Hepatitis C and alcohol exacerbate liver injury by suppression of FOXO3

American Journal of Pathology

Volumn 183, Issue 6, 2013, Pages 1803-1814

  Tumurbaatar, Batbayar ^a   Tikhanovich, Irina ^a   Li, Zhuan ^a   Ren, Jinyu ^a   Ralston, Robert ^b   Kuravi, Sudhakiranmayi ^a   Campbell, Roosevelt ^a   Chaturvedi, Gaurav ^a   Huang, Ting Ting ^c,d   Zhao, Jie ^a   Hao, Junfang ^e   O'Neil, Maura ^b   Weinman, Steven A ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^e University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALCOHOL; MANGANESE SUPEROXIDE DISMUTASE; STRUCTURAL PROTEIN; TRANSCRIPTION FACTOR FKHRL1;

ALCOHOL LIVER CIRRHOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DISEASE EXACERBATION; HEPATITIS C; INJURY; LIVER INJURY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEATOSIS;

ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HEPACIVIRUS; HEPATITIS C; HUMANS; LIVER DISEASES, ALCOHOLIC; MICE; MICE, KNOCKOUT; SUPEROXIDE DISMUTASE; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84888291397     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.08.013     Document Type: Article

References (50)

1. Y. Yilmaz, E. Dolar, E. Ulukaya, S. Akgoz, M. Keskin, M. Kiyici, O. Yerci, A.Y. Oral, C.B. Gul, S. Gurel, S.G. Nak, and M. Gulten Elevated serum levels of caspase-cleaved cytokeratin 18 (CK18-Asp396) in patients with nonalcoholic steatohepatitis and chronic hepatitis C Med Sci Monit 15 2009 CR189 CR193
2. G.C. Nguyen, J. Sam, and P.J. Thuluvath Hepatitis C is a predictor of acute liver injury among hospitalizations for acetaminophen overdose in the United States: a nationwide analysis Hepatology 48 2008 1336 1341
3. A.K. Singal, S. Sagi, Y.F. Kuo, and S. Weinman Impact of hepatitis C virus infection on the course and outcome of patients with acute alcoholic hepatitis Eur J Gastroenterol Hepatol 23 2011 204 209
4. S. Seronello, C. Ito, T. Wakita, and J. Choi Ethanol enhances hepatitis C virus replication through lipid metabolism and elevated NADH/NAD+ J Biol Chem 285 2010 845 854
5. G. Szabo, J.R. Wands, A. Eken, N.A. Osna, S.A. Weinman, K. Machida, and H. Joe Wang Alcohol and hepatitis C virus-interactions in immune dysfunctions and liver damage Alcohol Clin Exp Res 34 2010 1675 1686
6. N.A. Osna, R.L. White, V.M. Krutik, T. Wang, S.A. Weinman, and T.M. Donohue Jr. Proteasome activation by hepatitis C core protein is reversed by ethanol-induced oxidative stress Gastroenterology 134 2008 2144 2152
7. K. Otani, M. Korenaga, M.R. Beard, K. Li, T. Qian, L.A. Showalter, A.K. Singh, T. Wang, and S.A. Weinman Hepatitis C virus core protein, cytochrome P450 2E1, and alcohol produce combined mitochondrial injury and cytotoxicity in hepatoma cells Gastroenterology 128 2005 96 107
8. 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
9. J.I. Cohen, S. Roychowdhury, P.M. DiBello, D.W. Jacobsen, and L.E. Nagy Exogenous thioredoxin prevents ethanol-induced oxidative damage and apoptosis in mouse liver Hepatology 49 2009 1709 1717
10. M. Carvajal-Yepes, K. Himmelsbach, S. Schaedler, D. Ploen, J. Krause, L. Ludwig, T. Weiss, K. Klingel, and E. Hildt Hepatitis C virus impairs the induction of cytoprotective Nrf2 target genes by delocalization of small Maf proteins J Biol Chem 286 2011 8941 8951
11. F. Wen, K.E. Brown, B.E. Britigan, and W.N. Schmidt Hepatitis C core protein inhibits induction of heme oxygenase-1 and sensitizes hepatocytes to cytotoxicity Cell Biol Toxicol 24 2008 175 188
12. I. Tikhanovich, J. Cox, and S. Weinman FOXO transcription factors in liver function and disease J Gastroenterol Hepatol 28 Suppl 1 2013 125 131
13. D.R. Calnan, and A. Brunet The FoxO code Oncogene 27 2008 2276 2288
14. B.M. Burgering A brief introduction to FOXOlogy Oncogene 27 2008 2258 2262
15. A. van der Horst, and B.M. Burgering Stressing the role of FoxO proteins in lifespan and disease Nat Rev Mol Cell Biol 8 2007 440 450
16. H. Huang, and D.J. Tindall Dynamic FoxO transcription factors J Cell Sci 120 2007 2479 2487
17. L. Miao, and D.K. St Clair Regulation of superoxide dismutase genes: implications in disease Free Radic Biol Med 47 2009 344 356
18. Y. Zhao, Y. Wang, and W.G. Zhu Applications of post-translational modifications of FoxO family proteins in biological functions J Mol Cell Biol 3 2011 276 282
19. S.M. Hedrick The cunning little vixen: foxo and the cycle of life and death Nat Immunol 10 2009 1057 1063
20. L. Deng, I. Shoji, W. Ogawa, S. Kaneda, T. Soga, D.P. Jiang, Y.H. Ide, and H. Hotta Hepatitis C virus infection promotes hepatic gluconeogenesis through an NS5A-mediated FoxO1-dependent pathway J Virol 85 2011 8556 8568
21. M. Honda, K. Takehana, A. Sakai, Y. Tagata, T. Shirasaki, S. Nishitani, T. Muramatsu, T. Yamashita, Y. Nakamoto, E. Mizukoshi, Y. Sakai, T. Yamashita, M. Nakamura, T. Shimakami, M. Yi, S.M. Lemon, T. Suzuki, T. Wakita, S. Kaneko Hokuriku Liver Study Group Malnutrition impairs interferon signaling through mTOR and FoxO pathways in patients with chronic hepatitis C Gastroenterology 141 2011 128 140 140.e1-2
22. J. Kopycinska, A. Kempinska-Podhorodecka, T. Haas, E. Elias, R.A. Depinho, J. Paik, P. Milkiewicz, and M. Milkiewicz Activation of FoxO3a/Bim axis in patients with primary biliary cirrhosis Liver Int 33 2013 231 238
23. T. Kato, T. Date, A. Murayama, K. Morikawa, D. Akazawa, and T. Wakita Cell culture and infection system for hepatitis C virus Nat Protoc 1 2006 2334 2339
24. A. Brunet, A. Bonni, M.J. Zigmond, M.Z. Lin, P. Juo, L.S. Hu, M.J. Anderson, K.C. Arden, J. Blenis, and M.E. Greenberg Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor Cell 96 1999 857 868
25. K. Miyamoto, K.Y. Araki, K. Naka, F. Arai, K. Takubo, S. Yamazaki, S. Matsuoka, T. Miyamoto, K. Ito, M. Ohmura, C. Chen, K. Hosokawa, H. Nakauchi, K. Nakayama, K.I. Nakayama, M. Harada, N. Motoyama, T. Suda, and A. Hirao Foxo3a is essential for maintenance of the hematopoietic stem cell pool Cell Stem Cell 1 2007 101 112
26. M. Korenaga, T. Wang, Y. Li, L.A. Showalter, T. Chan, J. Sun, and S.A. Weinman Hepatitis C virus core protein inhibits mitochondrial electron transport and increases reactive oxygen species (ROS) production J Biol Chem 280 2005 37481 37488
27. H. Van Remmen, C. Salvador, H. Yang, T.T. Huang, C.J. Epstein, and A. Richardson Characterization of the antioxidant status of the heterozygous manganese superoxide dismutase knockout mouse Arch Biochem Biophys 363 1999 91 97
28. A. Dolganiuc, J. Petrasek, K. Kodys, D. Catalano, P. Mandrekar, A. Velayudham, and G. Szabo MicroRNA expression profile in Lieber-DeCarli diet-induced alcoholic and methionine choline deficient diet-induced nonalcoholic steatohepatitis models in mice Alcohol Clin Exp Res 33 2009 1704 1710
29. M.A. Gyamfi, I. Damjanov, S. French, and Y.J. Wan The pathogenesis of ethanol versus methionine and choline deficient diet-induced liver injury Biochem Pharmacol 75 2008 981 995
30. P. de la M Hall, C.S. Lieber, L.M. DeCarli, S.W. French, K.O. Lindros, H. Jarvelainen, C. Bode, A. Parlesak, and J.C. Bode Models of alcoholic liver disease in rodents: a critical evaluation Alcohol Clin Exp Res 25 Suppl ISBRA 2001 254S 261S
31. K.J. Blight, J.A. McKeating, and C.M. Rice Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication J Virol 76 2002 13001 13014
32. L. Deng, T. Adachi, K. Kitayama, Y. Bungyoku, S. Kitazawa, S. Ishido, I. Shoji, and H. Hotta Hepatitis C virus infection induces apoptosis through a Bax-triggered, mitochondrion-mediated, caspase 3-dependent pathway J Virol 82 2008 10375 10385
33. I. Qadri, M. Iwahashi, J.M. Capasso, M.W. Hopken, S. Flores, J. Schaack, and F.R. Simon Induced oxidative stress and activated expression of manganese superoxide dismutase during hepatitis C virus replication: role of JNK, p38 MAPK and AP-1 Biochem J 378 2004 919 928
34. Y.H. Lee, Q. Lin, U.A. Boelsterli, and M.C. Chung The Sod2 mutant mouse as a model for oxidative stress: a functional proteomics perspective Mass Spectrom Rev 29 2010 179 196
35. L.P. Van Der Heide, M.F. Hoekman, and M.P. Smidt The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation Biochem J 380 2004 297 309
36. R.A. Haeusler, K.H. Kaestner, and D. Accili FoxOs function synergistically to promote glucose production J Biol Chem 285 2010 35245 35248
37. R. Tao, D. Wei, H. Gao, Y. Liu, R.A. DePinho, and X.C. Dong Hepatic FoxOs regulate lipid metabolism via modulation of expression of the nicotinamide phosphoribosyltransferase gene J Biol Chem 286 2011 14681 14690
38. A. Banerjee, K. Meyer, B. Mazumdar, R.B. Ray, and R. Ray Hepatitis C virus differentially modulates activation of forkhead transcription factors and insulin-induced metabolic gene expression J Virol 84 2010 5936 5946
39. L. Valenti, R. Rametta, P. Dongiovanni, M. Maggioni, A.L. Fracanzani, M. Zappa, E. Lattuada, G. Roviaro, and S. Fargion Increased expression and activity of the transcription factor FOXO1 in nonalcoholic steatohepatitis Diabetes 57 2008 1355 1362
40. R.A. Coleman, B.M. Young, L.E. Turner, and R.T. Cook A practical method of chronic ethanol administration in mice Methods Mol Biol 447 2008 49 59
41. C.S. Lieber, and L.M. DeCarli Animal models of chronic ethanol toxicity Methods Enzymol 233 1994 585 594
42. H. Tsukamoto, H. Mkrtchyan, and A. Dynnyk Intragastric ethanol infusion model in rodents Methods Mol Biol 447 2008 33 48
43. 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
44. A.A. Nanji Role of different dietary fatty acids in the pathogenesis of experimental alcoholic liver disease Alcohol 34 2004 21 25
45. X. Liu, J. Yu, L. Jiang, A. Wang, F. Shi, H. Ye, and X. Zhou MicroRNA-222 regulates cell invasion by targeting matrix metalloproteinase 1 (MMP1) and manganese superoxide dismutase 2 (SOD2) in tongue squamous cell carcinoma cell lines Cancer Genomics & Proteomics 6 2009 131 139
46. T. Ogawa, M. Enomoto, H. Fujii, Y. Sekiya, K. Yoshizato, K. Ikeda, and N. Kawada MicroRNA-221/222 upregulation indicates the activation of stellate cells and the progression of liver fibrosis Gut 61 2012 1600 1609
47. I. Tikhanovich, S. Kuravi, R.V. Campbell, K.K. Kharbanda, A. Artigues, M.T. Villar, and S.A. Weinman Regulation of FOXO3 by phosphorylation and methylation in hepatitis C virus infection and alcohol exposure Hepatology 2013 http://dx.doi.org/10.1002/hep.26618
48. K. Yamagata, H. Daitoku, Y. Takahashi, K. Namiki, K. Hisatake, K. Kako, H. Mukai, Y. Kasuya, and A. Fukamizu Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt Mol Cell 32 2008 221 231
49. M. Okuda, K. Li, M.R. Beard, L.A. Showalter, F. Scholle, S.M. Lemon, and S.A. Weinman Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein Gastroenterology 122 2002 366 375
50. C. Piccoli, R. Scrima, G. Quarato, A. D'Aprile, M. Ripoli, L. Lecce, D. Boffoli, D. Moradpour, and N. Capitanio Hepatitis C virus protein expression causes calcium-mediated mitochondrial bioenergetic dysfunction and nitro-oxidative stress Hepatology 46 2007 58 65