Sulforaphane induces Nrf2 and protects against CYP2E1-dependent binge alcohol-induced liver steatosis

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 1, 2014, Pages 209-218

  Zhou, Richard ^a   Lin, Jianjun ^b   Wu, Defeng ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Second People's Hospital of Fujian Traditional Chinese Medicine   (China)

Author keywords

Binge alcohol; CYP2E1:cytochrome p4502E1; Liver steatosis; Nrf2; Sulforaphane

Indexed keywords

3 NITROTYROSINE; ALANINE AMINOTRANSFERASE; ALCOHOL; ASPARTATE AMINOTRANSFERASE; CHOLESTEROL; CYTOCHROME P450 2E1; GLUTATHIONE; HEME OXYGENASE 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PROTEIN P62; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; SULFORAPHANE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRANSCRIPTION FACTOR NRF2; TRIACYLGLYCEROL;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALCOHOL INTOXICATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; AUTOPHAGY; BINGE ALCOHOL INDUCED LIVER STEATOSIS; CATALYSIS; CENTRAL VEIN; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DOSAGE SCHEDULE COMPARISON; DRUG ACTIVITY; DRUG DOSE COMPARISON; ENZYME ACTIVITY; FATTY ACID OXIDATION; FATTY ACID SYNTHESIS; FATTY LIVER; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIPID PEROXIDATION; LIPID STORAGE; LIPOGENESIS; LIPOLYSIS; LIVER MICROSOME; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN TARGETING; TRANSCRIPTION INITIATION; TRIACYLGLYCEROL BLOOD LEVEL;

MUS;

BINGE ALCOHOL; CYP2E1:CYTOCHROME P4502E1; LIVER STEATOSIS; NRF2; SULFORAPHANE;

ANIMALS; ANTI-INFECTIVE AGENTS, LOCAL; ANTICARCINOGENIC AGENTS; AUTOPHAGY; BLOTTING, WESTERN; CYTOCHROME P-450 CYP2E1; ETHANOL; FATTY LIVER; GLUTATHIONE; HEME OXYGENASE-1; HEP G2 CELLS; HUMANS; ISOTHIOCYANATES; LIPID PEROXIDATION; LIVER; MALE; MICE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; TYROSINE;

EID: 84885344699     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.09.018     Document Type: Article

References (65)

1. R. Nordman, C. Riviere, and H. Rouach Implication of free radical mechanisms in ethanol-induced cellular injury Free Radic. Biol. Med. 12 1992 219 240
2. S.C. Bondy Ethanol toxicity and oxidative stress Toxicol. Lett. 63 1992 231 242
3. A.I. Cederbaum Introduction serial review: alcohol, oxidative stress and cell injury Free Radic. Biol. Med. 31 2001 1524 1526 (Pubitemid 34024973)
4. G.E. Arteel Oxidants and antioxidants in alcohol-induced liver disease Gastroenterology 124 2003 778 790 (Pubitemid 36268494)
5. S.Q. Yang, H.Z. Lin, M.D. Lane, M. Clemens, and A.M. Diehl Obesity increases sensitivity to endotoxin liver injury: implications for the pathogenesis of steatohepatitis Proc. Natl. Acad. Sci. U. S. A. 94 1997 2557 2562 (Pubitemid 27136914)
6. S. Yang, H. Lin, and A.M. Diehl Fatty liver vulnerability to endotoxin-induced damage despite NF-kappaB induction and inhibited caspase 3 activation Am. J. Physiol. Gastrointest. Liver Physiol. 281 2001 G382 G392
7. A. Koteish, S. Yang, H. Lin, X. Huang, and A.M. Diehl Chronic ethanol exposure potentiates lipopolysaccharide liver injury despite inhibiting Jun N-terminal kinase and caspase 3 activation J. Biol. Chem. 277 2002 13037 13044 (Pubitemid 34952672)
8. V. Purohit, B. Gao, and B.J. Song Molecular mechanisms of alcoholic fatty liver Alcohol. Clin. Exp. Res. 33 2009 191 205
9. M. You, and D.W. Crabb Recent advances in alcoholic liver disease II. Minireview: molecular mechanisms of alcoholic fatty liver Am. J. Physiol. GI Liver Physiol. 287 2004 G1 G6
10. M. You, and D.W. Crabb Molecular mechanisms of alcoholic fatty liver: role of sterol regulatory element-binding proteins Alcohol 34 2004 39 43
11. D.W. Crabb, and S. Liangpunsaku Alcohol and lipid metabolism J. Gastroenterol. Hepatol. 21 2006 S56 S60
12. M. Sozio, and D.W. Crabb Alcohol and lipid metabolism Am. J. Physiol. Endocrinol. Metab. 295 2008 E10 E16
13. N.R. DiLuzio Prevention of the acute ethanol-induced fatty liver by the simultaneous administration of antioxidants Life Sci. 3 1964 113 118
14. M.D. Wheeler, M. Nakagami, B.U. Bradford, T. Uesugi, R.P. Mason, H.D. Connor, A. Dikalova, M. Kadiiska, and R.G. Thurman Overexpression of manganese superoxide dismutase prevents alcohol-induced liver injury in the rat J. Biol. Chem. 276 2001 36664 36672
15. A.A. Caro, and A.I. Cederbaum Oxidative stress, toxicology and pharmacology of Cyp2E1 Annu. Rev. Pharmacol. Toxicol. 44 2004 27 42 (Pubitemid 38263832)
16. F.J. Gonzalez Role of cytochromes P450 in chemical toxicity and oxidative stress: studies with CYP2E1 Mutat. Res. 569 2005 101 110 (Pubitemid 39643260)
17. A. Butura, K. Nilsson, K. Morgan, T.R. Morgan, S. French, I. Johanssson, I. Schuppe-Koistinen, and M. Ingelman-Sundberg The impact of CYP2E1 on the development of alcoholic liver disease as studied in a transgenic mouse model J. Hepatol. 50 2008 572 583
18. M. Morimoto, A.L. Hagbjork, Y.J. Wan, P.C. Fu, P. Clot, E. Albano, M. Ingelman-Sundberg, and S.W. French Modulation of experimental alcohol-induced liver disease by cytochrome P450 2E1 inhibitors Hepatology 21 1995 1610 1617
19. Z. Gouillon, D. Lucas, J. Li, A.L. Hagbjork, B.A. French, P. Fu, C. Fang, M. Ingelman-Sundberg, T.M. Donohue Jr., and S.W. French Inhibition of ethanol-induced liver disease in the intragastric feeding rat model by chlomethiazole Proc. Soc. Exp. Biol. Med. 224 2000 302 308 (Pubitemid 30643509)
20. Y. Lu, J. Zhuge, X. Wang, J. Bai, and A.I. Cederbaum Cytochrome P4502E1 contributes to ethanol-induced fatty liver in mice Hepatology 47 2008 1483 1494 (Pubitemid 351702732)
21. Y. Lu, D. Wu, X. Wang, S.C. Ward, and A.I. Cederbaum Chronic alcohol-induced liver injury and oxidant stress are decreased in cytochrome P4502E1 knockout mice and restored in cytochrome P4502E1 knockin mice Free Radic. Biol. Med. 49 2010 1406 1416
22. T. Nguyen, P.J. Sherratt, and C.B. Pickett Regulatory mechanisms controlling gene expression mediated by the antioxidant response element Annu. Rev. Pharmacol. Toxicol. 43 2003 233 260 (Pubitemid 37372641)
23. T. Nguyen, C.S. Yang, and C.B. Pickett The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress Free Radic. Biol. Med. 37 2004 433 441 (Pubitemid 38901076)
24. H. Motohashi, and M. Yamamoto Nrf2-Keap1 defines a physiologically important stress response mechanism Trends Mol. Med. 10 2004 549 557 (Pubitemid 39433824)
25. W.O. Osburn, and T.W. Kensler Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults Mutat. Res. 659 2008 31 39
26. T.W. Kensler, P. Egner, P. Dolan, J.D. Groopman, and B.D. Roebuck Mechanisms of protection against aflatoxin tumorigenicity in rats fed oltipraz and related 1,2 dithiol-3-thiones and 1,3 dithiol-3-one Cancer Res. 47 1987 4271 4277 (Pubitemid 17128134)
27. R. Hu, C. Xu, G. Shen, M.R. Jain, T.U. Khor, A. Gopalkrishnan, W. Lin, B. Reddy, Y. Chan, and A.N.T. Kong Gene expression profiles induced by cancer chemopreventive isothiocyanate sulforaphane in the liver of C57BL/6J mice and C57B6/6J/Nrf2(- 1 -) mice Cancer Lett. 243 2006 170 192 (Pubitemid 44485856)
28. 2-cyano-3-12-dioxouleana-1,9 (11)-diem-27-oyl]imidazole Cancer Res. 66 2006 2488 2494
29. R.H. Lai, A.S. Keck, M.A. Walling, L.G. West, and E.H. Jeffery Evaluation of the safety and bioactivity of purified and semi-purified glucoraphanin Food Chem. Toxicol. 46 2008 195 201
30. C.E. Guerrero-Beltran, M. Calderon-Oliver, J. Pedriza-Chaverri, and Y.I. Chirino Protective effect of sulforaphane against oxidative stress: recent advances Exp. Toxicol. Pathol. 64 2010 503 508
31. N. Gan, L. Mi, X. Sun, G. Dai, F.L. Chung, and L. Song Sulforaphane protects microcystin-LR-induced toxicity through activation of the Nrf2-mediated defensive response Toxicol. Appl. Pharmacol. 247 2010 129 137
32. J. Chen, and Z.A. Shaikh Activation of Nrf2 by cadmium and its role in protection against cadmium-induced apoptosis in rat kidney cells Toxicol. Appl. Pharmacol. 241 2009 2009 81 89
33. A.E. Wagner, I. Ernst, R. Iori, C. Desel, and G. Rimbach Sulforaphane but not ascorbigen, indole-3-carbinole and ascorbic acid activates the transcription factor Ntf2 and induces phase-2 and antioxidant enzymes in human keratinocytes in culture Exp. Dermatol. 19 2010 137 144
34. T. Greco, J. Shafer, and G. Fiskum Sulforaphane inhibits mitochondrial permeability transition and oxidative stress Free Radic. Biol. Med. 51 2011 2164 2171
35. D. Wu, and A.I. Cederbaum Development and properties of HepG2 cells that constitutively express CYP2E1 L. Nagy, Alcohol: Methods and Protocols 2008 Humana Press 137 150
36. C. Cheung, A.M. Yu, J.M. Ward, J.W. Krausz, T.E. Akiyama, L. Feigenbaum, and F.J. Gonzalez The CYP2E1-humanized transgenic mouse: role of CYP2E1 in acetaminophen hepatoxicity Drug Metab. Dispos. 33 2005 449 457 (Pubitemid 40279947)
37. C. Cheung, and F.J. Gonzalez Humanized mouse lines and their application for prediction of human drug metabolism and toxicological risk assessment J. Pharmacol. Exp. Ther. 327 2008 288 299
38. P. Gong, and A.I. Cederbaum Nrf2 is increased by CYP2E1 in rodent liver and HepG2 cells and protects against oxidative stress caused by CYP2E1 Hepatology 43 2006 144 153 (Pubitemid 43733601)
39. P. Gong, and A.I. Cederbaum Transcription factor Nrf2 protects HepG2 cells against CYP2E1 plus arachidonic acid-dependent toxicity J. Biol. Chem. 281 2006 14573 14579 (Pubitemid 43855160)
40. 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 (Pubitemid 16221450)
41. T. Zeng, C. Zeng, F. Song, X. Zhao, L. Yu, Z. Zhu, and K. Xie The activation of HO-1/Nrf-2 contributes to the protective effects of diallyl disulfide (DADS) against ethanol-induced oxidative stress Biochim. Biophys. Acta 1830 2013 4848 4859
42. N.E. Saidu, R. Touma, I.A. Asalli, C. Jacob, and M. Montenarh Diallyl tetrasulfane activates both the elF2α and Nrf2/HO-1 pathways Biochim. Biophys. Acta 1830 2013 2214 2225
43. K.C. Wu, J.J. Liu, and C.D. Klaassen Nrf2 activation prevents cadmium-induced acute liver injury Toxicol. Appl. Pharmacol. 263 2012 14 20
44. H. Dong, and M.J. Czaja Regulation of lipid droplets by autophagy Trends Endocrinol. Metab. 22 2011 234 240
45. M. Amir, and M.J. Czaja Autophagy in nonalcoholic steatohepatitis Expert Rev. Gastrorenterol. Hepatol. 52 2011 159 166
46. W.X. Ding, M. Li, X. Chen, H.N. Ni, C.W. Lin, W. Gao, B. Lu, D.B. Stolz, D.L. Clemens, and X.M. Yin Autophagy reduces acute ethanol-induced hepatotoxicity and steatosis in mice Gastroenterology 139 2010 1740 1752
47. W.X. Ding, S. Manley, and H.N. Ni The emerging role of autophagy in alcoholic liver disease Exp. Biol. Med. 236 2011 546 556
48. D. Wu, X. Wang, R. Zhou, L. Yang, and A.I. Cederbaum Alcohol steatosis and cytotoxicity: the role of cytochrome P4502E1 and autophagy Free Radic. Biol. Med. 53 2012 1346 1357
49. B. Levine, and G. Kroemer Autophagy in the pathogenesis of disease Cell 132 2008 27 42
50. J. Lamle, S. Marhenke, J. Borlak, S. Marhenke, J. Borlak, R. von-Wasielewski, C.J. Eriksson, R. Geffers, M.P. Manns, and M. Yamamoto Nuclear factor-erythroid 2-related factor 2 prevents alcohol-induced fulminant liver injury Gastroenterology 134 2008 1159 1168
51. J. Dong, K.K. Sulik, and S. Chen Nrf2-mediated transcriptional induction of antioxidant response in mouse embryos exposed to ethanol in vivo Antioxid. Redox Signal. 10 2008 2023 2033
52. M. Narasimhan, L. Mahimainathan, M.L. Rathinam, A.K. Riar, and G.I. Henderson Overexpression of Nrf2 protects cerebral cortical neurons from ethanol-induced apoptotic death Mol. Pharmacol. 80 2011 988 999
53. P. Yao, A. Nussler, L. Hao Liu, F. Song, H. Schirmeier, and N. Nussler Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways J. Hepatol. 47 2007 253 261 (Pubitemid 47023137)
54. K.C. Wu, J.J. Liu, and C.D. Klaassen Role of Nrf2 in preventing ethanol-induced oxidative stress and lipid accumulation Toxicol. Appl. Pharmacol. 262 2012 321 329
55. Y. Lu, X.H. Zhang, and A.I. Cederbaum Ethanol induction of CYP2A5: role of CYP2E1-ROS-Nrf2 pathway Toxicol. Sci. 128 2012 427 438
56. W.J. Gilmore, G. Hartmann, M. Piquette-Miller, J. Marriott, and G.M. Kirby Effects of lipopolysaccharide-stimulated inflammation and pyrazole-mediated hepatocellular injury on mouse hepatic CYP2A5 expression Toxicology 184 2003 211 226 (Pubitemid 36009302)
57. R. Sharma, A. Sharma, P. Chaudhary, M. Sahu, S. Jaiswal, S. Awashti, and Y.C. Awashti Role of 4-hydroxynonenal in chemopreventive activities of sulforaphane Free Radic. Biol. Med. 52 2012 2177 2185
58. K. Okada, E. Warabi, H. Sugimoto, M. Horie, K. Tokushige, T. Ueda, N. Harada, K. Taguchi, E. Hashimoto, K. Itoh, T. Ishii, H. Utsunomiya, M. Yamamoto, and J. Shoda Ntf2 inhibits iron accumulation and counteracts oxidative stress-induced liver injury in nutritional steatohepatitis J. Gastroenterol. 47 2012 924 935
59. M.A. Abdelmegeed, A. Banerjee, S.H. Yoo, S. Jang, F.J. Gonzalez, and B.J. Song Critical role of cytochrome P4502E1 (CYP2E1) in the development of high fat-induced non-alcoholic steatohepatitis J. Hepatol. 57 2012 860 866
60. H. Zong, M. Armoni, C. Harel, E. Karnieli, and J.E. Pessin Cytochrome P4502E1 CYP2e1 knockout mice are protected against high-fat diet-induced obesity and insulin resistance Am. J. Physiol. Endocrinol. Metab. 302 2012 E532 E539
61. J. Aubert, K. Begriche, L. Knockaert, M.A. Robin, and B. Fromenty Increased expression of cytochrome P450 2E1 in nonalcoholic fatty liver disease: mechanisms and pathophysiological role Clin. Res. Hepatol. Gastroenterol. 35 2011 630 737
62. Y.K.J. Zhang, K.C. Wu, J.J. Liu, and C.D. Klaassen Nrf2 deficiency improves glucose tolerance in mice fed a high fat diet Toxicol. Appl. Pharmacol. 264 2012 305 314
63. S. Barcelo, J.M. Gardiner, A. Gescher, and J.K. Chipman CYP2E1-mediated mechanism of anti-genotoxicity of the broccoli constituent sulforaphane Carcinogenesis 17 1996 277 282 (Pubitemid 26091306)
64. S. Barcelo, K. Mace, A.M.A. Pfeifer, and J.K. Chipman Production of DNA strand breaks by N-nitrosodimethylamine and 2-amino-3-methylimidazol [4,5-f] quinoline in THLE cells expressing human CYP isoenzymes and inhibition by sulforaphane Mutat. Res. 402 1998 111 120 (Pubitemid 28440265)
65. A.M. Bataille, and J.E. Manautou Nrf2: a potential target for new therapeutics in liver disease Clin. Pharmacol. Ther. 92 2012 340 348