Ethanol and reactive species increase basal sequence heterogeneity of hepatitis C virus and produce variants with reduced susceptibility to antivirals

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Seronello, Scott ^a   Montanez, Jessica ^a   Presleigh, Kristen ^a   Barlow, Miriam ^a   Park, Seung Bum ^a   Choi, Jinah ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETALDEHYDE; ALCOHOL; ALPHA INTERFERON; AMINO ACID; BUTHIONINE SULFOXIMINE; CYCLOSPORIN; GLUTATHIONE; HYDROGEN PEROXIDE; IRON CHELATING AGENT; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; RIBAVIRIN; VIRUS RNA; ANTIVIRUS AGENT;

AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CONTROLLED STUDY; GENE SEQUENCE; GENOTYPE; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; LIVER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE ANALYSIS; VIRUS GENE; VIRUS REPLICATION; CELL LINE; DRUG EFFECT; GENETIC VARIABILITY; GENETICS; OXIDATIVE STRESS;

HEPATITIS C VIRUS;

ANTIVIRAL AGENTS; BASE SEQUENCE; CELL LINE; DRUG RESISTANCE, VIRAL; ETHANOL; GENETIC VARIATION; HEPACIVIRUS; HUMANS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, VIRAL;

EID: 80555129637     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027436     Document Type: Article

References (76)

1. Hofmann WP, Zeuzem S, Sarrazin C, (2005) Hepatitis C virus-related resistance mechanisms to interferon alpha-based antiviral therapy. J Clin Virol 32: 86-91.
2. Pawlotsky JM, (2003) The nature of interferon-alpha resistance in hepatitis C virus infection. Curr Opin Infect Dis 16: 587-592.
3. Halfon P, Locarnini S, (2007) Hepatitis C virus resistance to protease inhibitors. J Hepatol 55: 192-206.
4. Zubkova I, Choi YH, Chang E, Pirollo K, Uren T, et al. (2009) T-cell vaccines that elicit effective immune responses against HCV in chimpanzees may create greater immune pressure for viral mutation. Vaccine 27: 2594-2602.
5. Duan H, Struble E, Zhong L, Mihalik K, Major M, et al. (2010) Hepatitis C virus with a naturally occurring single amino-acid substitution in the E2 envelope protein escapes neutralization by naturally-induced and vaccine-induced antibodies. Vaccine 28: 4138-4144.
6. Sherman KE, Rouster SD, Mendenhall C, Thee D, (1999) Hepatitis cRNA quasispecies complexity in patients with alcoholic liver disease. Hepatology 30: 265-270.
7. Takahashi K, Takahashi T, Takahashi S, Watanabe K, Boku S, et al. (2001) Difference in quasispecies of the hypervariable region 1 of hepatitis C virus between alcoholic and non-alcoholic patients. J Gastroenterol Hepatol 16: 416-423.
8. Seronello S, Sheikh MY, Choi J, (2007) Redox regulation of hepatitis C in nonalcoholic and alcoholic liver. Free Radic Biol Med 43: 869-882.
9. de Mochel NS, Seronello S, Wang SH, Ito C, Zheng JX, et al. (2010) Hepatocyte NAD(P)H oxidases as an endogenous source of reactive oxygen species during hepatitis C virus infection. Hepatology 52: 47-59.
10. Kong Q, Lin CL, (2010) Oxidative damage to RNA: mechanisms, consequences, and diseases. Cell Mol Life Sci 67: 1817-1829.
11. Kamiya H, Suzuki A, Yamaguchi Y, Handa H, Harashima H, (2009) Incorporation of 8-hydroxyguanosine (8-oxo-7,8-dihydroguanosine) 5'-triphosphate by bacterial and human RNA polymerases. Free Radic Biol Med 46: 1703-1707.
12. Forman HJ, Cadenas E, (1997) Oxidative stress and signal transduction. New York Chapman & Hall.
13. Seronello S, Ito C, Wakita T, Choi J, (2010) Ethanol enhances hepatitis C virus replication through lipid metabolism and elevated NADH/NAD+. J Biol Chem 285: 845-854.
14. Choi J, Forman HJ, Ou JH, Lai MM, Seronello S, et al. (2006) Redox modulation of the hepatitis C virus replication complex is calcium dependent. Free Radic Biol Med 41: 1488-1498.
15. Barbaro G, Di Lorenzo G, Ribersani M, Soldini M, Giancaspro G, et al. (1999) Serum ferritin and hepatic glutathione concentrations in chronic hepatitis C patients related to the hepatitis C virus genotype. J Hepatol 30: 774-782.
16. Choi J, Lee KJ, Zheng Y, Yamaga AK, Lai MM, et al. (2004) Reactive oxygen species suppress hepatitis C virus RNA replication in human hepatoma cells. Hepatology 39: 81-89.
17. Huang Y, Staschke K, De Francesco R, Tan SL, (2007) Phosphorylation of hepatitis C virus NS5A nonstructural protein: a new paradigm for phosphorylation-dependent viral RNA replication? Virology 364: 1-9.
18. Rispeter K, Lu M, Behrens SE, Fumiko C, Yoshida T, et al. (2000) Hepatitis C virus variability: sequence analysis of an isolate after 10 years of chronic infection. Virus Genes 21: 179-188.
19. Doreswamy K, Shrilatha B, Rajeshkumar T, Muralidhara, (2004) Nickel-induced oxidative stress in testis of mice: evidence of DNA damage and genotoxic effects. J Androl 25: 996-1003.
20. Zhang T, Li Y, Lai JP, Douglas SD, Metzger DS, et al. (2003) Alcohol potentiates hepatitis C virus replicon expression. Hepatology 38: 57-65.
21. Trujillo-Murillo K, Alvarez-Martinez O, Garza-Rodriguez L, Martinez-Rodriguez H, Bosques-Padilla F, et al. (2007) Additive effect of ethanol and HCV subgenomic replicon expression on COX-2 protein levels and activity. J Viral Hepat 14: 608-617.
22. Huang H, Chen Y, Ye J, (2007) Inhibition of hepatitis C virus replication by peroxidation of arachidonate and restoration by vitamin E. Proc Natl Acad Sci U S A 104: 18666-18670.
23. Kuroki M, Ariumi Y, Ikeda M, Dansako H, Wakita T, et al. (2009) Arsenic trioxide inhibits hepatitis C virus RNA replication through modulation of the glutathione redox system and oxidative stress. J Virol 83: 2338-2348.
24. Kapadia SB, Chisari FV, (2005) Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc Natl Acad Sci U S A 102: 2561-2566.
25. Kohashi T, Maekawa S, Sakamoto N, Kurosaki M, Watanabe H, et al. (2006) Site-specific mutation of the interferon sensitivity-determining region (ISDR) modulates hepatitis C virus replication. J Viral Hepat 13: 582-590.
26. El-Shamy A, Nagano-Fujii M, Sasase N, Imoto S, Kim SR, et al. (2008) Sequence variation in hepatitis C virus nonstructural protein 5A predicts clinical outcome of pegylated interferon/ribavirin combination therapy. Hepatology 48: 38-47.
27. Eysseric H, Gonthier B, Soubeyran A, Bessard G, Saxod R, et al. (1997) There is not simple method to maintain a constant ethanol concentration in long-term cell culture: keys to a solution applied to the survey of astrocytic ethanol absorption. Alcohol 14: 111-115.
28. Tsukamoto S, Muto T, Nagoya T, Shimamura M, Saito M, et al. (1989) Determinations of ethanol, acetaldehyde and acetate in blood and urine during alcohol oxidation in man. Alcohol Alcohol 24: 101-108.
29. Bull JJ, Sanjuan R, Wilke CO, (2007) Theory of lethal mutagenesis for viruses. J Virol 81: 2930-2939.
30. Domingo E, Gomez J, (2007) Quasispecies and its impact on viral hepatitis. Virus Res 127: 131-150.
31. Choi J, Lee KJ, Zheng Y, Yamaga AK, Lai MMC, et al. (2004) Reactive oxygen species suppress hepatitis C virus RNA replication in human hepatoma cells. Hepatology 39: 81-89.
32. Sata M, Fukuizumi K, Uchimura Y, Nakano H, Ishii K, et al. (1996) Hepatitis C virus infection in patients with clinically diagnosed alcoholic liver diseases. J Viral Hepat 3: 143-148.
33. Oshita M, Hayashi N, Kasahara A, Hagiwara H, Mita E, et al. (1994) Increased serum hepatitis C virus RNA levels among alcoholic patients with chronic hepatitis C. Hepatology 20: 1115-1120.
34. Pessione F, Degos F, Marcellin P, Duchatelle V, Njapoum C, et al. (1998) Effect of alcohol consumption on serum hepatitis C virus RNA and histological lesions in chronic hepatitis C. Hepatology 27: 1717-1722.
35. Romero-Gomez M, Grande L, Nogales MC, Fernandez M, Chavez M, et al. (2001) Intrahepatic hepatitis C virus replication is increased in patients with regular alcohol consumption. Dig Liver Dis 33: 698-702.
36. Sawada M, Takada A, Takase S, Takada N, (1993) Effects of alcohol on the replication of hepatitis C virus. Alcohol Alcohol Suppl 1B: 85-90.
37. Carriere M, Rosenberg AR, Conti F, Chouzenoux S, Terris B, et al. (2006) Low density lipoprotein receptor transcripts correlates with liver hepatitis C virus RNA in patients with alcohol consumption. J Viral Hepat 13: 633-642.
38. Cromie SL, Jenkins PJ, Bowden DS, Dudley FJ, (1996) Chronic hepatitis C: effect of alcohol on hepatitic activity and viral titre. J Hepatol 25: 821-826.
39. Sanjuan R, Cuevas JM, Furio V, Holmes EC, Moya A, (2007) Selection for robustness in mutagenized RNA viruses. PLoS Genet 3: e93.
40. Pfeiffer JK, Kirkegaard K, (2005) Ribavirin resistance in hepatitis C virus replicon-containing cell lines conferred by changes in the cell line or mutations in the replicon RNA. J Virol 79: 2346-2355.
41. Yano M, Ikeda M, Abe K, Kawai Y, Kuroki M, et al. (2009) Oxidative stress induces anti-hepatitis C virus status via the activation of extracellular signal-regulated kinase. Hepatology 50: 678-688.
42. Simon AR, Rai U, Fanburg BL, Cochran BH, (1998) Activation of the JAK-STAT pathway by reactive oxygen species. Am J Physiol 275: C1640-1652.
43. Burlando B, Magnelli V, Panfoli I, Berti E, Viarengo A, (2003) Ligand-independent tyrosine kinase signalling in RTH 149 trout hepatoma cells: comparison among heavy metals and pro-oxidants. Cell Physiol Biochem 13: 147-154.
44. Lee SR, Kwon KS, Kim SR, Rhee SG, (1998) Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J Biol Chem 273: 15366-15372.
45. Dickinson DA, Forman HJ, (2002) Glutathione in defense and signaling: lessons from a small thiol. Ann N Y Acad Sci 973: 488-504.
46. Osada S, Imai H, Tomita H, Tokuyma Y, Okumura N, et al. (2006) Vascular endothelial growth factor protects hepatoma cells against oxidative stress-induced cell death. J Gastroenterol Hepatol 21: 988-993.
47. Haviryaji KS, Vemuri MC, (1997) Effect of ethanol on nuclear casein kinase II activity in brain. Neurochem Res 22: 699-704.
48. Yano M, Ikeda M, Abe KI, Dansako H, Ohkoshi S, et al. (2007) Comprehensive Analysis of the Effects of Ordinary Nutrients on Hepatitis C Virus RNA Replication in Cell Culture. Antimicrob Agents Chemother 51: 2016-2027.
49. Tsutsumi T, Suzuki T, Moriya K, Shintani Y, Fujie H, et al. (2003) Hepatitis C virus core protein activates ERK and p38 MAPK in cooperation with ethanol in transgenic mice. Hepatology 38: 820-828.
50. Svegliati-Baroni G, Ridolfi F, Di Sario A, Saccomanno S, Bendia E, et al. (2001) Intracellular signaling pathways involved in acetaldehyde-induced collagen and fibronectin gene expression in human hepatic stellate cells. Hepatology 33: 1130-1140.
51. Lin W, Tsai WL, Shao RX, Wu G, Peng LF, et al. (2010) Hepatitis C virus regulates transforming growth factor beta1 production through the generation of reactive oxygen species in a nuclear factor kappaB-dependent manner. Gastroenterology 138: 2509-2518, 2518 e2501.
52. Bebenek K, Boyer JC, Kunkel TA, (1999) The base substitution fidelity of HIV-1 reverse transcriptase on DNA and RNA templates probed with 8-oxo-deoxyguanosine triphosphate. Mutat Res 429: 149-158.
53. Burney S, Caulfield JL, Niles JC, Wishnok JS, Tannenbaum SR, (1999) The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat Res 424: 37-49.
54. Freistadt MS, Vaccaro JA, Eberle KE, (2007) Biochemical characterization of the fidelity of poliovirus RNA-dependent RNA polymerase. Virol J 4: 44.
55. Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J, (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 266: 37-56.
56. Beloqui O, Prieto J, Suarez M, Gil B, Qian CH, et al. (1993) N-acetyl cysteine enhances the response to interferon-alpha in chronic hepatitis C: a pilot study. J Interferon Res 13: 279-282.
57. Fargion S, Fracanzani AL, Sampietro M, Molteni V, Boldorini R, et al. (1997) Liver iron influences the response to interferon alpha therapy in chronic hepatitis C. Eur J Gastroenterol Hepatol 9: 497-503.
58. Fong TL, Han SH, Tsai NC, Morgan TR, Mizokami M, et al. (1998) A pilot randomized, controlled trial of the effect of iron depletion on long-term response to alpha-interferon in patients with chronic hepatitis C. J Hepatol 28: 369-374.
59. Look MP, Gerard A, Rao GS, Sudhop T, Fischer HP, et al. (1999) Interferon/antioxidant combination therapy for chronic hepatitis C--a controlled pilot trial. Antiviral Res 43: 113-122.
60. Fontana RJ, Israel J, LeClair P, Banner BF, Tortorelli K, et al. (2000) Iron reduction before and during interferon therapy of chronic hepatitis C: results of a multicenter, randomized, controlled trial. Hepatology 31: 730-736.
61. Gentile I, Viola C, Paesano L, D'Onofrio M, D'Agostino E, et al. (2009) Iron depletion before HCV antiviral therapy: a pilot, randomized, controlled trial. J Clin Apher 24: 190-196.
62. Feld JJ, Modi AA, El-Diwany R, Rotman Y, Thomas E, et al. (2011) S-adenosyl methionine improves early viral responses and interferon-stimulated gene induction in hepatitis C nonresponders. Gastroenterology 140: 830-839.
63. Filipowicz M, Bernsmeier C, Terracciano L, Duong FH, Heim MH, (2011) S-adenosyl-methionine and betaine improve early virological response in chronic hepatitis C patients with previous nonresponse. PLoS One 5: e15492.
64. Akaike T, (2001) Role of free radicals in viral pathogenesis and mutation. Rev Med Virol 11: 87-101.
65. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, et al. (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11: 791-796.
66. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J, (1982) Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42: 3858-3863.
67. Taguchi T, Nagano-Fujii M, Akutsu M, Kadoya H, Ohgimoto S, et al. (2004) Hepatitis C virus NS5A protein interacts with 2',5'-oligoadenylate synthetase and inhibits antiviral activity of IFN in an IFN sensitivity-determining region-independent manner. J Gen Virol 85: 959-969.
68. Fernandes F, Ansari IU, Striker R, (2010) cyclosporine inhibits a direct interaction between cyclophilins and hepatitis C NS5A. PLoS One 5: e9815.
69. Yang F, Robotham JM, Grise H, Frausto S, Madan V, et al. (2010) A major determinant of cyclophilin dependence and cyclosporine susceptibility of hepatitis C virus identified by a genetic approach. PLoS Pathog 6: e1001118.
70. Chatterji U, Lim P, Bobardt MD, Wieland S, Cordek DG, et al. (2010) HCV resistance to cyclosporin A does not correlate with a resistance of the NS5A-cyclophilin A interaction to cyclophilin inhibitors. J Hepatol 53: 50-56.
71. Fernandes F, Poole DS, Hoover S, Middleton R, Andrei AC, et al. (2007) Sensitivity of hepatitis C virus to cyclosporine A depends on nonstructural proteins NS5A and NS5B. Hepatology 46: 1026-1033.
72. Noguchi T, Otsubaki T, Ando I, Ogura N, Ikeda S, et al. (2008) Isolation and gene analysis of interferon alpha-resistant cell clones of the hepatitis C virus subgenome. Virology 375: 424-432.
73. Thomson M, Nascimbeni M, Gonzales S, Murthy KK, Rehermann B, et al. (2001) Emergence of a distinct pattern of viral mutations in chimpanzees infected with a homogeneous inoculum of hepatitis C virus. Gastroenterology 121: 1226-1233.
74. Hwang DR, Lai HY, Chang ML, Hsu JT, Yeh CT, (2005) Emergence of mutation clusters in the HCV genome during sequential viral passages in Sip-L expressing cells. J Virol Methods 129: 170-177.
75. Sumpter R Jr, Wang C, Foy E, Loo YM, Gale M Jr, (2004) Viral evolution and interferon resistance of hepatitis C virus RNA replication in a cell culture model. J Virol 78: 11591-11604.
76. Tellinghuisen TL, Foss KL, Treadaway JC, Rice CM, (2008) Identification of residues required for RNA replication in domains II and III of the hepatitis C virus NS5A protein. J Virol 82: 1073-1083.