Sequence diversity of hepatitis C virus: Implications for immune control and therapy

World Journal of Gastroenterology

Volumn 13, Issue 36, 2007, Pages 4808-4817

  Timm, Joerg ^a   Roggendorf, Michael ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Drug resistance; Escape; Evolution; Hepatitis C virus; Selection

Indexed keywords

ALPHA INTERFERON; ANTIVIRUS AGENT; CILUPREVIR; HCV 796; HEPATITIS C VACCINE; NONSTRUCTURAL PROTEIN 3; PEGINTERFERON; PLACEBO; PROTEINASE INHIBITOR; RIBAVIRIN; RNA POLYMERASE; SCH 503034; UNCLASSIFIED DRUG; VALOPICITABINE; VX 950;

ANTIVIRAL ACTIVITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DRUG EFFICACY; DRUG SENSITIVITY; EVOLUTIONARY ADAPTATION; GENE SEQUENCE; GENETIC DRIFT; GENETIC VARIABILITY; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNE RESPONSE; INFECTION CONTROL; INNATE IMMUNITY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MONOTHERAPY; NONHUMAN; PERSISTENT VIRUS INFECTION; PHYLOGENY; REVIEW; VIRUS GENOME; VIRUS ISOLATION; VIRUS MUTATION; VIRUS VIRULENCE;

EID: 34848881072     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v13.i36.4808     Document Type: Review

References (91)

1. World Health Organization. Hepatitis C-global prevalence (update). Weekly Epidemiological Record 1999; 74: 425
2. Fried MW, Shiffman ML, Reddy KR, Smith C, Marinos G, Goncales FL Jr, Haussinger D, Diago M, Carosi G, Dhumeaux D, Craxi A, Lin A, Hoffman J, Yu J. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 2002; 347: 975-982
3. Manns MP, McHutchison JG, Gordon SC, Rustgi VK, Shiffman M, Reindollar R, Goodman ZD, Koury K, Ling M, Albrecht JK. 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
4. Lindenbach BD, Rice CM. Unravelling hepatitis C virus replication from genome to function. Nature 2005; 436: 933-938
5. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Krausslich HG, Mizokami M, Bartenschlager R, Liang TJ. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 2005; 11: 791-796
6. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen JA, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA, Rice CM. Complete replication of hepatitis C virus in cell culture. Science 2005; 309: 623-626
7. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, Wieland SF, Uprichard SL, Wakita T, Chisari FV. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci USA 2005; 102: 9294-9299
8. Spahn CM, Kieft JS, Grassucci RA, Penczek PA, Zhou K, Doudna JA, Frank J. Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 2001; 291: 1959-1962
9. Lohmann V, Koch JO, Bartenschlager R. Processing pathways of the hepatitis C virus proteins. J Hepatol 1996; 24: 11-19
10. Liu Q, Tackney C, Bhat RA, Prince AM, Zhang P. Regulated processing of hepatitis C virus core protein is linked to subcellular localization. J Virol 1997; 71: 657-662
11. Bartosch B, Cosset FL. Cell entry of hepatitis C virus. Virology 2006; 348: 1-12
12. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G, Abrignani S. Binding of hepatitis C virus to CD81. Science 1998; 282: 938-941
13. Kapadia SB, Barth H, Baumert T, McKeating JA, Chisari FV. Initiation of hepatitis C virus infection is dependent on cholesterol and cooperativity between CD81 and scavenger receptor B type I. J Virol 2007; 81: 374-383
14. Akazawa D, Date T, Morikawa K, Murayama A, Miyamoto M, Kaga M, Barth H, Baumert TF, Dubuisson J, Wakita T. CD81 expression is important for the permissiveness of Huh7 cell clones for heterogeneous hepatitis C virus infection. J Virol 2007; 81: 5036-5045
15. Hsu M, Zhang J, Flint M, Logvinoff C, Cheng-Mayer C, Rice CM, McKeating JA. Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc Natl Acad Sci USA 2003; 100: 7271-7276
16. Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, Pascale S, Scarselli E, Cortese R, Nicosia A, Cosset FL. Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 2003; 278: 41624-41630
17. 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
18. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wolk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007; 446: 801-805
19. Pavlovic D, Neville DC, Argaud O, Blumberg B, Dwek RA, Fischer WB, Zitzmann N. The hepatitis C virus p7 protein forms an ion channel that is inhibited by long-alkyl-chain iminosugar derivatives. Proc Natl Acad Sci USA 2003; 100: 6104-6108
20. Griffin SD, Beales LP, Clarke DS, Worsfold O, Evans SD, Jaeger J, Harris MP, Rowlands DJ. The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, Amantadine. FEBS Lett 2003; 535: 34-38
21. Frick DN. The hepatitis C virus NS3 protein: a model RNA helicase and potential drug target. Curr Issues Mol Biol 2007; 9: 1-20
22. Tellinghuisen TL, Rice CM. Interaction between hepatitis C virus proteins and host cell factors. Curr Opin Microbiol 2002; 5: 419-427
23. Xu Z, Choi J, Yen TS, Lu W, Strohecker A, Govindarajan S, Chien D, Selby MJ, Ou J. Synthesis of a novel hepatitis C virus protein by ribosomal frameshift. EMBO J 2001; 20: 3840-3848
24. Simmonds P, Alberti A, Alter HJ, Bonino F, Bradley DW, Brechot C, Brouwer JT, Chan SW, Chayama K, Chen DS. A proposed system for the nomenclature of hepatitis C viral genotypes. Hepatology 1994; 19: 1321-1324
25. Pybus OG, Drummond AJ, Nakano T, Robertson BH, Rambaut A. The epidemiology and iatrogenic transmission of hepatitis C virus in Egypt: a Bayesian coalescent approach. Mol Biol Evol 2003; 20: 381-387
26. Ray SC, Arthur RR, Carella A, Bukh J, Thomas DL. Genetic epidemiology of hepatitis C virus throughout egypt. J Infect Dis 2000; 182: 698-707
27. Candotti D, Temple J, Sarkodie F, Allain JP. Frequent recovery and broad genotype 2 diversity characterize hepatitis C virus infection in Ghana, West Africa. J Virol 2003; 77: 7914-7923
28. Wong DA, Tong LK, Lim W. High prevalence of hepatitis C virus genotype 6 among certain risk groups in Hong Kong. Eur J Epidemiol 1998; 14: 421-426
29. Hissar SS, Goyal A, Kumar M, Pandey C, Suneetha PV, Sood A, Midha V, Sakhuja P, Malhotra V, Sarin SK. Hepatitis C virus genotype 3 predominates in North and Central India and is associated with significant histopathologic liver disease. J Med Virol 2006; 78: 452-458
30. 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-I T, Stuyver LJ, Thiel HJ, Viazov S, Weiner AJ, Widell A. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 2005; 42: 962-973
31. Combet C, Garnier N, Charavay C, Grando D, Crisan D, Lopez J, Dehne-Garcia A, Geourjon C, Bettler E, Hulo C, Le Mercier P, Bartenschlager R, Diepolder H, Moradpour D, Pawlotsky JM, Rice CM, Trepo C, Penin F, Deleage G. euHCVdb: the European hepatitis C virus database. Nucleic Acids Res 2007; 35: D363-D366
32. Kuiken C, Yusim K, Boykin L, Richardson R. The Los Alamos hepatitis C sequence database. Bioinformatics 2005; 21: 379-384
33. Simmonds P. Genetic diversity and evolution of hepatitis C virus-15 years on. J Gen Virol 2004; 85: 3173-3188
34. Drake JW, Charlesworth B, Charlesworth D, Crow JF. Rates of spontaneous mutation. Genetics 1998; 148: 1667-1686
35. Neumann AU, Lam NP, Dahari H, Gretch DR, Wiley TE, Layden TJ, Perelson AS. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science 1998; 282: 103-107
36. Quer J, Esteban JI, Cos J, Sauleda S, Ocana L, Martell M, Otero T, Cubero M, Palou E, Murillo P, Esteban R, Guardia J. Effect of bottlenecking on evolution of the nonstructural protein 3 gene of hepatitis C virus during sexually transmitted acute resolving infection. J Virol 2005; 79: 15131-15141
37. Nainan OV, Lu L, Gao FX, Meeks E, Robertson BH, Margolis HS. Selective transmission of hepatitis C virus genotypes and quasispecies in humans and experimentally infected chimpanzees. J Gen Virol 2006; 87: 83-91
38. Rispeter K, Lu M, Behrens SE, Fumiko C, Yoshida T, Roggendorf M. Hepatitis C virus variability: sequence analysis of an isolate after 10 years of chronic infection. Virus Genes 2000; 21: 179-188
39. Smith DB, Simmonds P. Characteristics of nucleotide substitution in the hepatitis C virus genome: constraints on sequence change in coding regions at both ends of the genome. J Mol Evol 1997; 45: 238-246
40. Kimura M. Evolutionary rate at the molecular level. Nature 1968; 217: 624-626
41. Cochrane A, Searle B, Hardie A, Robertson R, Delahooke T, Cameron S, Tedder RS, Dusheiko GM, De Lamballerie X, Simmonds P. A genetic analysis of hepatitis C virus transmission between injection drug users. J Infect Dis 2002; 186: 1212-1221
42. Pybus OG, Charleston MA, Gupta S, Rambaut A, Holmes EC, Harvey PH. The epidemic behavior of the hepatitis C virus. Science 2001; 292: 2323-2325
43. de Oliveira T, Pybus OG, Rambaut A, Salemi M, Cassol S, Ciccozzi M, Rezza G, Gattinara GC, D'Arrigo R, Amicosante M, Perrin L, Colizzi V, Perno CF. Molecular epidemiology: HIV-1 and HCV sequences from Libyan outbreak. Nature 2006; 444: 836-837
44. Allain JP, Dong Y, Vandamme AM, Moulton V, Salemi M. Evolutionary rate and genetic drift of hepatitis C virus are not correlated with the host immune response: studies of infected donor-recipient clusters. J Virol 2000; 74: 2541-2549
45. Grenfell BT, Pybus OG, Cog JR, Wood JL, Daly JM, Mumford JA, Holmes EC. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 2004; 303: 327-332
46. Farci P, Shimoda A, Coiana A, Diaz G, Peddis G, Melpolder JC, Strazzera A, Chien DY, Munoz SJ, Balestrieri A, Purcell RH, Alter HJ. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 2000; 288: 339-344
47. 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. Early changes in hepatitis C viral quasispecies during interferon therapy predict the therapeutic outcome. Proc Natl Acad Sci USA 2002; 99: 3081-3086
48. Chambers TJ, Fan X, Droll DA, Hembrador E, Slater T, Nickells MW, Dustin LB, Dibisceglie AM. Quasispecies heterogeneity within the E1/E2 region as a pretreatment variable during pegylated interferon therapy of chronic hepatitis C virus infection. J Virol 2005; 79: 3071-3083
49. Kato N, Ootsuyama Y, Sekiya H, Ohkoshi S, Nakazawa T, Hijikata M, Shimotohno K. Genetic drift in hypervariable region 1 of the viral genome in persistent hepatitis C virus infection. J Virol 1994; 68: 4776-4784
50. Weiner AJ, Geysen HM, Christopherson C, Hall JE, Mason KA, Saracco G, Bonino F, Crawford K, Marion CD, Crawford KA. Evidence for immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants: potential role in chronic HCV infections. Proc Natl Acad Sci USA 1992; 89: 3468-3472
51. Booth JC, Kumar U, Webster D, Monjardino J, Thomas HC. Comparison of the rate of sequence variation in the hypervariable region of E2/NS1 region of hepatitis C virus in normal and hypogammaglobulinemic patients. Hepatology 1998; 27: 223-227
52. Christie JM, Chapel H, Chapman RW, Rosenberg WM. Immune selection and genetic sequence variation in core and envelope regions of hepatitis C virus. Hepatalogy 1999; 30: 1037-1044
53. Ray SC, Mao Q, Lanford RE, Bassett S, Laeyendecker O, Wang YM, Thomas DL. Hypervariable region 1 sequence stability during hepatitis C virus replication in chimpanzees. J Virol 2000; 74: 3058-3066
54. Logvinoff C, Major ME, Oldach D, Heyward S, Talal A, Balfe P, Feinstone SM, Alter H, Rice CM, McKeating JA. Neutralizing antibody response during acute and chronic hepatitis C virus infection. Proc Natl Acad Sci USA 2004; 101: 10149-10154
55. Drummer HE, Maerz A, Poumbourios P. Cell surface expression of functional hepatitis C virus E1 and E2 glycoproteins. FEBS Lett 2003; 546: 385-390
56. Bartosch B, Bukh J, Meunier JC, Granier C, Engle RE, Blackwelder WC, Emerson SU, Cosset FL, Purcell RH. In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc Natl Acad Sci USA 2003; 100: 14199-14204
57. von Hahn T, Yoon JC, Alter H, Rice CM, Rehermann B, Balfe P, McKeating JA. Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterology 2007; 132: 667-678
58. Weiner A, Erickson AL, Kansopon J, Crawford K, Muchmore E, Hughes AL, Houghton M, Walker CM. Persistent hepatitis C virus infection in a chimpanzee is associated with emergence of a cytotoxic T lymphocyte escape variant. Proc Natl Acad Sci USA 1995; 92: 2755-2759
59. Erickson AL, Kimura Y, Igarashi S, Eichelberger J, Houghton M, Sidney J, McKinney D, Sette A, Hughes AL, Walker CM. The outcome of hepatitis C virus infection is predicted by escape mutations in epitopes targeted by cytotoxic T lymphocytes. Immunity 2001; 15: 883-895
60. Chang KM, Rehermann B, McHutchison JG, Pasquinelli C, Southwood S, Sette A, Chisari FV. Immunological significance of cytotoxic T lymphocyte epitope variants in patients chronically infected by the hepatitis C virus. J Clin Invest 1997; 100: 2376-2385
61. Guglietta S, Garbuglia AR, Pacciani V, Scotta C, Perrone MP, Laurenti L, Spada E, Mele A, Capobianchi MR, Taliani G, Folgori A, Vitelli A, Ruggeri L, Nicosia A, Piccolella E, Del Porto P. Positive selection of cytotoxic T lymphocyte escape variants during acute hepatitis C virus infection. Eur J Immunol 2005; 35: 2627-2637
62. Cox AL, Mosbruger T, Mao Q, Liu Z, Wang XH, Yang HC, Sidney J, Sette A, Pardoll D, Thomas DL, Ray SC. Cellular immune selection with hepatitis C virus persistence in humans. J Exp Med 2005; 201: 1741-1752
63. Tester I, Smyk-Pearson S, Wang P, Wertheimer A, Yao E, Lewinsohn DM, Tavis JE, Rosen HR. Immune evasion versus recovery after acute hepatitis C virus infection from a shared source. J Exp Med 2005; 201: 1725-1731
64. Timm J, Lauer GM, Kavanagh DG, Sheridan I, Kim AY, Lucas M, Pillay T, Ouchi K, Reyor LL, Schulze zur Wiesch J, Gandhi RT, Chung RT, Bhardwaj N, Klenerman P, Walker BD, Allen TM. CD8 epitope escape and reversion in acute HCV infection. J Exp Med 2004; 200: 1593-1604
65. Ray SC, Fanning L, Wang XH, Netski DM, Kenny-Walsh E, Thomas DL. Divergent and convergent evolution after a common-source outbreak of hepatitis C virus. J Exp Med 2005; 201: 1753-1759
66. Moore CB, John M, James IR, Christiansen FT, Witt CS, Mallal SA. Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 2002; 296: 1439-1443
67. Gaudieri S, Rauch A, Park LP, Freitas E, Herrmann S, Jeffrey G, Cheng W, Pfafferott K, Naidoo K, Chapman R, Battegay M, Weber R, Telenti A, Furrer H, James I, Lucas M, Mallal SA. Evidence of viral adaptation to HLA class I-restricted immune pressure in chronic hepatitis C virus infection. J Virol 2006; 80: 11094-11104
68. Timm J, Li B, Daniels MG, Bhattacharya T, Reyor LL, Allgaier R, Kuntzen T, Fischer W, Nolan BE, Duncan J, Schulze Zur Wiesch J, Kim AY, Frahm N, Brander C, Chung RT, Lauer GM, Korber BT, Allen TM. Human leukocyte antigen-associated sequence polymorphisms in hepatitis C virus reveal reproducible immune responses and constraints on viral evolution. Hepatology 2007; 46: 339-349
69. Eckels DD, Zhou H, Bian TH, Wang H. Identification of antigenic escape variants in an immunodominant epitope of hepatitis C virus. Int Immunol 1999; 11: 577-583
70. Wang H, Eckels DD. Mutations in immunodominant T cell epitopes derived from the nonstructural 3 protein of hepatitis C virus have the potential for generating escape variants that may have important consequences for T cell recognition. J Immunol 1999; 162: 4177-4183
71. Puig M, Mihalik K, Tilton JC, Williams O, Merchlinsky M, Connors M, Feinstone SM, Major ME. CD4+ immune escape and subsequent T-cell failure following chimpanzee immunization against hepatitis C virus. Hepatology 2006; 44: 736-745
72. Gale M Jr, Foy EM. Evasion of intracellular host defence by hepatitis C virus. Nature 2005; 436: 939-945
73. Li K, Foy E, Ferreon JC, Nakamura M, Ferreon AC, Ikeda M, Ray SC, Gale M Jr, Lemon SM. Immune evasion by hepatitis C virus NS3/4A protease-mediated deavage of the Toll-like receptor 3 adaptor protein TRIF. Proc Natl Acad Sci USA 2005; 102: 2992-2997
74. Breiman A, Grandvaux N, Lin R, Ottone C, Akira S, Yoneyama M, Fujita T, Hiscott J, Meurs EF. Inhibition of RIG-I-dependent signaling to the interferon pathway during hepatitis C virus expression and restoration of signaling by IKKepsion. J Virol 2005; 79: 3969-3978
75. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005; 437: 1167-1172
76. Gale M Jr, Blakely CM, Kwieciszewski B, Tan SL, Dossett M, Tang NM, Korth MJ, Polyak SJ, Gretch DR, Katze MG. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol Cell Biol 1998; 18: 5208-5218
77. Feld JJ, Hoofnagle JH. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 2005; 436: 967-972
78. Chayama K, Tsubota A, Kobayashi M, Okamoto K, Hashimoto M, Miyano Y, Koike H, Kobayashi M, Koida I, Arase Y, Saitoh S, Suzuki Y, Murashima N, Ikeda K, Kumada H. Pretreatment virus load and multiple amino acid substitutions in the interferon sensitivity-determining region predict the outcome of interferon treatment in patients with chronic genotype 1b hepatitis C virus infection. Hepatology 1997; 25: 745-749
79. Pascu M, Martus P, Hohne M, Wiedenmann B, Hopf U, Schreier E, Berg T. Sustained virological response in hepatitis C virus type 1b infected patients is predicted by the number of mutations within the NS5A-ISDR: a meta-analysis focused on geographical differences. Gut 2004; 53: 1345-1351
80. Aus dem Siepen M, Oniangue-Ndza C, Wiese M, Ross S, Roggendorf M, Viazov S. Interferon-alpha and ribavirin resistance of Huh7 cells transfected with HCV subgenomic replicon. Virus Res 2007; 125: 109-113
81. Hofmann WP, Polta A, Herrmann E, Mihm U, Kronenberger B, Sonntag T, Lohmann V, Schonberger B, Zeuzem S, Sarrazin C. Mutagenic effect of ribavirin on hepatitis C nonstructural 5B quasispecies in vitro and during antiviral therapy. Gastroenterology 2007; 132: 921-930
82. Lutchman G, Danehower S, Song BC, Liang TJ, Hoofnagle JH, Thomson M, Ghany MG. Mutation rate of the hepatitis C virus NS5B in patients undergoing treatment with ribavirin monotherapy. Gastroenterology 2007; 132: 1757-1766
83. 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
84. Hinrichsen H, Benhamou Y, Wedemeyer H, Reiser M, Sentjens RE, Calleja JL, Forns X, Erhardt A, Cronlein J, Chaves RL, Yong CL, Nehmiz G, Steinmann GG. Short-term antiviral efficacy of BILN 2061, a hepatitis C virus serine protease inhibitor, in hepatitis C genotype 1 patients. Gastroenterology 2004; 127: 1347-1355
85. Reiser M, Hinrichsen H, Benhamou Y, Reesink HW, Wedemeyer H, Avendano C, Riba N, Yong CL, Nehmiz G, Steinmann GG. Antiviral efficacy of NS3-serine protease inhibitor BILN-2061 in patients with chronic genotype 2 and 3 hepatitis C. Hepatology 2005; 41: 832-835
86. Pawlotsky JM, Chevaliez S, McHutchison JG. The hepatitis C virus life cycle as a target for new antiviral therapies. Gastroenterology 2007; 132: 1979-1998
87. Lin C, Lin K, Luong YP, Rao BG, Wei YY, Brennan DL, Fulghum JR, Hsiao HM, Ma S, Maxwell JP, Cottrell KM, Perni RB, Gates CA, Kwong AD. In vitro resistance studies of hepatitis C virus serine protease inhibitors, VX-950 and BILN 2061: structural analysis indicates different resistance mechanisms. J Biol Chem 2004; 279: 17508-17514
88. Tong X, Chase R, Skelton A, Chen T, Wright-Minogue J, Malcolm BA. Identification and analysis of fitness of resistance mutations against the HCV protease inhibitor SCH 503034. Antiviral Res 2006; 70: 28-38
89. Sarrazin C, Kieffer TL, Bartels D, Hanzelka B, Muh U, Welker M, Wincheringer D, Zhou Y, Chu HM, Lin C, Weegink C, Reesink H, Zeuzem S, Kwong AD. Dynamic hepatitis C virus genotypic and phenotypic changes in patients treated with the protease inhibitor telaprevir. Gastroenterology 2007; 132: 1767-1777
90. Grambas S, Bennett MS, Hay AJ. Influence of amantadine resistance mutations on the pH regulatory function of the M2 protein of influenza A viruses. Virology 1992; 191: 541-549
91. Altfeld M, Allen TM. Hitting HIV where it hurts: an alternative approach to HIV vaccine design. Trends Immunol 2006; 27: 504-510