Deletion of Nrf2 leads to rapid progression of steatohepatitis in mice fed atherogenic plus high-fat diet

Journal of Gastroenterology

Volumn 48, Issue 5, 2013, Pages 620-632

  Okada, Kosuke ^a   Warabi, Eiji ^a   Sugimoto, Hirokazu ^a   Horie, Masaki ^a   Gotoh, Naohiro ^b   Tokushige, Katsutoshi ^c   Hashimoto, Etsuko ^c   Utsunomiya, Hirotoshi ^d   Takahashi, Hiroshi ^a   Ishii, Tetsuro ^a   Yamamoto, Masayuki ^e   Shoda, Junichi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

^c TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^d WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^e TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Atherogenic plus high fat diet; Fatty acid; Nrf2 gene knockout mouse; Oxidative stress; Transcription factor

Indexed keywords

MESSENGER RNA; OLEIC ACID; TRANSCRIPTION FACTOR NRF2; TRIACYLGLYCEROL;

1C GENE; ACC 1 GENE; ALPHA SMA GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENIC DIET; CONTROLLED STUDY; DISEASE COURSE; EXPERIMENTAL MODEL; FAS GENE; FATTY ACID METABOLISM; FATTY ACID TRANSPORTING PEPTIDE 1 GENE; FATTY ACID TRANSPORTING PEPTIDE 3 GENE; FATTY ACID TRANSPORTING PEPTIDE 4 GENE; FATTY LIVER; FIBROGENESIS; GENE; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HISTOPATHOLOGY; IL 1BETA GENE; LIPID COMPOSITION; LIPID DIET; LIVER CIRRHOSIS; LXR GENE; MALE; MOUSE; NONHUMAN; NRF2 GENE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SCD 1 GENE; SREBP 1A GENE; TNF ALPHA GENE; TNF BETA1 GENE;

ANIMALS; DIET, ATHEROGENIC; DIET, HIGH-FAT; DISEASE PROGRESSION; FATTY LIVER; GENE DELETION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; TIME FACTORS;

EID: 84878111720     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-012-0659-z     Document Type: Article

References (37)

1. Vuppalanchi R, Naga C. Nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: selected practical issues in their evaluation and management. Hepatology. 2009;49:306-17.
2. Torres DM, Harrison SA. Diagnosis and therapy of nonalcoholic steatohepatitis. Gastroenterology. 2008;134:1682-98.
3. Marchesini G, Bugianesi E, Forlani G, Cerrelli F, Lenzi M, Manini R, et al. Nonalcoholic fatty liver, steatohepatitis, and metabolic syndrome. Hepatology. 2003;37:917-23.
4. Browning JD, Horton JD. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest. 2004;114:147-52.
5. Malaguarnera L, Madeddu R, Palio E, Arena N, Malaguarnera M. Heme oxygenase-1 levels and oxidative stress-related parameters in non-alcoholic fatty liver disease patients. J Hepatol. 2005;42:585-91.
6. Sumida Y, Nakashima T, Yoh T, Furutani M, Hirohama A, Kakisaka Y, et al. Serum thioredoxin levels as a predictor of steatohepatitis in patients with nonalcoholic fatty liver disease. J Hepatol. 2003;38:32-8.
7. Kotronen A, Seppala-Lindroos A, Bergholm R, Yki-Jarvinen H. Tissue specificity of insulin resistance in humans: fat in the liver rather than muscle is associated with features of the metabolic syndrome. Diabetologia. 2008;51:130-8.
8. Fromenty B, Robin MA, Igoudili A, Mansouri A, Pessayre D. The ins and outs of mitochondrial dysfunction in NASH. Diabetes Metab 2004;30:121-38.
9. Yang S, Zhu H, Li Y, Lin H, Gabrielson K, Trush MA, et al. Mitochondrial adaptations to obesity related oxidant stress. Arch Biochem Biophys. 2000;378:259-68.
10. Feldstein AE, Werneburg NW, Canbay A, Guicciardi ME, Bronk SF, Rydzewski R, et al. Free fatty acids promote hepatic lipotoxicity by stimulating TNF-α expression via a lysosomal pathway. Hepatology. 2004;40:185-94.
11. Allard JP, Aghdassi E, Mohammed S, Raman M, Avand G, Arendt BM, et al. Nutritional assessment and hepatic fatty acid composition in non-alcoholic fatty liver disease (NAFLD): a cross-sectional study. J Hepatol. 2008;48:300-7.
12. Zhang DD, Hannink M. Distinct cysteine in Keap1 are required for Keap1-dependent ubiquitination on Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol. 2003;23:8137-51.
13. Kwak MK, Itoh K, Yamamoto M, Sutter TR, Kensler TW. Role of transcription factor Nrf2 in the induction of hepatic phase 2 and antioxidative enzymes in vivo by the cancer chemoprotective agent, 3H-1, 2-dithiole-3-thione. Mol Med. 2001;7:135-45.
14. Okada K, Shoda J, Taguchi K, Maher JM, Ishizaki K, Inoue Y, et al. Ursodeoxycholic acid stimulates Nrf2-mediated hepatocellular transport, detoxification, and antioxidative stress systems in mice. Am J Physiol Gastrointest Liver Pysiol. 2008;295:G735-47.
15. Okada K, Shoda J, Taguchi K, Maher JM, Ishizaki K, Inoue Y, et al. Nrf2 counteracts cholestatic liver injury via stimulation of hepatic defense systems. Biochem Biophys Res Commun. 2009;389:431-6.
16. Tanaka Y, Aleksunes LM, Yeager RL, Gyamfi MA, Esterly N, Guo GL, et al. NF-E2-related factor 2 inhibits lipid accumulation and oxidative stress in mice fed high-fat diet. J Pharmacol Exp Ther. 2008;325:655-64.
17. Shin S, Wakabayashi J, Yates MS, Wakabayashi N, Dolan PM, Aja S, et al. Role of Nrf2 in prevention of high-fat diet-induced obesity by synthetic triterpenoid CDDO-Imidazolide. Eur J Pharmacol. 2009;620:138-44.
18. Kitteringham N, Abdullah A, Walsh J, Randle L, Jenkins RE, Sison R, et al. Proteomic analysis of Nrf2 deficient transgenic mice reveals cellular defense and lipid metabolism as primary Nrf2-dependent pathways in the liver. J Proteomics. 2010;73:1612-31.
19. Matsuzawa N, Takamura T, Kurita S, Nisu H, Ota T, Ando H, et al. Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology. 2007;46:1392-403.
20. Sugimoto H, Okada K, Shoda J, Warabi E, Ishige K, Ueda T, et al. Deletion of nuclear factor-E2-related factor-2 leads to rapid onset and progression of nutritional steatohepatitis in mice. Am J Physiol Gastrointest Liver Physiol. 2010;298:G283-94.
21. Gotoh N, Nagao K, Onoda S, Shirouchi B, Furuya K, Nagai T, et al. Effects of three different highly purified n-3 series highly unsaturated fatty acids on lipid metabolism in C57BL/KsJ-db/db mice. J Agric Food Chem. 2009;57:11047-54.
22. Matsuzaka T, Shimano H, Yahagi N, Kato T, Atsumi A, Yamamoto T, et al. Crucial role of a long-chain fatty acid elongase, Elovl6, in obesity-induced insulin resistance. Nat Med. 2007;13:1193-202.
23. Matsuzaka T, Shimano H. Elovl6: a new player in fatty acid metabolism and insulin sensitivity. J Mol Med. 2009;87:379-84.
24. Maruyama A, Tsukamoto S, Nishikawa K, Yoshida A, Harada N, Motojima K, et al. Nrf2 regulates the alternative first exons of CD36 in macrophages through specific antioxidant response elements. Arch Biochem Biophys. 2008;477:139-45.
25. Schwenk RW, Holloway GP, Luiken JJFP, Bonen A, Glatz JFC. Fatty acid transport across the cell membrane: regulation by fatty acid transporters. Prostaglandins Leukot Essent Fatty Acids. 2010;82:149-54.
26. Tomita K, Oike Y, Teratani T, Taguchi T, Noguchi M, Suzuki T, et al. Hepatic adipoR2 signaling plays a protective role against progression of nonalcoholic steatohepatitis in mice. Hepatology. 2008;48:458-73.
27. Adams LA, Lymp JF, Sauver JS, Sanderson SO, Lindor KD, Feldstein A, et al. The natural history of nonalcoholic fatty liver disease: a population based cohort study. Gastroenterology. 2005;129:113-21.
28. Puri P, Wiest MM, Cheung O, Mirshahi F, Sargeant C, Min HK, et al. The plasma lipidomic signature of nonalcoholic steatohepatitis. Hepatology. 2009;50:1827-38.
29. Araya J, Rodrigo R, Vidla LA, Thielemann L, Orellana M, Pettinelli P, et al. Increase in long-chain polyunsaturated fatty acid n-6/n-3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease. Clin Sci. 2004;106:635-43.
30. Moriya K, Todoroki T, Tsutsumi T, Fujie H, Shintani Y, Miyoshi H, et al. Increase in the concentration of carbon 18 monounsaturated fatty acids in the liver with hepatitis C: analysis in transgenic mice and humans. Biochem Biophys Res Commun. 2001;281:1207-12.
31. Feldstein A, Canbay A, Guicciardi ME, Higuchi H, Bronk SF, Gores GJ. Diet associated hepatic steatosis sensitizes to Fas mediated liver injury in mice. J Hepatol. 2003;39:978-83.
32. Mao J, DeMayo FJ, Li H, Abu-Elheiga L, Gu Z, Shaikenov TE, et al. Liver-specific deletion of acetyl-CoA carboxylase 1 reduces hepatic triglyceride accumulation without affecting glucose homeostasis. Proc Natl Acad Sci USA. 2006;103:8552-7.
33. Ntambi JM, Miyazaki M, Stoehr JP, Lan H, Kendziorski CM, Yandell BS, et al. Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc Natl Acad Sci USA. 2002;99:11482-6.
34. Miyazaki M, Flowers MT, Sampath H, Chu K, Otzelberger C, Liu X, et al. Hepatic stearoyl-CoA desaturase-1 deficiency protects mice from carbohydrate-induced adiposity and hepatic steatosis. Cell Metab. 2007;6:484-96.
35. Miquilena-Colina ME, Lima-Cabello E, Sanchez-Campos S, Garcia-Mediavilla MV, Fernandez-Beremejo M, Lazano-Rodriguez T, et al. Hepatic fatty acid translocase CD36 upregulation is associated with insulin resistance, hyperinsulinaemia and increased steatosis in non-alcoholic steatohepatitis and chronic hepatitis C. Gut. 2011;60:1394-402.
36. Pi J, Leung L, Xue P, Wang W, Hou Y, Liu D, et al. Deficiency in the nuclear factor E2-related factor-2 transcription factor results in impaired adipogenesis and protects against diet-induced obesity. J Biol Chem. 2010;285:9292-300.
37. Chartoumpekis DV, Ziros PG, Psyrogiannis AI, Papavassilou AG, Kyriazopoulou VE, Sykiotis GP, et al. Nrf2 represses FGF21 during long-term high-fat diet-induced obesity in mice. Diabetes. 2011;60:2465-73.