339 8808 (1992) 1523-1526
3. 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) 12784-12789
4. Chen C., and Mochly-Rosen D. Opposing effects of delta and xi PKC in ethanol-induced cardioprotection. J. Mol. Cell. Cardiol. 33 3 (2001) 581-585
5. 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) 2015-2022
6. 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) 601-607
7. Gross E.R., Gare M., Toller W.G., Kersten J.R., Warltier D.C., and Pagel P.S. Ethanol enhances the functional recovery of stunned myocardium independent of K(ATP) channels in dogs. Anesth. Analg. 92 2 (2001) 299-305
8. 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) 103-114
9. Chen C.H., Budas G.R., Churchill E.N., Disatnik M.H., Hurley T.D., and Mochly-Rosen D. Activation of aldehyde dehydrogenase-2 reduces ischemic damage to the heart. Science 321 5895 (2008) 1493-1495
10. Chen Z., Foster M.W., Zhang J., Mao L., Rockman H.A., Kawamoto T., et al. An essential role for mitochondrial aldehyde dehydrogenase in nitroglycerin bioactivation. Proc. Natl. Acad. Sci. U. S. A. 102 34 (2005) 12159-12164
11. Churchill E.N., Disatnik M.H., and Mochly-Rosen D. Time-dependent and ethanol-induced cardiac protection from ischemia mediated by mitochondrial translocation of varepsilonPKC and activation of aldehyde dehydrogenase 2. J. Mol. Cell. Cardiol. 46 2 (2009) 278-284
12. Perlman D.H., Bauer S.M., Ashrafian H., Bryan N.S., Garcia-Saura M.F., Lim C.C., et al. Mechanistic insights into nitrite-induced cardioprotection using an integrated metabolomic/proteomic approach. Circ. Res. 104 6 (2009) 796-804
13. Lagranha C.J., Steenbergen C., and Murphy E. Male-female differences in post translational modifications of mitochondrial proteins. FASEB J. 23 (2009) (1_MeetingAbstracts):508.501-
14. Vasiliou V., Pappa A., and Petersen D.R. Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem. Biol. Interact. 129 1-2 (2000) 1-19
15. Petersen D.R., and Doorn J.A. Reactions of 4-hydroxynonenal with proteins and cellular targets. Free Radic. Biol. Med. 37 7 (2004) 937-945
16. 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) H935-H943
17. 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) H14-H22
18. Uchida K., and Stadtman E.R. Modification of histidine residues in proteins by reaction with 4-hydroxynonenal. Proc. Natl. Acad. Sci. U. S. A. 89 10 (1992) 4544-4548
19. Khasar S.G., Lin Y.H., Martin A., Dadgar J., McMahon T., Wang D., et al. A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice. Neuron 24 1 (1999) 253-260
20. Gray M.O., Zhou H.Z., Schafhalter-Zoppoth I., Zhu P., Mochly-Rosen D., and Messing R.O. Preservation of base-line hemodynamic function and loss of inducible cardioprotection in adult mice lacking protein kinase C epsilon. J. Biol. Chem. 279 5 (2004) 3596-3604
21. Doorn J.A., Hurley T.D., and Petersen D.R. Inhibition of human mitochondrial aldehyde dehydrogenase by 4-hydroxynon-2-enal and 4-oxonon-2-enal. Chem. Res. Toxicol. 19 1 (2006) 102-110
22. Esterbauer H., Schaur R.J., and Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11 1 (1991) 81-128
23. Clerk A., Michael A., and Sugden P.H. Stimulation of multiple mitogen-activated protein kinase sub-families by oxidative stress and phosphorylation of the small heat shock protein, HSP25/27, in neonatal ventricular myocytes. Biochem. J. 333 Pt 3 (1998) 581-589
24. Bogoyevitch M.A., Gillespie-Brown J., Ketterman A.J., Fuller S.J., Ben-Levy R., Ashworth A., et al. Stimulation of the stress-activated mitogen-activated protein kinase subfamilies in perfused heart. p38/RK mitogen-activated protein kinases and c-Jun N-terminal kinases are activated by ischemia/reperfusion. Circ. Res. 79 2 (1996) 162-173
25. He H., Li H.L., Lin A., and Gottlieb R.A. Activation of the JNK pathway is important for cardiomyocyte death in response to simulated ischemia. Cell. Death Differ. 6 10 (1999) 987-991
26. Knight R.J., and Buxton D.B. Stimulation of c-Jun kinase and mitogen-activated protein kinase by ischemia and reperfusion in the perfused rat heart. Biochem. Biophys. Res. Commun. 218 1 (1996) 83-88
27. Yin T., Sandhu G., Wolfgang C.D., Burrier A., Webb R.L., Rigel D.F., et al. Tissue-specific pattern of stress kinase activation in ischemic/reperfused heart and kidney. J. Biol. Chem. 272 32 (1997) 19943-19950
28. Bolli R., Jeroudi M.O., Patel B.S., DuBose C.M., Lai E.K., Roberts R., et al. Direct evidence that oxygen-derived free radicals contribute to postischemic myocardial dysfunction in the intact dog. Proc. Natl. Acad. Sci. U. S. A. 86 12 (1989) 4695-4699
29. Cordis G.A., Maulik N., Bagchi D., Engelman R.M., and Das D.K. Estimation of the extent of lipid peroxidation in the ischemic and reperfused heart by monitoring lipid metabolic products with the aid of high-performance liquid chromatography. J. Chromatogr. 632 1-2 (1993) 97-103
30. Hill B.G., Awe S.O., Vladykovskaya E., Ahmed Y., Liu S.Q., Bhatnagar A., et al. Myocardial ischaemia inhibits mitochondrial metabolism of 4-hydroxy-trans-2-nonenal. Biochem. J. 417 2 (2009) 513-524
31. Uchida K., and Stadtman E.R. Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase. A possible involvement of intra- and intermolecular cross-linking reaction. J. Biol. Chem. 268 9 (1993) 6388-6393
32. Siems W.G., Hapner S.J., and van Kuijk F.J. 4-hydroxynonenal inhibits Na(+)-K(+)-ATPase. Free Radic. Biol. Med. 20 2 (1996) 215-223
33. Farout L., Mary J., Vinh J., Szweda L.I., and Friguet B. Inactivation of the proteasome by 4-hydroxy-2-nonenal is site specific and dependant on 20S proteasome subtypes. Arch. Biochem. Biophys. 453 1 (2006) 135-142
34. 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) 6033-6038
35. Werns S.W., Fantone J.C., Ventura A., and Lucchesi B.R. Myocardial glutathione depletion impairs recovery of isolated blood-perfused hearts after global ischaemia. J. Mol. Cell. Cardiol. 24 11 (1992) 1215-1220
36. 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) 8262-8267
37. 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) 3235-3239
38. Das J., Pany S., Rahman G.M., and Slater S.J. PKC epsilon has an alcohol binding site in its second cysteine rich regulatory domain. Biochem. J. (2009)
39. Hale S.L., and Kloner R.A. Ethanol does not exert myocardial preconditioning in an intact rabbit model of ischemia/reperfusion. Heart Dis. 3 5 (2001) 293-296
40. 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
41. 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) 271-275
42. Hintz K.K., Relling D.P., Saari J.T., Borgerding A.J., Duan J., Ren B.H., et al. Cardiac overexpression of alcohol dehydrogenase exacerbates cardiac contractile dysfunction, lipid peroxidation, and protein damage after chronic ethanol ingestion. Alcohol Clin. Exp. Res. 27 7 (2003) 1090-1098
43. 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) 283-294
44. Doser T.A., Turdi S., Thomas D.P., Epstein P.N., Li S.Y., and Ren J. Transgenic overexpression of aldehyde dehydrogenase-2 rescues chronic alcohol intake-induced myocardial hypertrophy and contractile dysfunction. Circulation 119 14 (2009) 1941-1949
45. 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) 1942-1950
46. Uchida K., Shiraishi M., Naito Y., Torii Y., Nakamura Y., and Osawa T. Activation of stress signaling pathways by the end product of lipid peroxidation. 4-hydroxy-2-nonenal is a potential inducer of intracellular peroxide production. J. Biol. Chem. 274 4 (1999) 2234-2242
47. Camandola S., Poli G., and Mattson M.P. The lipid peroxidation product 4-hydroxy-2,3-nonenal increases AP-1-binding activity through caspase activation in neurons. J. Neurochem. 74 1 (2000) 159-168
48. 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) 535-541
49. Cheng J.Z., Singhal S.S., Sharma A., Saini M., Yang Y., Awasthi S., et al. Transfection of mGSTA4 in HL-60 cells protects against 4-hydroxynonenal-induced apoptosis by inhibiting JNK-mediated signaling. Arch. Biochem. Biophys. 392 2 (2001) 197-207
50. Donovan N., Becker E.B., Konishi Y., and Bonni A. JNK phosphorylation and activation of BAD couples the stress-activated signaling pathway to the cell death machinery. J. Biol. Chem. 277 43 (2002) 40944-40949
51. Yamamoto K., Ichijo H., and Korsmeyer S.J. BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol. 19 12 (1999) 8469-8478
52. Aoki H., Kang P.M., Hampe J., Yoshimura K., Noma T., Matsuzaki M., et al. Direct activation of mitochondrial apoptosis machinery by c-Jun N-terminal kinase in adult cardiac myocytes. J. Biol. Chem. 277 12 (2002) 10244-10250