Inhibition of hepatic mitochondrial aldehyde dehydrogenase by carbon tetrachloride through JNK-mediated phosphorylation

Free Radical Biology and Medicine

Volumn 48, Issue 3, 2010, Pages 391-398

  Moon, Kwan Hoon ^a   Lee, Young Mi ^a,b   Song, Byoung Joon ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b Wonkwang University   (South Korea)

Author keywords

Acute liver damage; CCl4; Free radicals; JNK; Lipid peroxidation; Mitochondrial aldehyde dehydrogenase; Phosphorylation; Rat liver

Indexed keywords

ALDEHYDE DEHYDROGENASE ISOENZYME 2; ALKALINE PHOSPHATASE; CARBON TETRACHLORIDE; SERINE; STRESS ACTIVATED PROTEIN KINASE;

ACIDITY; ALKALINITY; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; INCUBATION TIME; ISOELECTRIC POINT; LIPID PEROXIDATION; LIVER NECROSIS; MALE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; RAT; TWO DIMENSIONAL ELECTROPHORESIS;

ALDEHYDE DEHYDROGENASE; ANIMALS; CARBON TETRACHLORIDE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MITOCHONDRIA, LIVER; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 73449119542     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.11.008     Document Type: Article

References (52)

1. Day C.P., Bashir R., James O.F., Bassendine M.F., Crabb D.W., Thomasson H.R., Li T.K., and Edenberg H.J. Investigation of the role of polymorphisms at the alcohol and aldehyde dehydrogenase loci in genetic predisposition to alcohol-related end-organ damage. Hepatology 14 (1991) 798-801
2. Esterbauer H., Schaur R.J., and Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11 (1991) 81-128
3. Hartley D.P., Ruth J.A., and Petersen D.R. The hepatocellular metabolism of 4-hydroxynonenal by alcohol dehydrogenase, aldehyde dehydrogenase, and glutathione S-transferase. Arch. Biochem. Biophys. 316 (1995) 197-205
4. Sydow K., Daiber A., Oelze M., Chen Z., August M., Wendt M., Ullrich V., Mulsch A., Schulz E., Keaney Jr. J.F., Stamler J.S., and Munzel T. Central role of mitochondrial aldehyde dehydrogenase and reactive oxygen species in nitroglycerin tolerance and cross-tolerance. J. Clin. Invest. 113 (2004) 482-489
5. Chen Z., Foster M.W., Zhang J., Mao L., Rockman H.A., Kawamoto T., Kitagawa K., Nakayama K.I., Hess D.T., and Stamler J.S. An essential role for mitochondrial aldehyde dehydrogenase in nitroglycerin bioactivation. Proc. Natl. Acad. Sci. USA 102 (2005) 12159-12164
6. Hjelle J.J., Grubbs J.H., Beer D.G., and Petersen D.R. Inhibition of rat liver aldehyde dehydrogenase by carbon tetrachloride. J. Pharmacol. Exp. Ther. 219 (1981) 821-826
7. Hjelle J.J., Grubbs J.H., Beer D.G., and Petersen D.R. Time course of the carbon tetrachloride-induced decrease in mitochondrial aldehyde dehydrogenase activity. Toxicol. Appl. Pharmacol. 67 (1983) 159-165
8. Mitchell D.Y., and Petersen D.R. Inhibition of rat liver aldehyde dehydrogenases by acrolein. Drug Metab. Dispos. 16 (1988) 37-42
9. Landin J.S., Cohen S.D., and Khairallah E.A. Identification of a 54-kDa mitochondrial acetaminophen-binding protein as aldehyde dehydrogenase. Toxicol. Appl. Pharmacol. 141 (1996) 299-307
10. Chen J.J., and Yu B.P. Detoxification of reactive aldehydes in mitochondria: effects of age and dietary restriction. Aging (Milano) 8 (1996) 334-340
11. Banfi P., Lanzi C., Falvella F.S., Gariboldi M., Gambetta R.A., and Dragani T.A. The daunorubicin-binding protein of Mr 54,000 is an aldehyde dehydrogenase and is down-regulated in mouse liver tumors and in tumor cell lines. Mol. Pharmacol. 46 (1994) 896-900
12. Watanabe A., Hobara N., Nakatsukasa H., Shiota T., Kobayashi M., and Nagashima H. Impaired acetaldehyde metabolism in partially hepatectomized rats. Res. Exp. Med. 185 (1985) 13-20
13. Yoshida A. Genetic polymorphisms of alcohol metabolizing enzymes related to alcohol sensitivity and alcoholic diseases. Alcohol Alcohol. 29 (1994) 693-696
14. Shen Y.C., Fan J.H., Edenberg H.J., Li T.K., Cui Y.H., Wang Y.F., Tian C.H., Zhou C.F., Zhou R.L., Wang J., Zhao Z.L., and Xia G.Y. Polymorphism of ADH and ALDH genes among four ethnic groups in China and effects upon the risk for alcoholism. Alcohol Clin. Exp. Res. 21 (1997) 1272-1277
15. Yokoyama A., Muramatsu T., Omori T., Yokoyama T., Matsushita S., Higuchi S., Maruyama K., and Ishii H. Alcohol and aldehyde dehydrogenase gene polymorphisms and oropharyngolaryngeal, esophageal and stomach cancers in Japanese alcoholics. Carcinogenesis 22 (2001) 433-439
16. Nomura T., Noma H., Shibahara T., Yokoyama A., Muramatusu T., and Ohmori T. Aldehyde dehydrogenase 2 and glutathione S-transferase M 1 polymorphisms in relation to the risk for oral cancer in Japanese drinkers. Oral Oncol. 36 (2000) 42-46
17. Park K.S., Cho S.Y., Kim H., and Paik Y.K. Proteomic alterations of the variants of human aldehyde dehydrogenase isozymes correlate with hepatocellular carcinoma. Int. J. Cancer 97 (2002) 261-265
18. Kim J., Kim S.H., Lee S.U., Ha G.H., Kang D.G., Ha N.Y., Ahn J.S., Cho H.Y., Kang S.J., Lee Y.J., Hong S.C., Ha W.S., Bae J.M., Lee C.W., and Kim J.W. Proteome analysis of human liver tumor tissue by two-dimensional gel electrophoresis and matrix assisted laser desorption/ionization-mass spectrometry for identification of disease-related proteins. Electrophoresis 23 (2002) 4142-4156
19. Takagi S., Iwai N., Yamauchi R., Kojima S., Yasuno S., Baba T., Terashima M., Tsutsumi Y., Suzuki S., Morii I., Hanai S., Ono K., Baba S., Tomoike H., Kawamura A., Miyazaki S., Nonogi H., and Goto Y. Aldehyde dehydrogenase 2 gene is a risk factor for myocardial infarction in Japanese men. Hypertens. Res. 25 (2002) 677-681
20. Jo S.A., Kim E.K., Park M.H., Han C., Park H.Y., Jang Y., Song B.J., and Jo I. A Glu487Lys polymorphism in the gene for mitochondrial aldehyde dehydrogenase 2 is associated with myocardial infarction in elderly Korean men. Clin. Chim. Acta 382 (2007) 43-47
21. Recknagel R.O., Glende Jr. E.A., Dolak J.A., and Waller R.L. Mechanisms of carbon tetrachloride toxicity. Pharmacol. Ther. 43 (1989) 139-154
22. Muriel P. Nitric oxide protection of rat liver from lipid peroxidation, collagen accumulation, and liver damage induced by carbon tetrachloride. Biochem. Pharmacol. 56 (1998) 773-779
23. Koop D.R. Oxidative and reductive metabolism by cytochrome P450 2E1. FASEB J. 6 (1992) 724-730
24. Iida C., Fujii K., Kishioka T., Nagae R., Onishi Y., Ichi I., and Kojo S. Activation of mitogen activated protein kinase (MAPK) during carbon tetrachloride intoxication in the rat liver. Arch. Toxicol. 81 (2007) 489-493
25. 2-terminal protein kinase-related cell death pathway. Mol. Pharmacol. 60 (2001) 847-856
26. Gunawan B.K., Liu Z.X., Han D., Hanawa N., Gaarde W.A., and Kaplowitz N. c-Jun N-terminal kinase plays a major role in murine acetaminophen hepatotoxicity. Gastroenterology 131 (2006) 165-178
27. Kharbanda S., Saxena S., Yoshida K., Pandey P., Kaneki M., Wang Q., Cheng K., Chen Y.N., Campbell A., Sudha T., Yuan Z.M., Narula J., Weichselbaum R., Nalin C., and Kufe D. Translocation of SAPK/JNK to mitochondria and interaction with Bcl-x(L) in response to DNA damage. J. Biol. Chem. 275 (2000) 322-327
28. Adler V., Schaffer A., Kim J., Dolan L., and Ronai Z. UV irradiation and heat shock mediate JNK activation via alternate pathways. J. Biol. Chem. 270 (1995) 26071-26077
29. 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 (2000) 535-541
30. Bae M.A., and Song B.J. Critical role of c-Jun N-terminal protein kinase activation in troglitazone-induced apoptosis of human HepG2 hepatoma cells. Mol. Pharmacol. 63 (2003) 401-408
31. Kim B.J., Ryu S.W., and Song B.J. JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J. Biol. Chem. 281 (2006) 21256-21265
32. Ozcan U., Cao Q., Yilmaz E., Lee A.H., Iwakoshi N.N., Ozdelen E., Tuncman G., Gorgun C., Glimcher L.H., and Hotamisligil G.S. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306 (2004) 457-461
33. Uehara T., Bennett B., Sakata S.T., Satoh Y., Bilter G.K., Westwick J.K., and Brenner D.A. JNK mediates hepatic ischemia reperfusion injury. J. Hepatol. 42 (2005) 850-859
34. Mendelson K.G., Contois L.R., Tevosian S.G., Davis R.J., and Paulson K.E. Independent regulation of JNK/p38 mitogen-activated protein kinases by metabolic oxidative stress in the liver. Proc. Natl. Acad. Sci. USA 93 (1996) 12908-12913
35. 4, its substrate. Biochem. Biophys. Res. Commun. 179 (1991) 449-454
36. Moon K.H., Hood B.L., Kim B.J., Hardwick J.P., Conrads T.P., Veenstra T.D., and Song B.J. Inactivation of oxidized and S-nitrosylated mitochondrial proteins in alcoholic fatty liver of rats. Hepatology 44 (2006) 1218-1230
37. Moon K.H., Upreti V.V., Yu L.R., Lee I.J., Ye X., Eddington N.D., Veenstra T.D., and Song B.J. Mechanism of 3,4-methylenedioxymethamphetamine (MDMA, ecstasy)-mediated mitochondrial dysfunction in rat liver. Proteomics 8 (2008) 3906-3918
38. Chen Q., Vazquez E.J., Moghaddas S., Hoppel C.L., and Lesnefsky E.J. Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 278 (2003) 36027-36031
39. Moon K.H., Kim B.J., and Song B.J. Inhibition of mitochondrial aldehyde dehydrogenase by nitric oxide-mediated S-nitrosylation. FEBS Lett. 579 (2005) 6115-6120
40. Moon K.H., Hood B.L., Mukhopadhyay P., Rajesh M., Abdelmegeed M.A., Kwon Y.I., Conrads T.P., Veenstra T.D., Song B.J., and Pacher P. Oxidative inactivation of key mitochondrial proteins leads to dysfunction and injury in hepatic ischemia reperfusion. Gastroenterology 135 (2008) 1344-1357
41. Svanas G.W., and Weiner H. Aldehyde dehydrogenase activity as the rate-limiting factor for acetaldehyde metabolism in rat liver. Arch. Biochem. Biophys. 236 (1985) 36-46
42. Luckey S.W., Tjalkens R.B., and Petersen D.R. Mechanism of inhibition of rat liver class 2 ALDH by 4-hydroxynonenal. Adv. Exp. Med. Biol. 463 (1999) 71-77
43. Schroeter H., Boyd C.S., Ahmed R., Spencer J.P., Duncan R.F., Rice-Evans C., and Cadenas E. c-Jun N-terminal kinase (JNK)-mediated modulation of brain mitochondria function: new target proteins for JNK signalling in mitochondrion-dependent apoptosis. Biochem. J. 372 (2003) 359-369
44. Lipsky J.J., Shen M.L., and Naylor S. Overview-in vitro inhibition of aldehyde dehydrogenase by disulfiram and metabolites. Chem. Biol. Interact. 130-132 (2001) 81-91
45. 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 (2006) 102-110
46. Song B.J., Moon K.H., Olsson N.U., and Salem Jr. N. Prevention of alcoholic fatty liver and mitochondrial dysfunction in the rat by long-chain polyunsaturated fatty acids. J. Hepatol. 49 (2008) 262-273
47. 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 (2008) 1493-1495
48. Hanawa N., Shinohara M., Saberi B., Gaarde W.A., Han D., and Kaplowitz N. Role of JNK translocation to mitochondria leading to inhibition of mitochondria bioenergetics in acetaminophen-induced liver injury. J. Biol. Chem. 283 (2008) 13565-13577
49. Bogoyevitch M.A., and Kobe B. Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol. Mol. Biol. Rev. 70 (2006) 1061-1095
50. Larson H.N., Weiner H., and Hurley T.D. Disruption of the coenzyme binding site and dimer interface revealed in the crystal structure of mitochondrial aldehyde dehydrogenase "Asian" variant. J. Biol. Chem. 280 (2005) 30550-30556
51. Rout U.K., and Weiner H. Involvement of serine 74 in the enzyme-coenzyme interaction of rat liver mitochondrial aldehyde dehydrogenase. Biochemistry 33 (1994) 8955-8961
52. Moon, K. H.; Abdelmegeed, M. A.; Song, B. J. Inactivation of cytosolic aldehyde dehydrogenase via S-nitrosylation in ethanol-exposed rat liver. FEBS Lett. 581:3967-3972; 2007.