Differential contribution of hepatitis C virus NS5A and core proteins to the induction of oxidative and nitrosative stress in human hepatocyte-derived cells

Journal of Hepatology

Volumn 43, Issue 4, 2005, Pages 606-613

  García Mediavilla, María Victoria ^a   Sánchez Campos, Sonia ^a   González Pérez, Pilar ^a   Gómez Gonzalo, Marta ^c   Majano, Pedro Lorenzo ^b   López Cabrera, Manuel ^c   Clemente, Gerardo ^b   García Monzón, Carmelo ^b   González Gallego, Javier ^a  

^a UNIVERSITY OF LEÓN   (Spain)

^b HOSPITAL UNIVERSITARIO SANTA CRISTINA   (Spain)

^c HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

Author keywords

Core protein; Hepatitis C virus; Inducible nitric oxide synthase; NS5A protein; Oxidative nitrosative stress

Indexed keywords

3 NITROTYROSINE; CORE PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LUCIFERASE; NONSTRUCTURAL PROTEIN 5A; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CELL RESPIRATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ASSAY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIVER CELL; NITROSATIVE STRESS; NORTHERN BLOTTING; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

CELL LINE; FLOW CYTOMETRY; GENES, REPORTER; HEPACIVIRUS; HEPATOCYTES; HUMANS; INFLAMMATION; LUCIFERASES; MODELS, BIOLOGICAL; NITRATES; NITROGEN COMPOUNDS; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; REACTIVE OXYGEN SPECIES; TRANSFECTION; VIRAL CORE PROTEINS;

EID: 24344440908     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2005.04.019     Document Type: Article

References (47)

1. B. Robertson, G. Myers, C. Howard, T. Brettin, J. Bukh, and B. Gaschen Classification, nomenclature, and database development for hepatitis C virus (HCV) and related viruses: proposals for standardization. International Committee on Virus Taxonomy Arch Virol 143 1998 2493 2503
2. K.E. Reed, and C.M. Rice Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties Curr Top Microbiol Immunol 242 2000 55 84
3. R. Bartenschlager, and V. Lohmann Replication of hepatitis C virus J Gen Virol 81 2000 1631 1648
4. I. Saito, T. Miyamura, A. Ohbayashi, H. Harada, T. Katayama, and S. Kikuchi Hepatitis C virus infection is associated with the development of hepatocellular carcinoma Proc Natl Acad Sci USA 87 1990 6547 6549
5. J.H. Hoofnagle Hepatitis C: the clinical spectrum of disease Hepatology 26 1997 15S 20S
6. R.P. González-Peralta, G.L. Davis, and J.Y. Lau Pathogenic mechanism of hepatocellular damage in chronic hepatitis C virus infection J Hepatol 21 1994 255 259
7. B. Rehermann, and F.V. Chisari Cell mediated immune response to the hepatitis C virus Curr Top Microbiol Immunol 242 2000 299 325
8. C.S. Lieber Role of oxidative stress and antioxidant therapy in alcoholic and non-alcoholic liver diseases Adv Pharmacol 38 1997 601 628
9. V. Higueras, A. Raya, J.M. Rodrigo, M.A. Serra, J. Roma, and F.J. Romero Interferon decreases serum lipid peroxidation products of hepatitis C patients Free Rad Biol Med 16 1994 131 133
10. F. Kageyama, Y. Kobayashi, T. Kawasaki, S. Toyokuni, K. Uchida, and H. Nakamura Successful interferon therapy reverses enhanced hepatic iron accumulation and lipid peroxidation in chronic hepatitis C Am J Gastroenterol 95 2000 1041 1050
11. N. Kato, H. Yoshida, S.K. Ono-Nita, J. Kato, T. Goto, and M. Otsuka Activation of intracellular signaling by hepatitis B and C viruses: C-viral core is the most potent signal inducer Hepatology 32 2000 405 412
12. G. Gong, G. Waris, R. Tanveer, and A. Siddiqui Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress and activates STAT-3 and NF-kappa B Proc Natl Acad Sci USA 98 2001 9599 9604
13. M.M. Lai Hepatitis C virus proteins: direct link to hepatic oxidative stress, steatosis, carcinogenesis and more Gastroenterology 122 2002 568 571
14. 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
15. S. Moncada, and A. Higgs The l-arginine-nitric oxide pathway N Engl J Med 329 1993 2002 2012
16. T. Nguyen, D. Brunson, C.L. Crespi, B. Penman, J.S. Wishnok, and S.R. Tannenbaum DNA damage and mutation in human cells exposed to nitric oxide in vitro Proc Natl Acad Sci USA 89 1992 3030 3034
17. C.R. Lyons The role of nitric oxide in inflammation Adv Immunol 60 1995 323 371
18. P.L. Majano, C. García-Monzón, M. López-Cabrera, E. Lara-Pezzi, E. Fernández-Ruiz, and C. García-Iglesias Inducible nitric oxide synthase expression in chronic viral hepatitis. Evidence for a virus-induced gene upregulation J Clin Invest 101 1998 1343 1352
19. S. Mihm, A. Fayyazi, and G. Ramadori Hepatic expression of inducible nitric oxide synthase transcripts in chronic hepatitis C virus infection: relation to hepatic viral load and liver injury Hepatology 26 1997 451 458
20. H. Ischiropoulos, L. Zhu, J. Chen, M. Tsai, J.C. Martin, and C.D. Smith Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase Arch Biochem Biophys 298 1992 431 437
21. J.S. Stamler Redox signaling: nitrosylation and related target interactions of nitric oxide Cell 78 1994 931 936
22. C. García-Monzón, P.L. Majano, I. Zubia, P. Sanz, A. Apolonario, and R. Moreno-Otero Intrahepatic accumulation of nitrotyrosine in chronic viral hepatitis is associated with histological severity of liver disease J Hepatol 32 2000 331 338
23. N. Zhu, A. Khoshnan, R. Schneider, M. Matsumoto, G. Dennert, and C. Gare Hepatitis C virus core protein binds to the cytoplasmatic domain of tumor necrosis factor (TNF) receptor 1 and enhances TNF-induced apoptosis J Virol 72 1998 3691 3697
24. J. Marks-Konczalik, S.C. Chu, and J. Moss Cytokine-mediated transcriptional induction of the human inducible nitric oxide synthase gene requires both activator protein 1 and nuclear factor-κB-binding sites J Biol Chem 273 1998 22201 22208
25. J.S. Lee, and S.S. Thorgeirsson Functional and genomic implications of global gene expression profiles in cell lines from human hepatocellular cancer Hepatology 35 2002 1134 1143
26. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods 25 2001 402 408
27. M.J. Tuñón, S. Sánchez-Campos, B. Gutiérrez, M.J. Culebras, and J. González-Gallego Effects of FK506 and rapamycin on generation of reactive oxygen species, nitric oxide production and nuclear factor kappa B activation in rat hepatocytes Biochem Pharmacol 66 2003 439 445
28. A.S. Keston, and T.R. Brand The fluorimetric analysis of ultramicro quantities of hydrogen peroxide Anal Biochem 11 1965 1 5
29. P.G. Gunasekar, A.G. Kanthasamy, J.L. Borowitz, and G.E. Isom Monitoring intracellular nitric oxide formation by dichlorofluorescin in neuronal cells J Neurosci Methods 61 1995 15 21
30. C. Gabriel, A. Camins, F.X. Sureda, L. Aquirre, E. Escubedo, and M. Pallas Determination of nitric oxide generation in mammalian neurons using dichlorofluorescin diacetate and flow cytometry J Pharmacol Toxicol Methods 38 1997 93 98
31. H. Possel, H. Noack, W. Augustin, G. Keilhoff, and G. Wolf 2,7-Dihydrodiclorofluorescein diacetate as a fluorescent marker for peroxynitrite formation Fed Eur Biochem Soc Lett 416 1997 175 178
32. N. De Maria, A. Colantoni, S. Fagiuoli, G.-J. Liu, B.K. Rogers, and F. Farinati Association between reactive oxygen species and disease activity in chronic hepatitis C Free Rad Biol Med 21 1996 291 295
33. F. Morisco, V. Verde, V. Fogliano, A. Ritieni, R. Marmo, and G. De Luise Oxidative status in chronic hepatitis C: the influence of antiviral therapy and prognostic value of serum hydroperoxide assay Free Radic Res 38 2004 573 580
34. S. Cuzzocrea, B. Zingarelli, D. Villari, A.P. Caputi, and G. Longo Evidence for in vivo peroxynitrite production in human chronic hepatitis Life Sci 63 1998 25 30
35. S. Schweyer, S. Mihm, H.J. Radzun, H. Hartmann, and A. Fayyazi Liver infiltrating T lymphocytes express interferon gamma and inducible nitric oxide synthase in chronic hepatitis C virus infection Gut 46 2000 255 259
36. G.R. Reyes The nonstructural NS5A protein of hepatitis C virus: an expanding, multifunctional role in enhancing hepatitis C virus pathogenesis J Biomed Sci 9 2002 187 197
37. T. Yoshida, T. Hanada, T. Tokuhisa, K. Kosai, M. Sata, and M. Kohara Activation of STAT3 by the hepatitis C virus core protein leads to cellular transformation J Exp Med 196 2002 641 653
38. D.I. Tai, S.L. Tsai, Y.M. Chen, Y.L. Chuang, C.Y. Peng, and I.S. Sheen Activation of nuclear factor kappaB in hepatitis C virus infection: implications for pathogenesis and hepatocarcinogenesis Hepatology 31 2000 656 664
39. P. Boya, E. Larrea, I. Sola, P.L. Majano, C. Jiménez, and M.P. Civeira Nuclear factor-kappa B in the liver of patients with chronic hepatitis C: decreased RelA expression is associated with enhanced fibrosis progression Hepatology 34 2001 1041 1048
40. S. de Lucas, J. Bartolome, M.J. Amaro, and V. Carreno Hepatitis C virus core protein transactivates the inducible nitric oxide synthase promoter via NF-kappaB activation Antivir Res 60 2003 117 124
41. L.R. You, C.M. Chen, and Y.H. Lee Hepatitis C virus core protein enhances NF-kappaB signal pathway triggering by lymphotoxin-beta receptor ligand and tumor necrosis factor alpha J Virol 73 1999 1672 1681
42. Y.M. Chung, K.J. Park, S.Y. Choi, S.B. Hwang, and S.Y. Lee Hepatitis C virus core protein potentiates TNF-alpha-induced NF-kappaB activation through TRAF2-IKKbeta-dependent pathway Biochem Biophys Res Commun 284 2001 15 19
43. A. Shrivastava, S.K. Manna, R. Ray, and B.B. Aggarwal Ectopic expression of hepatitis C virus core protein differentially regulates nuclear transcription factors J Virol 72 1998 9722 9728
44. N. Zhu, A. Khoshnan, R. Schneider, M. Matsumoto, G. Dennert, and C. Ware Hepatitis C virus core protein binds to the cytoplasmic domain of tumor necrosis factor (TNF) receptor 1 and enhances TNF-induced apoptosis J Virol 72 1998 3691 3697
45. K.J. Park, S.H. Choi, S.Y. Lee, S.B. Hwang, and M.M. Lai Nonstructural 5A protein of hepatitis C virus modulates tumor necrosis factor alpha-stimulated nuclear factor kappa B activation J Biol Chem 277 2002 13122 13128
46. G. Waris, K.D. Tardif, and A. Siddiqui Endoplasmic reticulum (ER) stress: hepatitis C virus induce an ER-nucleus signal transduction pathway and activates NF-kappaB and STAT-3 Biochem Pharmacol 64 2002 1425 1430
47. G. Waris, A. Livolsi, V. Imbert, J.F. Peyron, and A. Siddiqui Hepatitis C virus NS5A and subgenomic replicon activate NF-kappaB via tyrosine phosphorylation of IkappaBalpha and its degradation by calpain protease J Biol Chem 278 2003 40778 40787