Ribavirin potentiates interferon action by augmenting interferon-stimulated gene induction in hepatitis C virus cell culture models

Hepatology

Volumn 53, Issue 1, 2011, Pages 32-41

  Thomas, Emmanuel ^a   Feld, Jordan J ^a,b   Li, Qisheng ^a   Hu, Zongyi ^a   Fried, Michael W ^c   Liang, T Jake ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b TORONTO WESTERN HOSPITAL   (Canada)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYCLOHEXIMIDE; DOUBLE STRANDED RNA; GUANOSINE DERIVATIVE; INTERFERON REGULATORY FACTOR 7; INTERFERON REGULATORY FACTOR 9; PEGINTERFERON; RIBAVIRIN;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; GENE; GENE EXPRESSION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IN VIVO STUDY; INTERFERON STIMULATED GENE; MICROARRAY ANALYSIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

DRUG SYNERGISM; GUANOSINE; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; INTERFERON ALFA-2A; INTERFERON REGULATORY FACTOR-7; INTERFERON-STIMULATED GENE FACTOR 3, GAMMA SUBUNIT; NF-KAPPA B; POLYETHYLENE GLYCOLS; PROTEINS; RIBAVIRIN; TUMOR CELLS, CULTURED;

EID: 78751545582     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.23985     Document Type: Article

References (62)

1. Sidwell RW, Huffman JH, Khare GP, Allen LB, Witkowski JT, Robins RK. Broad-spectrum antiviral activity of Virazole: 1-beta-D-ribofuranosyl-1, 2, 4-triazole-3-carboxamide. Science 1972; 177: 705-706.
2. Hoofnagle JH, Seeff LB. Peginterferon and ribavirin for chronic hepatitis C. N Engl J Med 2006; 355: 2444-2451.
3. Pawlotsky JM, Dahari H, Neumann AU, Hezode C, Germanidis G, Lonjon I, et al. Antiviral action of ribavirin in chronic hepatitis C. Gastroenterology 2004; 126: 703-714.
4. Fried MW, Shiffman ML, Reddy KR, Smith C, Marinos G, Gonçales FL Jr, et al. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 2002; 347: 975-982.
5. Dixit NM, Layden-Almer JE, Layden TJ, Perelson AS. Modelling how ribavirin improves interferon response rates in hepatitis C virus infection. Nature 2004; 432: 922-924.
6. Feld JJ, Hoofnagle JH. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 2005; 436: 967-972.
7. Hofmann WP, Herrmann E, Sarrazin C, Zeuzem S. Ribavirin mode of action in chronic hepatitis C: from clinical use back to molecular mechanisms. Liver Int 2008; 28: 1332-1343.
8. Crotty S, Maag D, Arnold JJ, Zhong W, Lau JY, Hong Z, et al. The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen. Nat Med 2000; 6: 1375-1379.
9. Crotty S, Cameron CE, Andino R. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad Sci U S A 2001; 98: 6895-6900.
10. Maag D, Castro C, Hong Z, Cameron CE. Hepatitis C virus RNA-dependent RNA polymerase (NS5B) as a mediator of the antiviral activity of ribavirin. J Biol Chem 2001; 276: 46094-46098.
11. Malinoski F, Stollar V. Inhibitors of IMP dehydrogenase prevent sindbis virus replication and reduce GTP levels in Aedes albopictus cells. Virology 1981; 110: 281-289.
12. Zhou S, Liu R, Baroudy BM, Malcolm BA, Reyes GR. The effect of ribavirin and IMPDH inhibitors on hepatitis C virus subgenomic replicon RNA. Virology 2003; 310: 333-342.
13. Tam RC, Pai B, Bard J, Lim C, Averett DR, Phan UT, et al. Ribavirin polarizes human T cell responses towards a Type 1 cytokine profile. J Hepatol 1999; 30: 376-382.
14. Feld JJ, Nanda S, Huang Y, Chen W, Cam M, Pusek SN, et al. Hepatic gene expression during treatment with peginterferon and ribavirin: identifying molecular pathways for treatment response. HEPATOLOGY 2007; 46: 1548-1563.
15. Zhang Y, Jamaluddin M, Wang S, Tian B, Garofalo RP, Casola A, et al. Ribavirin treatment up-regulates antiviral gene expression via the interferon-stimulated response element in respiratory syncytial virus-infected epithelial cells. J Virol 2003; 77: 5933-5947.
16. Feld JJ, Lutchman GA, Heller T, Hara K, Pfeiffer JK, Leff RD, et al. Ribavirin improves early responses to peginterferon through improved interferon signaling. Gastroenterology 2010; 139: 154-162.
17. Borden EC, Sen GC, Uze G, Silverman RH, Ransohoff RM, Foster GR, et al. Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov 2007; 6: 975-990.
18. Brok J, Gluud LL, Gluud C. Ribavirin monotherapy for chronic hepatitis C infection: a Cochrane Hepato-Biliary Group systematic review and meta-analysis of randomized trials. Am J Gastroenterol 2006; 101: 842-847.
19. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, et al. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 2005; 102: 9294-9299.
20. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 2005; 11: 791-796.
21. Zhang J, Randall G, Higginbottom A, Monk P, Rice CM, McKeating JA. CD81 is required for hepatitis C virus glycoprotein-mediated viral infection. J Virol 2004; 78: 1448-1455.
22. Chen L, Borozan I, Feld J, Sun J, Tannis LL, Coltescu C, et al. Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 2005; 128: 1437-1444.
23. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, Munk ME, et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010; 327: 198-201.
24. Walters KA, Syder AJ, Lederer SL, Diamond DL, Paeper B, Rice CM, et al. Genomic analysis reveals a potential role for cell cycle perturbation in HCV-mediated apoptosis of cultured hepatocytes. PLoS Pathog 2009; 5( 1): e1000269.
25. Sumpter R Jr, Loo Y-M, Foy E, Li K, Yoneyama M, Fujita T, et al. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 2005; 79: 2689-2699.
26. Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, et al. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000; 13: 539-548.
27. Yarilina A, Park-Min KH, Antoniv T, Hu X, Ivashkiv LB. TNF activates an IRF1-dependent autocrine loop leading to sustained expression of chemokines and STAT1-dependent type I interferon-response genes. Nat Immunol 2008; 9: 378-387.
28. Lee DH, Goldberg AL. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol 1998; 8: 397-403.
29. Hellerbrand C, Jobin C, Iimuro Y, Licato L, Sartor RB, Brenner DA. Inhibition of NFkappaB in activated rat hepatic stellate cells by proteasome inhibitors and an IkappaB super-repressor. HEPATOLOGY 1998; 27: 1285-1295.
30. Doyle SL, O'Neill LA. Toll-like receptors: from the discovery of NFkappaB to new insights into transcriptional regulations in innate immunity. Biochem Pharmacol 2006; 72: 1102-1113.
31. Takeuchi O, Akira S. MyD88 as a bottle neck in Toll/IL-1 signaling. Curr Top Microbiol Immunol 2002; 270: 155-167.
32. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 2005; 6: 981-988.
33. Onoguchi K, Yoneyama M, Takemura A, Akira S, Taniguchi T, Namiki H, et al. Viral infections activate types I and III interferon genes through a common mechanism. J Biol Chem 2007; 282: 7576-7581.
34. Kisseleva T, Brenner DA. Role of hepatic stellate cells in fibrogenesis and the reversal of fibrosis. J Gastroenterol Hepatol 2007; 22( Suppl. 1): S73-S78.
35. Hoofnagle JH, Ghany MG, Kleiner DE, Doo E, Heller T, Promrat K, et al. Maintenance therapy with ribavirin in patients with chronic hepatitis C who fail to respond to combination therapy with interferon alfa and ribavirin. HEPATOLOGY 2003; 38: 66-74.
36. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005; 434: 772-777.
37. Kimura T, Kadokawa Y, Harada H, Matsumoto M, Sato M, Kashiwazaki Y, et al. Essential and non-redundant roles of p48 (ISGF3 gamma) and IRF-1 in both type I and type II interferon responses, as revealed by gene targeting studies. Genes Cells 1996; 1: 115-124.
38. Randall G, Panis M, Cooper JD, Tellinghuisen TL, Sukhodolets KE, Pfeffer S, et al. Cellular cofactors affecting hepatitis C virus infection and replication. Proc Natl Acad Sci U S A 2007; 104: 12884-12889.
39. Taylor MW, Tsukahara T, Brodsky L, Schaley J, Sanda C, Stephens MJ, et al. Changes in gene expression during pegylated interferon and ribavirin therapy of chronic hepatitis C virus distinguish responders from nonresponders to antiviral therapy. J Virol 2007; 81: 3391-3401.
40. Sen GC, Sarkar SN. The interferon-stimulated genes: targets of direct signaling by interferons, double-stranded RNA, and viruses. Curr Top Microbiol Immunol 2007; 316: 233-250.
41. Lanford RE, Guerra B, Lee H, Averett DR, Pfeiffer B, Chavez D, et al. Antiviral effect and virus-host interactions in response to alpha interferon, gamma interferon, poly(i)-poly(c), tumor necrosis factor alpha, and ribavirin in hepatitis C virus subgenomic replicons. J Virol 2003; 77: 1092-1104.
42. Young KC, Lindsay KL, Lee KJ, Liu WC, He JW, Milstein SL, Lai MM. Identification of a ribavirin-resistant NS5B mutation of hepatitis C virus during ribavirin monotherapy. HEPATOLOGY 2003; 38: 869-878.
43. Kim SS, Peng LF, Lin W, Choe WH, Sakamoto N, Schreiber SL, et al. A cell-based, high-throughput screen for small molecule regulators of hepatitis C virus replication. Gastroenterology 2007; 132: 311-320.
44. Fried MW, Jensen DM, Rodriguez-Torres M, Nyberg LM, Di Bisceglie AM, Morgan TR, et al. Improved outcomes in patients with hepatitis C with difficult-to-treat characteristics: randomized study of higher doses of peginterferon alpha-2a and ribavirin. HEPATOLOGY 2008; 48: 1033-1043.
45. Lindahl K, Stahle L, Bruchfeld A, Schvarcz R. High-dose ribavirin in combination with standard dose peginterferon for treatment of patients with chronic hepatitis C. HEPATOLOGY 2005; 41: 275-279.
46. Manns MP, McHutchison JG, Gordon SC, Rustgi VK, Shiffman M, Reindollar R, et al. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet 2001; 358: 958-965.
47. Snoeck E, Wade JR, Duff F, Lamb M, Jorga K. Predicting sustained virological response and anaemia in chronic hepatitis C patients treated with peginterferon alfa-2a (40KD) plus ribavirin. Br J Clin Pharmacol 2006; 62: 699-709.
48. Maynard M, Pradat P, Gagnieu MC, Souvignet C, Trepo C. Prediction of sustained virological response by ribavirin plasma concentration at week 4 of therapy in hepatitis C virus genotype 1 patients. Antivir Ther 2008; 13: 607-611.
49. Jen JF, Glue P, Gupta S, Zambas D, Hajian G. Population pharmacokinetic and pharmacodynamic analysis of ribavirin in patients with chronic hepatitis C. Ther Drug Monit 2000: 22: 555-565.
50. Toyoda H, Kumada T, Kiriyama S, Sone Y, Tanikawa M, Hisanaga Y, et al. Correlation of serum ribavirin concentration with pretreatment renal function estimates in patients with chronic hepatitis C receiving combination antiviral therapy with peginterferon and ribavirin. J Viral Hepat 2008; 15: 651-658.
51. Glue P. The clinical pharmacology of ribavirin. Semin Liver Dis 1999; 19(Suppl. 1): 17-24.
52. Baiocchi L, De Leonardis F, Delle Monache M, Nosotti L, Conti RL, Lenci I, et al. Plasma/erythrocyte ribavirin x100 ratio as an indicator of sustained virological response in HCV genotype 1 patients with early virological response. Antivir Ther 2010; 15: 633-639.
53. Homma M, Matsuzaki Y, Inoue Y, Shibata M, Mitamura K, Tanaka N, et al. Marked elevation of erythrocyte ribavirin levels in interferon and ribavirin-induced anemia. Clin Gastroenterol Hepatol 2004; 2: 337-339.
54. Ibarra KD, Pfeiffer JK. Reduced ribavirin antiviral efficacy via nucleoside transporter-mediated drug resistance. J Virol 2009; 83: 4538-4547.
55. Hu S, Xie Z, Onishi A, Yu X, Jiang L, Lin J, et al. Profiling the human protein-DNA interactome reveals ERK2 as a transcriptional repressor of interferon signaling. Cell 2009; 139: 610-622.
56. Henry SD, Metselaar HJ, Lonsdale RC, Kok A, Haagmans BL, Tilanus HW, et al. Mycophenolic acid inhibits hepatitis C virus replication and acts in synergy with cyclosporin A and interferon-alpha. Gastroenterology 2006; 131: 1452-1462.
57. Gish RG. Treating HCV with ribavirin analogues and ribavirin-like molecules. J Antimicrob Chemother 2006; 57: 8-13.
58. Rustgi VK, Lee WM, Lawitz E, Gordon SC, Afdhal N, Poordad F, et al. Merimepodib, pegylated interferon, and ribavirin in genotype 1 chronic hepatitis C pegylated interferon and ribavirin nonresponders. HEPATOLOGY 2009; 50: 1719-1726.
59. Gale M Jr, Foy EM. Evasion of intracellular host defence by hepatitis C virus. Nature 2005; 436: 939-945.
60. Shiffman ML. What future for ribavirin? Liver Int 2009; 29(Suppl. 1): 68-73.
61. Weiskirchen R, Gressner AM. Isolation and culture of hepatic stellate cells. Methods Mol Med 2005; 117: 99-113.
62. Kato T, Matsumura T, Heller T, Saito S, Sapp RK, Murthy K, et al. Production of infectious hepatitis C virus of various genotypes in cell cultures. J Virol 2007; 81: 4405-4411.