Identification of alpha interferon-induced envelope mutations of hepatitis C virus in vitro associated with increased viral fitness and interferon resistance

Journal of Virology

Volumn 87, Issue 23, 2013, Pages 12776-12793

  Serre, Stéphanie B N ^a,b   Krarup, Henrik B ^c   Bukh, Jens ^a,b   Gottwein, Judith M ^a,b  

^a Mental Health Services CPH   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c AALBORG UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ALPHA INTERFERON; ALPHA2B INTERFERON; GLUTAMIC ACID; ISOLEUCINE; PHENYLALANINE; THREONINE; VALINE; VIRUS PROTEIN;

ARTICLE; CELL STRAIN; CELL STRAIN HUH7.5; CONTROLLED STUDY; GENOTYPE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROBIAL ACTIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MODIFICATION; VIRAL GENETICS; VIRAL PHENOMENA AND FUNCTIONS; VIRUS CULTURE; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS MUTATION; VIRUS RECOMBINANT; VIRUS RELEASE; VIRUS RESISTANCE; VIRUS STRAIN; VIRUS TRANSMISSION;

ANTIVIRAL AGENTS; CELL LINE, TUMOR; DRUG RESISTANCE, VIRAL; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; INTERFERON-ALPHA; MUTATION, MISSENSE; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION; VIRUS SHEDDING;

EID: 84887158912     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00901-13     Document Type: Article

References (74)

1. Mohd HK, Groeger J, Flaxman AD, Wiersma ST. 2013. Global epidemiology of hepatitis C virus infection:new estimates of age-specific antibody to HCV seroprevalence. Hepatology 57:1333-1342.
2. Gottwein JM, Bukh J. 2008. Cutting the Gordian knot-development and biological relevance of hepatitis C virus cell culture systems. Adv. Virus Res. 71:51-133.
3. Simmonds P, Bukh J, Combet C, Deleage G, Enomoto N, Feinstone S, Halfon P, Inchauspe G, Kuiken C, Maertens G, Mizokami M, Murphy DG, Okamoto H, Pawlotsky JM, Penin F, Sablon E, Shin IT, Stuyver LJ, Thiel HJ, Viazov S, Weiner AJ, Widell A. 2005. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42:962-973.
4. Hoofnagle JH, Mullen KD, Jones DB, Rustgi V, Di BA, Peters M, Waggoner JG, Park Y, Jones EA. 1986. Treatment of chronic non-A, non-B hepatitis with recombinant human alpha interferon. A preliminary report. N. Engl. J. Med. 315:1575-1578.
5. Strader DB, Wright T, Thomas DL, Seeff LB. 2004. Diagnosis, management, and treatment of hepatitis C. Hepatology 39:1147-1171.
6. Heim MH. 2013. Innate immunity and HCV. J. Hepatol. 58:564-574.
7. Wohnsland A, Hofmann WP, Sarrazin C. 2007. Viral determinants of resistance to treatment in patients with hepatitis C. Clin. Microbiol. Rev. 20:23-38.
8. Asselah T, Estrabaud E, Bieche I, Lapalus M, De MS, Vidaud M, Saadoun D, Soumelis V, Marcellin P. 2010. Hepatitis C:viral and host factors associated with non-response to pegylated interferon plus ribavirin. Liver Int. 30:1259-1269.
9. Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, Heinzen EL, Qiu P, Bertelsen AH, Muir AJ, Sulkowski M, McHutchison JG, Goldstein DB. 2009. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 461:399-401.
10. Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O'Huigin C, Kidd J, Kidd K, Khakoo SI, Alexander G, Goedert JJ, Kirk GD, Donfield SM, Rosen HR, Tobler LH, Busch MP, McHutchison JG, Goldstein DB, Carrington M. 2009. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 461:798-801.
11. Estrabaud E, Vidaud M, Marcellin P, Asselah T. 2012. Genomics and HCVinfection:progression of fibrosis and treatment response. J. Hepatol. 57:1110-1125.
12. Farci P, Strazzera R, Alter HJ, Farci S, Degioannis D, Coiana A, Peddis G, Usai F, Serra G, Chessa L, Diaz G, Balestrieri A, Purcell RH. 2002. Early changes in hepatitis C viral quasispecies during interferon therapy predict the therapeutic outcome. Proc. Natl. Acad. Sci. U.S.A. 99:3081-3086.
13. Aus dem Siepen M, Oniangue-Ndza C, Wiese M, Ross S, Roggendorf M, Viazov S. 2007. Interferon-alpha and ribavirin resistance of Huh7 cells transfected with HCV subgenomic replicon. Virus Res. 125:109-113.
14. Naka K, Takemoto K, Abe K, Dansako H, Ikeda M, Shimotohno K, Kato N. 2005. Interferon resistance of hepatitis C virus repliconharbouring cells is caused by functional disruption of type I interferon receptors. J. Gen. Virol. 86:2787-2792.
15. Namba K, Naka K, Dansako H, Nozaki A, Ikeda M, Shiratori Y, Shimotohno K, Kato N. 2004. Establishment of hepatitis C virus replicon cell lines possessing interferon-resistant phenotype. Biochem. Biophys. Res. Commun. 323:299-309.
16. Hazari S, Taylor L, Haque S, Garry RF, Florman S, Luftig R, Regenstein F, Dash S. 2007. Reduced expression of Jak-1 and Tyk-2 proteins leads to interferon resistance in hepatitis C virus replicon. Virol. J. 4:89.
17. Zhu H, Nelson DR, Crawford JM, Liu C. 2005. Defective Jak-Stat activation in hepatoma cells is associated with hepatitis C viral IFN-alpha resistance. J. Interferon Cytokine Res. 25:528-539.
18. Guo JT, Bichko VV, Seeger C. 2001. Effect of alpha interferon on the hepatitis C virus replicon. J. Virol. 75:8516-8523.
19. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Krausslich HG, Mizokami M, Bartenschlager R, Liang TJ. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791-796.
20. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, Wieland SF, Uprichard SL, Wakita T, Chisari FV. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U.S.A. 102:9294-9299.
21. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA, Rice CM. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626.
22. Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, Steinmann E, Abid K, Negro F, Dreux M, Cosset FL, Bartenschlager R. 2006. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. U.S.A. 103:7408-7413.
23. Yi M, Ma Y, Yates J, Lemon SM. 2007. Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. J. Virol. 81:629-638.
24. Gottwein JM, Scheel TK, Jensen TB, Lademann JB, Prentoe JC, Knudsen ML, Hoegh AM, Bukh J. 2009. Development and characterization of hepatitis C virus genotype 1-7 cell culture systems:role of CD81 and scavenger receptor class B type I and effect of antiviral drugs. Hepatology 49:364-377.
25. Scheel TK, Gottwein JM, Jensen TB, Prentoe JC, Hoegh AM, Alter HJ, Eugen-Olsen J, Bukh J. 2008. Development of JFH1-based cell culture systems for hepatitis C virus genotype 4a and evidence for cross-genotype neutralization. Proc. Natl. Acad. Sci. U.S.A. 105:997-1002.
26. Scheel TK, Gottwein JM, Carlsen TH, Li YP, Jensen TB, Spengler U, Weis N, Bukh J. 2011. Efficient culture adaptation of hepatitis C virus recombinants with genotype-specific core-NS2 by using previously identified mutations. J. Virol. 85:2891-2906.
27. Gottwein JM, Scheel TK, Hoegh AM, Lademann JB, Eugen-Olsen J, Lisby G, Bukh J. 2007. Robust hepatitis C genotype 3a cell culture releasing adapted intergenotypic 3a/2a (S52/JFH1) viruses. Gastroenterology 133:1614-1626.
28. Callens N, Ciczora Y, Bartosch B, Vu-Dac N, Cosset FL, Pawlotsky JM, Penin F, Dubuisson J. 2005. Basic residues in hypervariable region 1 of hepatitis C virus envelope glycoprotein e2 contribute to virus entry. J. Virol. 79:15331-15341.
29. Pestka JM, Zeisel MB, Blaser E, Schurmann P, Bartosch B, Cosset FL, Patel AH, Meisel H, Baumert J, Viazov S, Rispeter K, Blum HE, Roggendorf M, Baumert TF. 2007. Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C. Proc. Natl. Acad. Sci. U.S.A. 104:6025-6030.
30. Carlsen TH, Scheel TK, Ramirez S, Foung SK, Bukh J. 2013. Characterization of hepatitis C virus recombinants with chimeric E1/E2 envelope proteins and identification of single amino acids in the E2 stem region important for entry. J. Virol. 87:1385-1399.
31. Blight KJ, McKeating JA, Rice CM. 2002. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 76: 13001-13014.
32. Russell RS, Meunier JC, Takikawa S, Faulk K, Engle RE, Bukh J, Purcell RH, Emerson SU. 2008. Advantages of a single-cycle production assay to study cell culture-adaptive mutations of hepatitis C virus. Proc. Natl. Acad. Sci. U.S.A. 105:4370-4375.
33. Dubuisson J, Hsu HH, Cheung RC, Greenberg HB, Russell DG, Rice CM. 1994. Formation and intracellular localization of hepatitis C virus envelope glycoprotein complexes expressed by recombinant vaccinia and Sindbis viruses. J. Virol. 68:6147-6160.
34. Albecka A, Montserret R, Krey T, Tarr AW, Diesis E, Ball JK, Descamps V, Duverlie G, Rey F, Penin F, Dubuisson J. 2011. Identification of new functional regions in hepatitis C virus envelope glycoprotein E2. J. Virol. 85:1777-1792.
35. Kuiken C, Combet C, Bukh J, Shin I, Deleage G, Mizokami M, Richardson R, Sablon E, Yusim K, Pawlotsky JM, Simmonds P. 2006. A comprehensive system for consistent numbering of HCV sequences, proteins and epitopes. Hepatology 44:1355-1361.
36. Combet C, Garnier N, Charavay C, Grando D, Crisan D, Lopez J, Dehne-Garcia A, Geourjon C, Bettler E, Hulo C, Le MP, Bartenschlager R, Diepolder H, Moradpour D, Pawlotsky JM, Rice CM, Trepo C, Penin F, Deleage G. 2007. euHCVdb:the European hepatitis C virus database. Nucleic Acids Res. 35:D363-D366.
37. Kuiken C, Mizokami M, Deleage G, Yusim K, Penin F, Shin I, Charavay C, Tao N, Crisan D, Grando D, Dalwani A, Geourjon C, Agrawal A, Combet C. 2006. Hepatitis C databases, principles and utility to researchers. Hepatology 43:1157-1165.
38. Gottwein JM, Scheel TK, Jensen TB, Ghanem L, Bukh J. 2011. Differential efficacy of protease inhibitors againstHCVgenotypes 2a, 3a, 5a, and 6a NS3/4A protease recombinant viruses. Gastroenterology 141:1067-1079.
39. Noguchi T, Otsubaki T, Ando I, Ogura N, Ikeda S, Shimotohno K. 2008. Isolation and gene analysis of interferon alpha-resistant cell clones of the hepatitis C virus subgenome. Virology 375:424-432.
40. Perales C, Beach NM, Gallego I, Soria ME, Quer J, Esteban JI, Rice C, Domingo E, Sheldon J. 2013. Response of hepatitis C virus to long-term passage in the presence of alpha interferon:multiple mutations and a common phenotype. J. Virol. 87:7593-7607.
41. Gottwein JM, Jensen TB, Mathiesen CK, Meuleman P, Serre SB, Lademann JB, Ghanem L, Scheel TK, Leroux-Roels G, Bukh J. 2011. Development and application of hepatitis C reporter viruses with genotype 1 to 7 core-nonstructural protein 2 (NS2) expressing fluorescent proteins or luciferase in modified JFH1 NS5A. J. Virol. 85:8913-8928.
42. Li K, Foy E, Ferreon JC, Nakamura M, Ferreon AC, Ikeda M, Ray SC, Gale M, Jr, Lemon SM. 2005. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl. Acad. Sci. U.S.A. 102:2992-2997.
43. Li K, Chen Z, Kato N, Gale M, Jr, Lemon SM. 2005. Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-beta production in hepatocytes. J. Biol. Chem. 280:16739-16747.
44. Sumpter R, Jr, Loo YM, Foy E, Li K, Yoneyama M, Fujita T, Lemon SM, Gale M, Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 79:2689-2699.
45. Li YP, Ramirez S, Gottwein JM, Bukh J. 2011. Non-genotype-specific role of the hepatitis C virus 5' untranslated region in virus production and in inhibition by interferon. Virology 421:222-234.
46. Scheel TK, Gottwein JM, Mikkelsen LS, Jensen TB, Bukh J. 2011. RecombinantHCVvariants with NS5A from genotypes 1-7 have different sensitivities to an NS5A inhibitor but not interferon-alpha. Gastroenterology 140:1032-1042.
47. Li YP, Ramirez S, Jensen SB, Purcell RH, Gottwein JM, Bukh J. 2012. Highly efficient full-length hepatitis C virus genotype 1 (strain TN) infectious culture system. Proc. Natl. Acad. Sci. U.S.A. 109:19757-19762.
48. 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.
49. Sarrazin C, Mihm U, Herrmann E, Welsch C, Albrecht M, Sarrazin U, Traver S, Lengauer T, Zeuzem S. 2005. Clinical significance of in vitro replication-enhancing mutations of the hepatitis C virus (HCV) replicon in patients with chronic HCV infection. J. Infect. Dis. 192:1710-1719.
50. Zhong J, Gastaminza P, Chung J, Stamataki Z, Isogawa M, Cheng G, McKeating JA, Chisari FV. 2006. Persistent hepatitis C virus infection in vitro:coevolution of virus and host. J. Virol. 80:11082-11093.
51. Li YP, Ramirez S, Gottwein JM, Scheel TK, Mikkelsen L, Purcell RH, Bukh J. 2012. Robust full-length hepatitis C virus genotype 2a and 2b infectious cultures using mutations identified by a systematic approach applicable to patient strains. Proc. Natl. Acad. Sci. U.S.A. 109:E1101-E1110.
52. Jensen TB, Gottwein JM, Scheel TK, Hoegh AM, Eugen-Olsen J, Bukh J. 2008. Highly efficient JFH1-based cell-culture system for hepatitis C virus genotype 5a:failure of homologous neutralizing-antibody treatment to control infection. J. Infect. Dis. 198:1756-1765.
53. Yi M, Villanueva RA, Thomas DL, Wakita T, Lemon SM. 2006. Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells. Proc. Natl. Acad. Sci. U.S.A. 103:2310-2315.
54. Imhof I, Simmonds P. 2010. Development of an intergenotypic hepatitis C virus (HCV) cell culture method to assess antiviral susceptibilities and resistance development of HCV NS3 protease genes from HCV genotypes 1 to 6. J. Virol. 84:4597-4610.
55. Shimakami T, Welsch C, Yamane D, McGivern DR, Yi M, Zeuzem S, Lemon SM. 2011. Protease inhibitor-resistant hepatitis C virus mutants with reduced fitness from impaired production of infectious virus. Gastroenterology 140:667-675.
56. Gottwein JM, Jensen SB, Li YP, Ghanem L, Scheel TK, Serre SB, Mikkelsen L, Bukh J. 2013. Combination treatment with hepatitis C virus protease and NS5A inhibitors is effective against recombinant genotype 1a, 2a, and 3a viruses. Antimicrob. Agents Chemother. 57:1291-1303.
57. McMullan LK, Grakoui A, Evans MJ, Mihalik K, Puig M, Branch AD, Feinstone SM, Rice CM. 2007. Evidence for a functional RNA element in the hepatitis C virus core gene. Proc. Natl. Acad. Sci. U.S.A. 104:2879-2884.
58. Sarrazin C, Zeuzem S. 2010. Resistance to direct antiviral agents in patients with hepatitis C virus infection. Gastroenterology 138:447-462.
59. Sarrazin C, Hezode C, Zeuzem S, Pawlotsky JM. 2012. Antiviral strategies in hepatitis C virus infection. J. Hepatol. 56(Suppl 1):S88-S100.
60. Susser S, Vermehren J, Forestier N, Welker MW, Grigorian N, Fuller C, Perner D, Zeuzem S, Sarrazin C. 2011. Analysis of long-term persistence of resistance mutations within the hepatitis C virus NS3 protease after treatment with telaprevir or boceprevir. J. Clin. Virol. 52:321-327.
61. Vuillermoz I, Khattab E, Sablon E, Ottevaere I, Durantel D, Vieux C, Trepo C, Zoulim F. 2004. Genetic variability of hepatitis C virus in chronically infected patients with viral breakthrough during interferonribavirin therapy. J. Med. Virol. 74:41-53.
62. Akuta N, Suzuki F, Kawamura Y, Yatsuji H, Sezaki H, Suzuki Y, Hosaka T, Kobayashi M, Kobayashi M, Arase Y, Ikeda K, Kumada H. 2007. Predictors of viral kinetics to peginterferon plus ribavirin combination therapy in Japanese patients infected with hepatitis C virus genotype 1b. J. Med. Virol. 79:1686-1695.
63. Akuta N, Suzuki F, Sezaki H, Suzuki Y, Hosaka T, Someya T, Kobayashi M, Saitoh S, Watahiki S, Sato J, Matsuda M, Kobayashi M, Arase Y, Ikeda K, Kumada H. 2005. Association of amino acid substitution pattern in core protein of hepatitis C virus genotype 1b high viral load and nonvirological response to interferon-ribavirin combination therapy. Intervirology 48:372-380.
64. Funaoka Y, Sakamoto N, Suda G, Itsui Y, Nakagawa M, Kakinuma S, Watanabe T, Mishima K, Ueyama M, Onozuka I, Nitta S, Kitazume A, Kiyohashi K, Murakawa M, Azuma S, Tsuchiya K, Watanabe M. 2011. Analysis of interferon signaling by infectious hepatitis C virus clones with substitutions of core amino acids 70 and 91. J. Virol. 85:5986-5994.
65. Taylor DR, Shi ST, Romano PR, Barber GN, Lai MM. 1999. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285:107-110.
66. Saludes V, Gonzalez-Candelas F, Planas R, Sola R, Ausina V, Martro E. 2013. Evolutionary dynamics of the E1-E2 viral populations during combination therapy in non-responder patients chronically infected with hepatitis C virus subtype 1b. Infect. Genet. Evol. 13:1-10.
67. Enomoto N, Sakuma I, Asahina Y, Kurosaki M, Murakami T, Yamamoto C, Izumi N, Marumo F, Sato C. 1995. Comparison of full-length sequences of interferon-sensitive and resistant hepatitisCvirus 1b. Sensitivity to interferon is conferred by amino acid substitutions in the NS5A region. J. Clin. Investig. 96:224-230.
68. Enomoto N, Sakuma I, Asahina Y, Kurosaki M, Murakami T, Yamamoto C, Ogura Y, Izumi N, Marumo F, Sato C. 1996. Mutations in the nonstructural protein 5A gene and response to interferon in patients with chronic hepatitis C virus 1b infection. N. Engl. J. Med. 334:77-81.
69. Yahoo N, Sabahi F, Shahzamani K, Malboobi MA, Jabbari H, Sharifi H, Mousavi-Fard SH, Merat S. 2011. Mutations in the E2 and NS5A regions in patients infected with hepatitis C virus genotype 1a and their correlation with response to treatment. J. Med. Virol. 83:1332-1337.
70. Wilkins C, Woodward J, Lau DT, Barnes A, Joyce M, McFarlane N, McKeating JA, Tyrrell DL, Gale M, Jr. 2013. IFITM1 is a tight junction protein that inhibits hepatitis C virus entry. Hepatology 57:461-469.
71. Schvoerer E, Moenne-Loccoz R, Murray JM, Velay A, Turek M, Fofana I, Fafi-Kremer S, Erba AC, Habersetzer F, Doffoel M, Gut JP, Donlin MJ, Tavis JE, Zeisel MB, Stoll-Keller F, Baumert TF. 2013. Hepatitis C virus envelope glycoprotein signatures are associated with treatment failure and modulation of viral entry and neutralization. J. Infect. Dis. 207: 1306-1315.
72. Helle F, Vieyres G, Elkrief L, Popescu CI, Wychowski C, Descamps V, Castelain S, Roingeard P, Duverlie G, Dubuisson J. 2010. Role of N-linked glycans in the functions of hepatitis C virus envelope proteins incorporated into infectious virions. J. Virol. 84:11905-11915.
73. Fraser J, Boo I, Poumbourios P, Drummer HE. 2011. Hepatitis C virus (HCV) envelope glycoproteins E1 and E2 contain reduced cysteine residues essential for virus entry. J. Biol. Chem. 286:31984-31992.
74. Kapadia SB, Barth H, Baumert T, McKeating JA, Chisari FV. 2007. Initiation of hepatitis C virus infection is dependent on cholesterol and cooperativity between CD81 and scavenger receptor B type I. J. Virol. 81:374-383.