Binge alcohol promotes hypoxic liver injury through a CYP2E1-HIF-1α-dependent apoptosis pathway in mice and humans

Free Radical Biology and Medicine

Volumn 77, Issue , 2014, Pages 183-194

  Yun, Jun Won ^a   Son, Min Jeong ^b   Abdelmegeed, Mohamed A ^a   Banerjee, Atrayee ^a   Morgan, Timothy R ^c,d   Yoo, Seong Ho ^b   Song, Byoung Joon ^a  

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

^b Seoul National University College of Medicine   (South Korea)

^c VA LONG BEACH HEALTHCARE SYSTEM   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alcohol metabolizing enzymes; Apoptosis; Binge ethanol; CYP2E1; Free radicals; Human liver injury; Hypoxia; Protein nitration

Indexed keywords

3 NITROTYROSINE; 4 [BIS(2 CHLOROETHYL)OXIDOAMINO]PHENYLALANINE; CYTOCHROME P450 2E1; DNA NUCLEOTIDYLEXOTRANSFERASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; PROTEIN BNIP3; PROTEIN P53; ALCOHOL; HIF1A PROTEIN, HUMAN;

ALCOHOL BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINGE DRINKING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; FEMALE; HUMAN; HUMAN TISSUE; KNOCKOUT MOUSE; LIVER HISTOLOGY; LIVER INJURY; LIVER ISCHEMIA; LIVER TOXICITY; MALE; MOUSE; NICK END LABELING; NITRATION; NONHUMAN; WILD TYPE; 129 MOUSE; ADOLESCENT; ADULT; AGED; ANIMAL; CELL HYPOXIA; ENZYMOLOGY; LIVER; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; TOXIC HEPATITIS; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ANIMALS; APOPTOSIS; BINGE DRINKING; CELL HYPOXIA; CYTOCHROME P-450 CYP2E1; DRUG-INDUCED LIVER INJURY; ETHANOL; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER; MALE; MICE, 129 STRAIN; MIDDLE AGED; YOUNG ADULT;

EID: 84908311556     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.08.030     Document Type: Article

References (55)

1. H. Tsukamoto, and X.P. Xi Incomplete compensation of enhanced hepatic oxygen consumption in rats with alcoholic centrilobular liver necrosis Hepatology 9 1989 302 306
2. E. Brandon-Warner, L.W. Schrum, C.M. Schmidt, and I.H. McKillop Rodent models of alcoholic liver disease: of mice and men Alcohol 46 2012 715 725
3. A. Bertola, S. Mathews, S.H. Ki, H. Wang, and B. Gao Mouse model of chronic and binge ethanol feeding (the NIAAA model) Nat. Protoc. 8 2013 627 637
4. S. Stewart, D. Jones, and C.P. Day Alcoholic liver disease: new insights into mechanisms and preventative strategies Trends Mol. Med. 7 2001 408 413
5. Centers for Disease Control and Prevention Fact sheets: binge drinking Vol. 2011 2010 CDC Atlanta
6. National Institute on Alcohol Abuse and Alcoholism Moderate & binge drinking 2012 NIAAA Rockville, MD
7. P. Mathurin, and M.R. Lucey Management of alcoholic hepatitis J. Hepatol. 56 2012 S39 S45
8. P. Mathurin, and P. Deltenre Effect of binge drinking on the liver: an alarming public health issue? Gut 58 2009 613 617
9. R.B. Hamanaka, and N.S. Chandel Mitochondrial reactive oxygen species regulate hypoxic signaling Curr. Opin. Cell Biol. 21 2009 894 899
10. A.E. Greijer, and E. van der Wall The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis J. Clin. Pathol. 57 2004 1009 1014
11. 2-regulated prolyl hydroxylation Science 292 2001 468 472
12. X. Wang, D. Wu, L. Yang, L. Gan, and A.I. Cederbaum Cytochrome P450 2E1 potentiates ethanol induction of hypoxia and HIF-1α in vivo Free Radic. Biol. Med. 63 2013 175 186
13. T. He, M. Ai, X.H. Zhao, and Y.Q. Xing Inducible nitric oxide synthase mediates hypoxia-induced hypoxia-inducible factor-1 alpha activation and vascular endothelial growth factor expression in oxygen-induced retinopathy Pathobiology 74 2007 336 343
14. M.A. Robinson, J.E. Baumgardner, and C.M. Otto Oxygen-dependent regulation of nitric oxide production by inducible nitric oxide synthase Free Radic. Biol. Med. 51 2011 1952 1965
15. C.S. Lieber Metabolism of alcohol Clin. Liver Dis 9 2005 1 35
16. I. Dupont, P. Bodenez, F. Berthou, B. Simon, L.G. Bardou, and D. Lucas Cytochrome P-450 2E1 activity and oxidative stress in alcoholic patients Alcohol Alcohol. 35 2000 98 103
17. M.A. Abdelmegeed, A. Banerjee, S. Jang, S.H. Yoo, J.W. Yun, F.J. Gonzalez, A. Keshavarzian, and B.J. Song CYP2E1 potentiates binge alcohol-induced gut leakiness, steatohepatitis, and apoptosis Free Radic. Biol. Med. 65 2013 1238 1245
18. G.E. Arteel, J.A. Raleigh, B.U. Bradford, and R.G. Thurman Acute alcohol produces hypoxia directly in rat liver tissue in vivo: role of Kupffer cells Am. J. Physiol. 271 1996 G494 G500
19. P. de la M Hall, C.S. Lieber, L.M. DeCarli, S.W. French, K.O. Lindros, H. Järveläinen, C. Bode, A. Parlesak, and J.C. Bode Models of alcoholic liver disease in rodents: a critical evaluation Alcohol. Clin. Exp. Res. 25 2001 254S 261S
20. K. Sun, N. Halberg, M. Khan, U.J. Magalang, and P.E. Scherer Selective inhibition of hypoxia-inducible factor 1α ameliorates adipose tissue dysfunction Mol. Cell. Biol. 33 2013 904 917
21. M.A. Abdelmegeed, K.H. Moon, J.P. Hardwick, F.J. Gonzalez, and B.J. Song Role of peroxisome proliferator-activated receptor-α in fasting-mediated oxidative stress Free Radic. Biol. Med. 47 2009 767 778
22. B.J. Song, S.K. Suh, and K.H. Moon A simple method to systematically study oxidatively modified proteins in biological samples and its applications Methods Enzymol. 473 2010 251 264
23. L.A. Reinke, and M.J. Moyer p-Nitrophenol hydroxylation: a microsomal oxidation which is highly inducible by ethanol Drug Metab. Dispos. 13 1985 548 552
24. M.A. Abdelmegeed, A. Banerjee, S.H. Yoo, S. Jang, F.J. Gonzalez, and B.J. Song Critical role of cytochrome P450 2E1 (CYP2E1) in the development of high fat-induced non-alcoholic steatohepatitis J. Hepatol. 57 2012 860 866
25. U. Bruning, L. Cerone, Z. Neufeld, S.F. Fitzpatrick, A. Cheong, C.C. Scholz, D.A. Simpson, M.O. Leonard, M.M. Tambuwala, E.P. Cummins, and C.T. Taylor MicroRNA-155 promotes resolution of hypoxia-inducible factor 1 alpha activity during prolonged hypoxia Mol. Cell. Biol. 19 2011 4087 4096
26. C.L. Dalgard, H. Lu, A. Mohyeldin, and A. Verma Endogenous 2-oxoacids differentially regulate expression of oxygen sensors Biochem. J. 380 2004 419 424
27. H. Suzuki, A. Tomida, and T. Tsuruo Dephosphorylated hypoxia-inducible factor 1alpha as a mediator of p53-dependent apoptosis during hypoxia Oncogene 20 2001 5779 5788
28. V. Hampl, D.N. Cornfield, N.J. Cowan, and S.L. Archer Hypoxia potentiates nitric oxide synthesis and transiently increases cytosolic calcium levels in pulmonary artery endothelial cells Eur. Respir. J. 8 1995 515 522
29. X. Zhu, L.M. Heunks, E.M. Versteeg, H.F. van der Heijden, L. Ennen, T.H. van Kuppevelt, J. Vina, and P.N. Dekhuijzen Hypoxia-induced dysfunction of rat diaphragm: role of peroxynitrite Am. J. Physiol. Lung Cell. Mol. Physiol 288 2005 L16 L26
30. H. Ischiropoulos Biological selectivity and functional aspects of protein tyrosine nitration Biochem. Biophys. Res. Commun. 305 2003 776 783
31. N. Abello, H.A. Kerstjens, D.S. Postma, and R. Bischoff Protein tyrosine nitration: selectivity, physicochemical and biological consequences, denitration, and proteomics methods for the identification of tyrosine-nitrated proteins J. Proteome Res. 8 2009 3222 3238
32. S.D. Shukla, S.B. Pruett, G. Szabo, and G.E. Arteel Binge ethanol and liver: new molecular developments Alcohol. Clin. Exp. Res. 37 2013 550 557
33. Y. Lu, J. Zhuge, X. Wang, J. Bai, and A.I. Cederbaum Cytochrome P450 2E1 contributes to ethanol-induced fatty liver in mice Hepatology 47 2008 1483 1494
34. Y. Lu, and A.I. Cederbaum CYP2E1 and oxidative liver injury by alcohol Free Radic. Biol. Med. 44 2008 723 738
35. E. Albano, P. Clot, M. Morimoto, A. Tomasi, M. Ingelman-Sundberg, and S.W. French Role of cytochrome P4502E1-dependent formation of hydroxyethyl free radical in the development of liver damage in rats intragastrically fed with ethanol Hepatology 23 1996 155 163
36. P. Clot, E. Albano, E. Eliasson, M. Tabone, S. Aricò, Y. Israel, C. Moncada, and M. Ingelman-Sundberg Cytochrome P4502E1 hydroxyethyl radical adducts as the major antigen in autoantibody formation among alcoholics Gastroenterology 111 1996 206 216
37. B.J. Roberts, S.E. Shoaf, K.S. Jeong, and B.J. Song Induction of CYP2E1 in liver, kidney, brain and intestine during chronic ethanol administration and withdrawal: evidence that CYP2E1 possesses a rapid phase half-life of 6 hours or less Biochem. Biophys. Res. Commun. 205 1994 1064 1071
38. A.D. Ross, G. Varghese, B. Oporto, F.J. Carmichael, and Y. Israel Effect of propylthiouracil treatment on NADPH-cytochrome P450 reductase levels, oxygen consumption and hydroxyl radical formation in liver microsomes from rats fed ethanol or acetone chronically Biochem. Pharmacol. 49 1995 979 989
39. S.W. French The role of hypoxia in the pathogenesis of alcoholic liver disease Hepatol. Res. 29 2004 69 74
40. A. Pawlicka, E. Bańkowski, L. Chrostek, and M. Szmitkowski An increase of collagen biosynthesis precedes other symptoms of ethanol-induced liver damage in rats Drug Alcohol Depend. 22 1988 113 116
41. S. Yamada, M. Yamada, Y. Murawaki, and C. Hirayama Increase in lipoperoxide and prolyl hydroxylase activity in rat liver following chronic ethanol feeding Biochem. Pharmacol. 40 1990 1015 1019
42. A. Giménez, J. Caballería, A. Parés, S. Alié, R. Deulofeu, H. Andreu, and J. Rodés Influence of dietary zinc on hepatic collagen and prolyl hydroxylase activity in alcoholic rats Hepatology 16 1992 815 819
43. F. Bardag-Gorce, J. Li, B.A. French, and S.W. French The effect of ethanol-induced CYP2E1 on proteasome activity: the role of hydroxynonenal Exp. Mol. Pathol. 78 2004 109 115
44. F. Bardag-Gorce, R. Venkatesh, J. Li, B.A. French, and S.W. French Hyperphosphorylation of rat liver proteasome subunits: the effects of ethanol and okadaic acid are compared Life Sci. 75 2004 585 597
45. B.J. Kim, B.L. Hood, R.A. Aragon, J.P. Hardwick, T.P. Conrads, T.D. Veenstra, and B.J. Song Increased oxidation and degradation of cytosolic proteins in alcohol-exposed mouse liver and hepatoma cells Proteomics 6 2006 1250 1260
46. F. Bardag-Gorce, Q.X. Yuan, J. Li, B.A. French, C. Fang, M. Ingelman-Sundberg, and S.W. French The effect of ethanol-induced cytochrome p4502E1 on the inhibition of proteasome activity by alcohol Biochem. Biophys. Res. Commun. 279 2000 23 29
47. A.J. D'Souza, S.D. Desai, X.L. Rudner, M.N. Kelly, S. Ruan, and J.E. Shellito Suppression of the macrophage proteasome by ethanol impairs MHC class I antigen processing and presentation PLoS One 8 2013 e56890
48. X.Y. Wu, Z.X. Fu, and X.H. Wang Effect of hypoxia-inducible factor 1-α on survivin in colorectal cancer Mol. Med. Rep 3 2010 409 415
49. Z. Dong, J.Z. Wang, F. Yu, and M.A. Venkatachalam Apoptosis-resistance of hypoxic cells: multiple factors involved and a role for IAP-2 Am. J. Pathol. 163 2003 663 671
50. N. Akakura, M. Kobayashi, I. Horiuchi, A. Suzuki, J. Wang, J. Chen, H. Niizeki, K. Kawamura, M. Hosokawa, and M. Asaka Constitutive expression of hypoxia-inducible factor-1alpha renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation Cancer Res. 61 2001 6548 6554
51. S. Roychowddhury, J.C. Chiang, M.R. McMullen, and L.E. Nagy Moderate, chronic ethanol feeding exacerbates carbon-tetrachloride-induced hepatic fibrosis via hepatocyte-specific hypoxia-inducible factor 1α Pharmacol. Res. Perspect 2 2014 e00061
52. B.R. Zelickson, G.A. Benavides, M.S. Johnson, B.K. Chacko, A. Venkatraman, A. Landar, A.M. Betancourt, S.M. Bailey, and V.M. Darley-Usmar Nitric oxide and hypoxia exacerbate alcohol-induced mitochondrial dysfunction in hepatocytes Biochim. Biophys. Acta 1807 2011 1573 1582
53. M.A. Abdelmegeed, S. Jang, A. Banerjee, J.P. Hardwick, and B.J. Song Robust protein nitration contributes to acetaminophen-induced mitochondrial dysfunction and acute liver injury Free Radic. Biol. Med. 60 2013 211 222
54. K.H. Moon, B.L. Hood, B.J. Kim, J.P. Hardwick, T.P. Conrads, T.D. Veenstra, and B.J. Song Inactivation of oxidized and S-nitrosylated mitochondrial proteins in alcoholic fatty liver of rats Hepatology 44 2006 1218 1230
55. T.M. Leung, and N. Nieto CYP2E1 and oxidant stress in alcoholic and non-alcoholic fatty liver disease J. Hepatol. 58 2013 395 398