Reduced heme oxygenase-1 expression in steatotic livers infected with hepatitis C virus

European Journal of Internal Medicine

Volumn 23, Issue 7, 2012, Pages 649-655

  Abdalla, Maher Y ^a   Mathahs, Meleah M ^b   Ahmad, Iman M ^a  

^a HASHEMITE UNIVERSITY   (Jordan)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

HCV; HO 1; NAFLD; Oxidative stress

Indexed keywords

DICHLOROFLUORESCEIN; HEME OXYGENASE 1; HYDROETHIDINE; OXYGEN; PEROXIDE; REACTIVE OXYGEN METABOLITE;

ARTICLE; CONTROLLED STUDY; FLUORESCENCE; FROZEN SECTION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LIVER; LIVER BIOPSY; LIVER CELL; LIVER VEIN; NONALCOHOLIC FATTY LIVER; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANTIOXIDANTS; BIOPSY; FATTY LIVER; HEME OXYGENASE-1; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; IMMUNOHISTOCHEMISTRY; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84865679791     PISSN: 09536205     EISSN: 18790828     Source Type: Journal    
DOI: 10.1016/j.ejim.2012.05.001     Document Type: Article

References (50)

1. C.E. Ruhl, and J.E. Everhart Epidemiology of nonalcoholic fatty liver Clin Liver Dis 8 2004 501 519
2. I.R. Wanless, and J.S. Lentz Fatty liver hepatitis (steatohepatitis) and obesity: an autopsy study with analysis of risk factors Hepatology 12 1990 1106 1110
3. Jea Ludwig Nonalcoholic steatohepatitis: Mayo Clinic experiences with a hitherto unnamed disease Mayo Clin Proc 55 1980 434 438
4. J. Lewis, and S. Mohanty Nonalcoholic fatty liver disease: a review and update Dig Dis Sci 55 2010 560 578
5. G. Marchesini, and R. Marzocchi Metabolic syndrome and NASH Clin Liver Dis 11 2007 105 117
6. T. Poynard, M.-F. Yuen, V. Ratzin, and C.L. Lai Viral hepatitis C Lancet 362 2003 2095 2100
7. S. Saadeh, G. Cammell, W.D. Carey, Z. Younossi, D. Barnes, and K. Easley The role of liver biopsy in chronic hepatitis C Hepatology 33 2001 196 200
8. A. Lonardo, L.E. Adinolfi, P. Loria, N. Carulli, G. Ruggiero, and C.P. Day Steatosis and hepatitis C virus: mechanisms and significance for hepatic and extrahepatic disease Gastroenterology 126 2004 586 597
9. K. Koike, T. Tsutsumi, H. Yotsuyanagi, and K. Moriya Lipid metabolism and liver disease in hepatitis C viral infection Oncology 78 2010 24 30
10. A. Zekry, J.G. McHutchison, and A.M. Diehl Insulin resistance and steatosis in hepatitis C virus infection Gut 54 2005 903 906
11. L. Stein, M. Dong, and R. Loomba Insulin sensitizers in nonalcoholic fatty liver disease and steatohepatitis: current status Adv Ther 26 2009 893 907
12. A. Federico, M. Trappoliere, and C. Loguercio Treatment of patients with non-alcoholic fatty liver disease: current views and perspectives Dig Liver Dis 38 2006 789 801
13. K. Begriche, A. Igoudjil, D. Pessayre, and B. Fromenty Mitochondrial dysfunction in NASH: causes, consequences and possible means to prevent it Mitochondrion 6 2006 1 28
14. G. Serviddio, J. Sastre, F. Bellanti, J. Viña, G. Vendemiale, and E. Altomare Mitochondrial involvement in non-alcoholic steatohepatitis Mol Aspects Med 29 2008 22 35
15. J. Ludwig, D.B. McGill, and KD L Nonalcoholic steatohepatitis J Gastroenterol Hepatol 12 1997 398 403
16. A.J. Sanyal, C. Campbell-Sargent, F. Mirshahi, W.B. Rizzo, M.J. Contos, and R.K. Sterling Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities Gastroenterology 120 2001 1183 1192
17. H. Lerat, M. Honda, M.R. Beard, K. Loesch, J. Sun, and Y. Yang Steatosis and liver cancer in transgenic mice expressing the structural and nonstructural proteins of hepatitis c virus Gastroenterology 122 2002 352 365
18. G.C. Farrell, and C.Z. Larter Nonalcoholic fatty liver disease: from steatosis to cirrhosis Hepatology 43 2006 S99 S112
19. A. Rubio, E. Guruceaga, M. Vquez-Chantada, J. Sandoval, L.A. Martinez-Cruz, and V. Segura Identification of a gene-pathway associated with non-alcoholic steatohepatitis J Hepatol 46 2007 708 718
20. A.E. Feldstein, N.W. Werneburg, Z. Li, S.F. Bronk, and G.J. Gores Bax inhibition protects against free fatty acid-induced lysosomal permeabilization Am J Physiol Gastrointest Liver Physiol 290 2006 G1339 G1346
21. X. Guo, V.Y. Shin, and C.H. Cho Modulation of heme oxygenase in tissue injury and its implication in protection against gastrointestinal diseases Life Sci 69 2001 3113 3119
22. M.F. Tsan Superoxide dismutase and pulmonary oxygen toxicity Proc Soc Exp Biol Med 203 1993 286 290
23. S. Immenschuh, and G. Ramadori Gene regulation of heme oxygenase-1 as a therapeutic target Biochem Pharmacol 60 2000 1121 1128
24. M.D. Maines Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications FASEB J 2 1988 2557 2568
25. A.M. Choi, and J. Alam Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury Am J Respir Cell Mol Biol 15 1996 9 19
26. M.Y. Abdalla, I.M. Ahmad, D.R. Spitz, W.N. Schmidt, and B.E. Britigan Hepatitis C virus-core and non structural proteins lead to different effects on cellular antioxidant defenses J Med Virol 76 2005 489 497
27. M.Y. Abdalla, B.E. Britigan, F. Wen, M. Icardi, M.L. McCormick, and D.R. LaBrecque Down-regulation of heme oxygenase-1 by hepatitis C virus infection in vivo and by the in vitro expression of hepatitis C core protein J Infect Dis 190 2004 1109 1118
28. U. Protzer, S. Seyfried, M. Quasdorff, G. Sass, M. Svorcova, and D. Webb Antiviral activity and hepatoprotection by heme oxygenase-1 in hepatitis b Virus infection Gastroenterology 133 2007 1156 1165
29. L. Malaguarnera, R. Madeddu, E. Palio, N. Arena, and M. Malaguarnera Heme oxygenase-1 levels and oxidative stress-related parameters in non-alcoholic fatty liver disease patients J Hepatol 42 2005 585 591
30. Z. Zhu, A.T. Wilson, M.M. Mathahs, F. Wen, K.E. Brown, and B.A. Luxon Heme oxygenase-1 suppresses hepatitis C virus replication and increases resistance of hepatocytes to oxidant injury Hepatology 48 2008 1430 1439
31. Y. Shan, J. Zheng, R.W. Lambrecht, and H.L. Bonkovsky Reciprocal effects of micro-RNA-122 on expression of heme oxygenase-1 and hepatitis C virus genes in human hepatocytes Gastroenterology 133 2007 1166 1174
32. C. Lieber Role of oxidative stress and antioxidant therapy in alcoholic and nonalcoholic liver diseases Adv Pharmacol 38 1997 601 628
33. F. Wen, K. Brown, B. Britigan, and W. Schmidt Hepatitis C core protein inhibits induction of heme oxygenase-1 and sensitizes hepatocytes to cytotoxicity Cell Biol Toxicol 24 2008 175 188
34. M. Okuda, K. Li, M.R. Beard, L.A. Showalter, F. Scholle, and S.M. Lemon Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein Gastroenterology 122 2002 366 375
35. F.J. Miller Jr., W.J. Sharp, X. Fang, L.W. Oberley, T.D. Oberley, and N.L. Weintraub Oxidative stress in human abdominal aortic aneurysms: a potential mediator of aneurysmal remodeling Arterioscler Thromb Vasc Biol 22 2002 560 565
36. W.O. Carter, P.K. Narayanan, and J.P. Robinson Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells J Leukoc Biol 55 1994 253 258
37. H. Zhu, G. Bannenberg, P. Moldéus, and H. Shertzer Oxidation pathways for the intracellular probe 2′,7′-dichlorofluorescin Arch Toxicol 68 1994 582 587
38. K.E. Brown, K.A. Broadhurst, M.M. Mathahs, E.M. Brunt, and W.N. Schmidt Expression of HSP47, a collagen-specific chaperone, in normal and diseased human liver Lab Invest 85 2005 789 797
39. M. Koruk, S. Taysi, M.C. Savas, O. Yilmaz, F. Akcay, and M. Karakok Oxidative stress and enzymatic antioxidant status in patients with nonalcoholic steatohepatitis Ann Clin Lab Sci 34 2004 57 62
40. A. Kitase, K. Hino, T. Furutani, M. Okuda, T. Gondo, and I. Hidaka In situ detection of oxidized n-3 polyunsaturated fatty acids in chronic hepatitis C: correlation with hepatic steatosis J Gastroenterol 40 2005 617 624
41. J. Yu, E.S. Chu, R. Wang, S. Wang, C.W. Wu, and V.W. Wong Heme oxygenase-1 protects against steatohepatitis in both cultured hepatocytes and mice Gastroenterology 138 2010 694-704.e691
42. F.H. Bach Heme oxygenase-1: a therapeutic amplification funnel FASEB J 19 2005 1216 1219
43. S. Shibahara, M. Nakayama, T. Kitamuro, R. Udono-Fujimori, and K. Takahashi Repression of heme oxygenase-1 expression as a defense strategy in humans Exp Biol Med 228 2003 472 473
44. D.M. Suttner, and P.A. Dennery Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron FASEB J 13 1999 1800 1809
45. E. Lehmann, W.H. El-Tantawy, M. Ocker, R. Bartenschlager, V. Lohmann, and S. Hashemolhosseini The heme oxygenase 1 product biliverdin interferes with hepatitis C virus replication by increasing antiviral interferon response Hepatology 51 2010 398 404
46. K. Devadas, and S. Dhawan Hemin activation ameliorates HIV-1 infection via heme oxygenase-1 induction J Immunol 176 2006 4252 4257
47. P. Stoll, C. Schwer, U. Goebel, H. Buerkle, A. Hoetzel, and R. Schmidt Hepatic steatosis prevents heme oxygenase-1 induction by isoflurane in the rat liver World J Gastroenterol 7 2011 4184 4190
48. S. Pal, S.J. Polyak, N. Bano, W.C. Qiu, R.L. Carithers, and M. Shuhart Hepatitis C virus induces oxidative stress, DNA damage and modulates the DNA repair enzyme NEIL1 J Gastroenterol Hepatol 2010 627 634
49. F. Farinati, R. Cardin, N. De Maria, G. Della Libera, C. Marafin, and E. Lecis Iron storage, lipid peroxidation and glutathione turnover in chronic anti-HCV positive hepatitis J Hepatol 22 1995 449 456
50. K. Otani, M. Korenaga, M.R. Beard, K. Li, T. Qian, and L.A. Showalter Hepatitis C virus core protein, cytochrome P450 2E1, and alcohol produce combined mitochondrial injury and cytotoxicity in hepatoma cells Gastroenterology 128 2005 96 107