Clinical significance of hepatitis C virus genotypes and quasispecies

Seminars in Liver Disease

Volumn 20, Issue 1, 2000, Pages 103-126

  Farci, Patrizia ^a   Purcell, Robert H ^b  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Clinical implications; Genetic variability; Genotypes; Hepatitis C virus; Quasispecies

Indexed keywords

ARTICLE; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNE RESPONSE; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSMISSION;

DNA REPLICATION; GENOTYPE; HEPACIVIRUS; HEPATITIS C; HUMANS; SPECIES SPECIFICITY; VARIATION (GENETICS);

EID: 0033932002     PISSN: 02728087     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (239)

1. National Institutes of Health Consensus Development Conference Panel Statement: Management of hepatitis C. Hepatology 1997;26:2S-10S
2. Seeff LB. Natural history of viral hepatitis, type C. Semin Gastrointest Dis 1995;6:20-27
3. Di Bisceglie AM. Hepatitis C and hepatocellular carcinoma. Semin Liver Dis 1995;15:64-69
4. Detre KM, Belle SH, Lombardero M. Liver transplantation for chronic viral hepatitis. Viral Hepat Rev 1996;2:219-228
5. Alter MJ, Margolis HS, Krawczynski K, et al. The natural history of community-acquired hepatitis C in the United States. N Engl J Med 1992;327:1899-1902
6. Alter HJ. To C or not to C: These are the questions. Blood 1995; 85:1681-1695
7. Di Bisceglie AM, Goodman ZD, Ishask KG, et al. Long-term clinical and histopathological follow-up of chronic posttransfusion hepatitis. Hepatology 1991;14:969-974
8. Farci P, Alter HJ, Wong D, et al. Long-term study of hepatits C virus replication in non-A, non-B hepatitis. N Engl J Med 1991; 325:98-104
9. Seeff LB. Natural history of hepatitis C. Hepatology 1997;26: 21S-28S
10. Hoofnagle JH. Hepatitis C: The clinical spectrum of disease. Hepatology 1997;26:15S-20S
11. Seeff LB, Buskell-Bales Z, Wright EC, et al. Long-term mortalily after transfusion-associated non-A, non-B hepatitis. N Engl J Med 1992;327:1906-1911
12. Tong MJ, el-Farra NS, Reikes AR, Co RL. Clinical outcomes after transfusion-associated hepatitis C. N Engl J Med 1995;332: 1463-1466
13. Farci P, Alter HJ, Govindarajan S, et al. Lack of protective immunity against reinfection with hepatitis C virus. Science 1992;258:135-140
14. Prince AM, Brotman B, Huima T, et al. Immunity in hepatitis C infection. J Infect Dis 1992;165:438-443
15. Wyatt CA, Andrus L, Brotman B, et al. Immunity in chimpanzees chronically infected with hepatitis C virus: Role of minor quasispecies in reinfection. J Virol 1998;72:1725-1730
16. Lai ME, Mazzoleni AP, Argiolu F, et al. Hepatitis C virus in multiple episodes of acute hepatitis in polytransfused thalassemic children. Lancet 1994;343:388-390
17. Kao JH, Chen PJ, Lai MY, Chen DS. Superinfection of heterologous hepatitis C virus in a patient with chronic type C hepatitis. Gastroenterology 1992;105:583-587
18. Okamoto H, Mishiro S, Tokita H, et al. Superinfection of chimpanzees carrying hepatitis C virus of genotype II/1b with that of genotype III/2a or I/1a. Hepatology 1994;20:1131-1136
19. Kobayashi M, Tanaka E, Matsumoto A, et al. Antibody response to E2/NS1 hepatitis C virus protein in patients with acute hepatitis C. J Gastroenterol Hepatol 1997;12:73-76
20. Koziel MJ, Walker BD. Characteristics of the intrahepatic cytotoxic T lymphocyte response in chronic hepatitis C virus infection. Semin Immunopathol 1997;19:69-83
21. Chang K-M, Rehermann B, Chisari FV. Immunopathology of hepatitis C. Semin Immunopathol 1997;19:57-68
22. Shimizu YK, Feinstone SM, Kohara M, et al. Hepatitis C virus: Detection of intracellular virus particles by electron microscopy. Hepatology 1996;23:205-209
23. International Union of Microbiological Societies. Murphy FA, Fauquet CM, Bishop DHL, et al. eds. Virus Taxonomy, 7th ed. New York: Springer-Verlag, 1995, pp. 424-427
24. Houghton M. Hepatitis C virus. In: Fields BN, Knipe DM, Howley PM, Chanock RH, eds. Fields Virology, 3rd ed. Philadelphia: Lippincott-Raven, 1996, pp. 1035-1058
25. Tsukiyama-Kohara K, Kohara I, Nomoto A. Internal ribosome entry site within hepatitis C virus RNA. J Virol 1992;66: 1476-1483
26. Tanaka T, Kato N, Cho M, Shimotohno K. A novel sequence found at the 3′terminus of hepatitis C virus genome. Biochem Biophys Res Commum 1995;215:744-749
27. Choo Q-L, Richman KH, Han JH, et al. Genetic organization and diversity of the hepatitis C virus. Proc Natl Acad Sci USA 1991;88:2451-2455
28. Holland J, Spindler K, Horodyski F, et al. Rapid evolution of RNA genomes. Science 1982;215:1577-1585
29. Ogata N, Alter HJ, Miller RH, Purcell RH. Nucleotide sequence and mutation rate of the H strain of hepatitis C virus. Proc Natl Acad Sci USA 1991;88:3392-3396
30. Okamoto H, Kojima M, Okada S-I, et al. Genetic drift of hepatitis C virus during an 8.2-year infection in a chimpanzee: Variability and stability. Virology 1992;190:894-899
31. Holland J, Domingo E, De La Torre JC, Steinhauer DA. Mutation frequencies at defined single codon sites in vesicular stomatitis virus can be increased only slightly by chemical mutagenesis. J Virol 1990;64:3960-3962
32. Martell M, Esteban JL, Quer J, et al. Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: Quasispecies nature of HCV genome distribution. J Virol 1992;66:3225-3229
33. Nowak MA. Variability of HIV infections. J Theor Biol 1992; 155:1-20
34. Weiner AJ, Brauer MJ, Rosemblatt J, et al. Variable and hypervariable domains are found in the regions of HCV corresponding to the flavivirus envelope and NS1 proteins and the pestivirus envelope glycoproteins. Virology 1991;180:842-848
35. Hijikata M, Kato N, Ootsuyama Y, et al. Hypervariable regions in the putative glycoprotein of hepatitis C virus. Biochem Biophys Res Commun 1991;175:220-228
36. Okamoto H, Mishiro S. Genetic heterogeneity of hepatitis C virus. Intervirology 1994;43:68-76
37. Bukh J, Miller RH, Purcell RH. Genetic heterogeneity of hepatitis C virus: Quasispecies and genotypes. Semin Liver Dis 1995; 15:41-63
38. Simmonds P. Variability of hepatitis C virus. Hepatology 1995; 21:570-583
39. Chan S-W, McOmish F, Holmes EC, et al. Analysis of a new hepatitis C virus type and its phylogenetic relationship to existing variants. J Gen Virol 1992;73:1131-1141
40. Simmonds P, Holmes E C, Cha T-A, et al. Classification of hepatitis C virus into six major genotypes and a series of subtypes by phylogenetic analysis of the NS-5 region. Gen Virol 1993;74: 2391-2399
41. Maertens G, Stuyver L. Genotypes and genetic variation of hepatitis C virus. In: Harrison TJ, Zuckerman A, eds. The Molecular Medicine of Viral Hepatitis. Chichester, England: Medical Science Series, John Wiley & Sons Ltd; 1997, pp. 183-233
42. Forns X, Bukh J. Methods for determining the hepatitis C virus genotype. Viral Hepat Rev 1998;4:1-19
43. Tokita H, Okamoto H, Tsuda F, et al. Hepatitis C virus variants from Vietnam are classifiable into the seventh, eighth and ninth major genetic groups. Proc Natl Acad Sci USA 1994;91: 11022-11026
44. Tokita H, Okamoto H, Luengrojanakul P, et al. Hepatitis C virus variants from Thailand classifiable into five novel genotypes in the sixth (6h), seventh (7c, 7d) and ninth (9b, 9c) major genetic groups. J Gen Virol 1995;76 :2329-2335
45. Mizokami M, Gojobori T, Ohba K-I, et al. Hepatitis C virus types 7, 8 and 9 should be classified as type 6 subtypes. J Hepatol 1996;24:622-624
46. Simmonds P, Mellor J, Sakuldamrongpanich T, et al. Evolutionary analysis of variants of hepatitis C virus found in South-East Asia: Comparison with classifications based upon sequence similarity. J Gen Virol 1996;77:3 013-3024
47. Bukh J, Purcell RH, Miller RH. At least 12 genotypes of hepatitis C virus predicted by sequence analysis of the putative E1 gene of isolates collected worldwide. Proc Natl Acad Sci USA 1993;90:8234-8238
48. Simmonds P, Holmes EC, Cha T-A, et al. Classification of hepatitis C virus into six major genotypes and a series of subtypes by phylogenetic analysis of the NS-5 region. J Gen Virol 1993;74: 2391-2399
49. Purcell RH. The hepatitis C virus: Overview. Hepatology 1997; 26:11S-14S
50. Mondelli MU. Clinical Implications of Viral Genotypes. International Consensus Conference on Hepatitis C. European Association for the Study of the Liver, Paris, 1999
51. Okamoto H, Sugiyama Y, Okada S, et al. Typing hepatitis C virus by polymerase chain reaction with type-specific primers: Application to clinical surveys and tracing infectious sources. J Gen Virol 1992;73:673-679
52. Ichimura H, Tamura I, Kurimura O, et al. Hepatitis C virus genotypes, reactivity to recombinant immunoblot assay 2 antigens and liver disease. J Med Virol 1994;43:212-215
53. Hadiwandowo S, Tsuda F, Okamoto H, et al. Hepatitis B virus subtypes and hepatitis C virus genotypes in patients with chronic liver disease or on maintenance hemodialysis in Indonesia. J Med Virol 1994;43:182-186
54. Bréchot C. Hepatitis C virus genetic variability: clinical implications. Am J Gastroenterol 1994;89:41S-47S
55. Silini EM, Bono F, Cividini A, et al. Differential distribution of hepatitis C virus genotypes in patients with and without liver function abnormalities. Hepatology 1995;21:285-290
56. Puoti C, Magrini A, Stati T, et al. Clinical, histological, and virological features of hepatitis C virus carriers with persistently normal or abnormal alanine transaminase levels. Hepatology 1997;26:1393-1398
57. Guadagnino V, Stroffolini T, Rapicetta M, et al. Prevalence, risk factors, and genotype distribution of hepatitis C virus infection in the general population: A community-based survey in southern Italy. Hepatology 1997;26:1006-1011
58. Silini EM, Mondelli MU. Significance of hepatitis C virus genotypes. Viral Hepat Rev 1995;1:111-120
59. Jarvis LM, Ludlam CA, Ellender JA, et al. Investigation of the relative infectivity and pathogenicity of different hepatitis C virus genotypes in hemophiliacs. Blood 1996;87:3007-3011
60. Smith DB, Davidson F, Yap P-L, et al. Levels of hepatitis C virus in blood donors infected with different virus genotypes. J Infect Dis 1996;173:727-730
61. Lau JYN, Davis GL, Prescott LE, et al. Distribution of hepatitis C virus genotypes determined by line probe assay in patients with chronic hepatitis C seen at tertiary referral centers in the United States. Ann Intern Med 1996;24:868-876
62. Gane EJ, Naoumov NV, Quian K-P, et al. A longitudinal analysis of hepatitis C virus replication following liver transplantation. Gastroenterology 1996;110:167-177
63. Pozzato G, Moretti M, Franzin F, et al. Severity of liver disease with different hepatitis C viral clones. Lancet 1991;338: 509
64. Pozzato G, Kaneko S, Moretti M, et al. Different genotypes of hepatitis C virus are associated with different severity of chronic liver disease. J Med Virol 1994;43:291-296
65. Qu D, Li J-S, Vitvitski L, et al. Hepatitis C virus genotypes in France: Comparison of clinical features of patients infected with HCV type I and type II. J Hepatol 1994;21:70-75
66. Pistello M, Maggi F, Vatteroni L, et al. Prevalence of hepatitis C virus genotypes in Italy. J Clin Microbiol 1994;32:232-234
67. Zein NN, Poterucha JJ, Gross JB Jr, et al. Increased risk of hepatocellular carcinoma in patients infected with hepatitis C genotype 1b. Am J Gastroenterol 1996;91:2560-2562
68. Cathomas G, McGandy CE, Terracciano LM, et al. Detection and typing of hepatitis C RNA in liver biopsies and its relation to histopathology. Virchows Arch 1996;429:353-358
69. Booth JC, Doster GR, Levine T, et al. The relationship of histology to genotype in chronic HCV infection. Liver 1997;17: 144-151
70. Kobayashi M, Tanaka E, Sodeyama T, et al. The natural course of chronic hepatitis C: A comparison between patients with genotypes 1 and 2 hepatitis C viruses. Hepatology 1996;23:695-699
71. Mita E, Hayashi N, Kanazawa Y, et al. Hepatitis C virus genotype and RNA titer in the progression of type C chronic liver disease. J Hepatol 1994;21:468-473
72. Kobayashi M, Kumada H, Chayama K, et al. Prevalence of HCV genotype among patients with chronic liver diseases in the Tokyo metropolitan area. J Gastroenterol 1994;29-583-587
73. Yamada M, Kakumu S, Yoshioka K, et al. Hepatitis C virus genotypes are not responsible for development of serious liver disease. Dig Dis Sci 1994;39:234-239
74. Naoumov NV, Chokshi S, Metivier E, et al. Hepatitis C virus infection in the development of hepatocelluler carcinoma in cirrhosis. J Hepatol 1997;27:331-336
75. Guido M, Rugge M, Thung SN, et al. Hepatitis C virus serotypes and liver pathology. Liver 1996;16:353-357
76. Ravaggi A, Rossini A, Mazza C, et al. Hepatitis C virus genotypes in northern Italy: Clinical and virological features. J Clin Microbiol 1996;34:2822-2825
77. Lee DS, Sung YC, Whang YS. Distribution of HCV genotypes among blood donors, patients with chronic liver disease, hepatocellular carcinoma, and patients on maintenance hemodialysis in Korea. J Med Virol 1996;49:55-60
78. Mangia A, Cascavilla I, Lezzi G, et al. HCV genotypes in patients with liver disease of different stages and severity. J Hepatol 1997;26:1173-1178
79. Kleter B, Brouwer JT, Nevens F, et al. Hepatitis C virus genotypes: Epidemiological and clinical associations. Benelux Study Group on Treatment of Chronic Hepatitis C. Liver 1998;18: 32-38
80. Nousbaum J-B, Pol S, Nalpas B, et al. Hepatitis C virus type 1b (II) infection in France and Italy. Ann Intern Med 1995;122: 161-168
81. Lopez-Labrador FX, Ampurdanes S, Forns X, et al. Hepatitis C virus (HCV) genotypes in Spanish patients with HCV infection: Relationship between HCV genotype 1b, cirrhosis and hepatocellular carcinoma. J Hepatol 1997;27:959-965
82. Bruno S, Silini E, Crosignani A, et al. Hepatitis C virus genotypes and risk of hepatocellular carcinoma in cirrhosis: A prospective study. Hepatology 1997;25:754-758
83. Benvegnù L, Pontisso P, Cavalletto D, et al. Lack of correlation between hepatitis C virus genotypes and clinical course of hepatitis C virus-related cirrhosis. Hepatology 1997;25:211-215
84. Serfaty L, Aumaitre H, Chazouilleres O, et al. Determinants of outcome of compensated hepatitis C virus-related cirrhosis. Hepatology 1998;27:1435-1440
85. Silini E, Bottelli R, Asti M, et al. Hepatitis C virus genotypes and risk of hepatocellular carcinoma in cirrhosis: A case control study. Gastroenterology 1996;111:199-205
86. Hatzakis A, Katsoulidou A, Kaklamani E, et al. Hepatitis C virus 1b is the dominant genotype in HCV-related carcinogenesis: A case-control study. Int J Cancer 1996;68:51-53
87. Donato F, Tagger A, Chiesa R, et al. Hepatitis B and C virus infection, alcohol drinking and hepatocellular carcinoma; A case-control study in Italy. Hepatology 1997;26:579-584
88. Féray C, Gigou M, Samuel D, et al. Influence of the genotypes of hepatitis C virus on the severity of recurrent liver disease after liver transplatation. Gastroenterology 1995;108:1088-1096
89. Gane EJ, Portmann BC, Naoumov NV, et al. Long-term outcome of hepatitis C infection after liver transplantation. N Engl J Med 1996;334:815-820
90. Caccamo L, Gridelli B, Sampietro M, et al. Hepatitis C virus genotypes and reinfection of the graft during long-term follow-up in 35 liver transplant recipients. Transplant Int 1996;9:204S-209S
91. Belli LS, Silini E, Alberti A, et al. Hepatitis C virus genotypes, hepatitis, and hepatitis C virus recurrence after liver transplantation. Liver Transplant Surg 1996;2:200-205
92. Gordon FD, Poterucha JJ, Germer J, et al. Relationship between hepatitis C genotype and severity of recurrent hepatitis C after liver transplantation. Trasplantation 1997;63:1419-1423
93. Zhou S, Terrault NA, Ferrell L, et al. Severity of liver disease in liver transplantation recipients with hepatitis C virus infection: Relationship to genotype and level of viremia. Hepatology 1996; 24:1041-1046
94. Vargas HE, Laskus T, Wang LF, et al. The influence of hepatitis C virus genotypes on the outcome of liver transplantation. Liver Transplant Surg 1998;4:22-27
95. Laskus T, Wanf LF, Rakela J, et al. Dynamic behavior of hepatitis C virus in chronically infected patients receiving liver graft from infected donors. Virology 1996;220:171-176
96. Poynard T, Bedossa P, Opolon P, et al. Natural history of liver fibrosis progression in patients with chronic hepatitis C. Lancet 1997;349:825-832
97. Cacciola I, Pollicino T, Squadrito G, et al. Occult hepatitis B virus infection in patients with chronic hepatitis C liver disease. N Engl J Med 1999;341:22-26
98. McHutchinson JG, Gordon ST, Schiff ER, et al. Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. N Engl J Med 1998;339:1485-1492
99. Davis GL, Mur RE, Rustgi V, et al. Interferon alfa-2b alone or in combination with ribavirin for the treatment of relapse of chronic hepatitis C. N Engl J Med 1998;339:1493-1499
100. Davis GL, Lau JYN. Factors predictive of a beneficial response to therapy of hepatitis C. Hepatology 1997;26:122S-127S
101. Taylor DR, Shi ST, Romano PR, et al. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 1999;285:107-110
102. Eigen M. Self organization of matter and the evolution of biological macromolecules. Naturwissenschaften 1972;58:465:523
103. Eigen M, Schuster P. The Hypercycle. A Principle of Natural Self-Organization. Berlin: Springer, 1979
104. Eigen M, Biebricher CK. Sequence space and quasispecies distribution. In: Domingo E, Holland JJ, Ahlquist P, eds. RNA Genetics. Boca Raton, FL: CRC Press, 1988, pp. 211-245
105. Domingo E, Holland JJ. High error rates, population equilibrium and evolution of RNA replication systems. In: Domingo E, Holland JJ, Ahlquist P, eds. RNA Genetics, Vol 3. Boca Raton, FL: CRC, 1988, pp 3-36
106. Holland JJ, De La Torre JC, Steinhauer DA. RNA virus populations as quasispecies. Curr Top Microbiol Immunol 1992; 176:1-20
107. Domingo E. Biological significance of viral quasispecies. J Viral Hepat 1996;2:2 47-261
108. Steinhauer DA, Holland JJ. Rapid evolution of RNA viruses. Annu Rev Microbiol 1987;41:409-433
109. Domingo E, Sabo D, Taniguchi T, Weissmann C. Nucleotide sequence heterogeneity of an RNA phage population. Cell 1978; 13:735-744
110. Branch AD, Benenfeld BJ, Paul CP, et al. Analysis of ultraviolet-induced RNA-RNA cross-links: A means for probing RNA structure-function relationships. Methods Enzymol 1989;180:418-442
111. Gretch DR, Polyak SJ. The Quasispecies Nature of Hepatitis C Virus: Research Methods and Biological Implications. Hepatitis C Virus: Genetic Heterogeneity and Viral Load. GEMHEP. Paris: John Libbey Eurotext, 1997, pp. 57-69
112. Gómez J, Martell M, Quer B, et al. Hepatitis C viral quasispecies. J Viral Hepat 1999;6:3-16
113. Orita M, Iwahana H, Kanazawa H, et al. Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proc Natl Acad Sci USA 1989; 86:2766-2770
114. Moribe T, Hayashi N, Kanazawa Y, et al. Hepatitis C viral complexity detected by single-strand conformation polymorphisms and response to interferon therapy. Gastroenterology 1995;108:789-795
115. Lu M, Funsch B, Wiese M, Roggendorf M. Analysis of hepatitis C virus quasispecies populations by temperature gradient gel electrophoresis. J Gen Virol 1995;76:881-887
116. Wilson JJ, Polyak SJ, Day TD, Gretch DR. Characterization of simple and complex hepatitis C virus quasispecies by heteroduplex gel shift analysis: Correlation with nucleotide sequencing. J Gen Virol 1995;76:1763-1771
117. Forns X, Purcell RH, Bukh J. Quasispecies in viral persistence and pathogenesis of hepatitis C virus. Trends Microbiol 1999;7: 402-410
118. Higashi Y, Kakumu S, Yoshioka K, et al. Dynamics of genome change in the E2/NS1 region of hepatitis C virus in vivo. Virology 1993;197:659-668
119. Kato N, Ootsuyama Y, Tanaka T, et al. Marked sequence diversity in the putative envelope proteins of hepatitis C viruses. Virus Res 1992;22:107-123
120. Murakawa K, Esumi M, Kato T, et al. Heterogeneity within the nonstructural protein 5-encoding region of hepatitis C viruses from a single patient. Gene 1992;117:229-232
121. Tanaka T, Kato N, Nakagawa M, et al. Molecular cloning of hepatitis C virus genome from a single Japanese carrier: Sequence variation within the same individual and among infected individuals. Virus Res 1992;23:39-53
122. Yanagy M, Purcell RH, Emerson SU, Bukh J. Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into the liver of a chimpanzee. Proc Natl Acad Sci USA 1997;94:8738-8743
123. Farci P, Alter HJ, Wong DC, et al. Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc Natl Acad Sci USA 1994;91:7792-7796
124. Yanagi M, St. Claire M, Shapiro M, et al. Transcripts of a chimeric cDNA clone of hepatitis C virus genotype 1b are infectious in vivo. Virology 1998;244:161-172
125. Farci P, Shimoda A, Wong D, et al. Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proc Natl Acad Sci USA 1996;93:15394-15399
126. Koziol DE, Holland PV, Ailing DW, et al. Antibody to hepatitis B core antigen as a paradoxical marker for non-A, non-B hepatitis agents in donated blood. Ann Intern Med 1986;104:488-495
127. Domingo E. RNA virus evolution and the control of viral disease. Progr Drug Res 1989;33:93-133
128. Domingo E, Martinez-Salas E, Sobrino F, et al. The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance - a review. Gene 1985;40:1-8
129. Choo QL, Kuo G, Ralston R, et al. Vaccination of chimpanzees against infection by the hepatitis C virus. Proc Natl Acad Sci USA 1994;91:1294-1298
130. Houghton M, Choo Q-L, Chien D, et al. Development of an HCV vaccine. In Rizzetto M, Purcell RH, Gerin JL, Verme G, eds. Viral Hepatitis and Liver Disease. Turin: Minerva Meolia 1997; pp. 656-659
131. Shimizu YK, Iwamoto A, Hijikata M, et al. Evidence for in vitro replication of hepatitis C virus genome in a human T-cell line. Proc Natl Acad Sci USA 1992;89:5477-5481
132. Shimizu YK, Igarashi H, Kiyohara T, et al. A Hyperimmune serum against a synthetic peptide corresponding to the hypervariable region I of hepatitis C virus can prevent viral infection in cell cultures. Virology 1996;223:409-412
133. Shimizu YK, Hijikata M, Iwamoto A, et al. Neutralizing antibodies against hepatitis C virus and the emergence of neutralization escape mutants. J Virol 1994;68:1494-1500
134. Zibert A, Schreier E, Roggendorf M. Antibodies in human sera specific to hypervariable region 1 of hepatitis C virus can block viral attachment. Virology 1994;208:653-661
135. Pileri P, Uematsu Y, Campagnoli S, et al. Binding of hepatitis C virus to CD81. Science 1998;282:938-941
136. Rosa D, Campagnoli S, Moretto C, et al. A quantitative test to estimate neutralizing antibodies to hepatitis C virus: Cytofluorometric assessment of envelope glycoprotein E2 binding to target cells. Proc Natl Acad Sci USA 1996;93:1759-1763
137. Weiner AJ, Geysen HM, Christopherson C, et al. Evidence for immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants: Potential role in chronic HCV infection. Proc Natl Acad Sci USA 1992;89:3468-3472
138. Kato N, Ootsuyama Y, Sekiya H, et al. Genetic drift in hypervariable region 1 of the viral genome in persistent hepatitis C virus infection. J Virol 1994;68:4776-4784
139. Kumar U, Brown J, Monjardino J, Thomas HC. Sequence variation in the large envelope glycoprotein (E2/NS1) of hepatitis C virus during chronic infection. J Infect Dis 1993;167: 726-730
140. Kurosaki M, Enomoto N, Marumo F, Sato C. Rapid sequence variation of the hypervariable region of hepatitis C virus during the course of chronic infection. Hepatology 1993;18:1293-1299
141. Sakamoto N, Enomoto N, Kurosaki M, et al. Sequential change of the hypervariable region of the hepatitis C virus genome in acute infection. J Med Virol 1994;42:103-108
142. Kato N, Sekiya H, Ootsuyama Y, et al. Humoral immune response to hypervariable region 1 of the putative envelope glycoprotein (gp70) of hepatitis C virus. J Virol 1993;67:3923-3930
143. Lesniewski RR, Boardway KM, Casey JM, et al. Hypervariable 5′-terminus of hepatitis C virus E2/NS1 encodes antigenically distinct variants. J Med Virol 1993;40:150-156
144. Scarselli E, Cerino A, Esposito G, et al. Occurrence of antibodies reactive with more than one variant of the putative envelope glycoprotein (E2; gp70) hypervariable region 1 in hepatitis C viremic patients. J Virol 1995;69:4407-4412
145. Taniguchi S, Okamoto H, Sakamoto M, et al. A structurally flexible and antigenically variable N-terminal domain of the hepatitis C virus (E2/NS1) protein: Implication for an escape from antibody. Virology 1993;195:297-301
146. van Doorn LJ, Capriles I, Maertens G, et al. Sequence evolution of the hypervariable region in the putative envelope region E2/NS1 of hepatitis C virus is correlated with specific humoral immune response. J Virol 1995;69:773-778
147. Kumar U, Monjardino J, Thomas HC. Hypervariable region of hepatitis C virus envelope glycoprotein (E2/NS1) in an agammaglobulinemic patient. Gastroenterology 1994;106:1072-1075
148. Zibert A, Meisel H, Kraas W, et al. Early antibody response against hypervariable region 1 is associated with acute self-limiting infectioms of hepatitis C virus. Hepatology 1997;25: 1245-1249
149. Allander T, Beyene A, Jacobson SH, et al. Patients infected with the same hepatitis C virus strain display different kinetics of the isolate-specific antibody response. J Infect Dis 1997;175:26-31
150. Zibert A, Kraas W, Meisel H, et al. Epitope mapping of antibodies directed against hypervariable region 1 in acute self-limiting and chronic infections due to hepatitis C virus. J Virol 1997;71: 4123-4127
151. Mondelli MU, Cerino A, Lisa A, et al. Antibody responses to hepatitis C virus hypervariable region 1: Evidence for cross-reactivity and immune-mediated sequence variation. Hepatology 1999;30:537-545
152. McAllister J, Casino C, Davidson F, et al. Long-term evolution of the hypervariable region of hepatitis C virus in a common-source-infected cohort. J Virol 1998;72:4893-4905
153. Kolykhalov AA, Agapov EV, Blight K, et al. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 1997;277:570-574
154. Major ME, Mihalik K, Fernandez J, et al. Long-term follow-up of chimpanzees inoculated with the first infectious clone for hepatitis C virus. J Virol 1999;73:3317-3325
155. Bukh J, Yanagi M, Emerson SU, Purcell RH. Course of infection and evolution of monoclonal hepatitis C virus (HCV) strain H77 in chimpanzees transfected with RNA transcripts from an infectious cDNA clone. Hepatology 1998;28:319A
156. Hong Z, Beaudet-Miller M, Lanford RE, et al. Generation of transmissible hepatitis C virions from a molecular clone in chimpanzees. Virology 1999;256:36-44
157. Forns X, Emerson SU, Purcell RH, Bukh J. Deletion mutant of hepatitis C virus (HCV) molecular infectious clone lacking the hypervariable region 1 (HVR1) is viable but attenuated in vivo. Hepatology 1999;30:422A
158. Chisari FV. Im munobiology and pathogenesis of viral hepatitis. In: Rizzetto M, Purcell RH, Gerin JI, Verme G, eds. Viral Hepatitis and Liver Disease. Turin: Minerva Medica, 1997, pp. 405-415
159. Botarelli P, Brunetto MR, Minutello MA, et al. T-lymphocyte response to hepatitis C virus in different clinical courses of infection. Gastroenterology 1993;104:580-587.
160. Missale G, Bertoni R, Lamonaca V, et al. Different clinical behaviors of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response. J Clin Invest 1996;98:706-714
161. Diepolder HM, Zachoval R, Hoffmann RM, et al. Possible mechanism involving T-lymphocyte response to non-structural protein 3 in viral clearance in acute hepatitis C virus infection. Lancet 1995;346:1006-1007
162. Erickson AL, Houghton M, Choo QL, et al. Hepatitis C virus-specific CTL responses in the liver of chimpanzees with acute and chronic hepatitis C. J Immunol 1993;151:4189-4199
163. Cooper S, Erickson AL, Adams EJ, et al. Analysis of a successful immune response against hepatitis C virus. Immunity 1999;10:439-449
164. Thimme R, La Jolla CA, Bukh J, et al. HCV persists despite a multispecific peripheral and intrahepatic T cell response in acutely infected chimpanzees. Hepatology 1999;30:422A
165. Weiner A, Erickson AL, Kansopon J, et al. 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
166. Chang K-M, Rehermann B, McHutchison JG, et al. Immunological significance of cytotoxic T lymphocyte epitope variants in patients chronically infected by the hepatitis C virus. J Clin Invest 1997;100:2376-2385
167. Kaneko T, Moriyama T, Udaka K, et al. Impaired induction of cytotoxic T lymphocytes by antagonism of a weak agonist borne by a variant hepatitis C virus epitope. Eur J Immunol 1997;27: 1782-1787
168. 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
169. Tsai S-L, Chen Y-M, Chen M-H, et al. Hepatitis C virus variants circumventing cytotoxic T-lymphocyte activity as a mechanism of chronicity. Gastroenterology 1998;115:954-966
170. Farci P, Shirmoda A, Colana A, et al. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 2000;288:339-344
171. Farci P, Alter HJ, Shimoda A, et al. Hepatitis C virus-associated fulminant hepatic failure. N Engl J Med 1996;335:631-634
172. Farci P, Munoz SJ, Shimoda A, et al. Experimental transmission of hepatitis C virus-associated fulminant hepatitis to a chimpanzee. J Infect Dis 1999;179:1007-1011
173. Manzin A, Solforosi L, Petrelli E, et al. Evolution of hypervariable region 1 of hepatitis C virus in primary infection. J Virol 1998;72:6271-6276
174. Ray SC, Wang Y-M, Laeyendecker O, et al. Acute hepatitis C virus structural gene sequences as predictors of persistent viremia: Hypervariable region 1 as a decoy. J Virol 1999;73: 2938-2946
175. Honda M, Kaneko S, Sakai A, et al. Degree of diversity of hepatitis C virus quasispecies and progression of liver disease. Hepatology 1994;20:1144-1151
176. Naito M, Hayashi N, Moribe T, et al. Hepatitis C viral quasispecies in hepatitis C virus carriers with normal liver enzymes and patients with type C chronic liver disease. Hepatology 1995; 22:407-412
177. Koizumik, Enomoto N, Kurosaki M, et al. Diversity of quasispecies in various disease stages of chronic hepatitis C virus infection and its significance in interferon treatment. Hepatology 1995;22:30-35
178. González-Peralta RP, Quian K, She JY, et al. Clinical implications of viral quasispecies heterogeneity in chronic hepatitis C. J Med Virol 1996;49:242-247
179. Kao JH, Chen PJ, Lai MY, et al. Quasispecies of hepatitis C virus and genetic drift of the hypervariable region in chronic type C hepatitis. J Infect Dis 1995;172:261-264
180. Yuki N, Hayashi N, Moribe T, et al. Relation of disease activity during chronic hepatitis C infection to complexity of hypervariable region 1 quasispecies. Hepatology 1997;25: 439-444
181. Toyoda H, Fukuda Y, Koyama Y, et al. Nucleotide sequence diversity of hypervariable region 1 of hepatitis C virus in Japanese hemophiliacs with chronic hepatitis C and patients with chronic posttransfusion hepatitis C. Blood 1996;88:1488-1493
182. Sherman KE, Rouster SD, Mendenhall C, Thee D. Hepatitis cRNA quasispecies complexity in patients with alcoholic liver disease. Hepatology 1999;30:265-270
183. Martell M, Esteban JI, Quer J, et al. Dynamic behavior of hepatitis C virus quasispecies in patients undergoing orthotopic liver transplantation. J Virol 1994;68:3425-3436
184. Gretch DR, Polyak SJ, Wilson JJ, et al. Tracking hepatitis C virus quasispecies major and minor variants in symptomatic and asymptomatic liver transplant recipients. J Virol 1996;70: 7622-7631
185. Sullivan DG, Wilson JJ, Carithers RL Jr, et al. Multigene tracking of hepatitis C virus quasispecies after liver transplantation: correlation of genetic diversification in the envelope region with asymptomatic or mild disease patterns. J Virol 1998;72: 10036-10043
186. Lawal Z, Petrik J, Wong VS, et al. Hepatitis C virus genomic variability in untreated and immunosuppressed patients. Virology 1997;228:107-111
187. Ni Y-H, Chang M-H, Chen P-J, et al. Decreased diversity of hepatitis C virus quasispecies during bone marrow transplantation. J Med Virol 1999;58:132-138
188. Sherman KE, Andreatta C, O'Brien J, et al. Hepatitis C in human immunodeficiency virus-coinfected patients: Increased variability in the hypervariable envelope coding domain. Hepatology 1996;23:688-694
189. Toyoda H, Fukuda Y, Koyama Y, et al. Effect of immunosuppression on composition of quasispecies population of hepatitis C virus in patients with chronic hepatitis C coinfected with human immunodeficiency virus. J Hepatol 1997;26:975-982
190. Odeberg J, Yun Z, Sönnerborg A, et al. Variation of hepatitis C virus hypervariable region 1 in immunocompromised patients. J Infect Dis 1997;175:938-943
191. Booth JCL, Kumar U, Webster D, et al. 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
192. Laskus T, Radkowski M, Wang L-F, et al. Hepatitis C virus quasispecies in patients infected with HIV-1: Correlation with extrahepatic viral replication. Virology 1998;248:164-171
193. Sakamoto N, Enomoto N, Kurosaki M, et al. Comparison of the hypervariable region of hepatitis C virus genomes in plasma and liver. J Med Virol 1995;46:7-11
194. Fuji K, Hino K, Okazaki M, et al. Differences in hypervariable region 1 quasispecies of hepatitis C virus between human serum and peripheral blood mononuclear cells. Biochem Biophys Res Commun 1996;225:771-776
195. Cabot B, Esteban JI, Martell M, et al. Structure of replicating hepatitis C virus (HCV) quasispecies in the liver may not be reflected by analysis of circulating HCV virions. Virol 1997;71: 1732-1734
196. Shimizu YK, Igarashi H, Kanematu T, et al. Sequence analysis of the hepatitis C virus genome recovered from serum, liver, and peripheral blood mononuclear cells of infected chimpanzees. J Virol 1997;71:5769-5773
197. Maggi F, Fornai C, Vatteroni ML, et al. Differences in hepatitis C virus quasispecies composition between liver, peripheral blood mononuclear cells and plasma. J Gen Virol 1997;78:1521-1525
198. Navas S, Martin J, Quiroga JA, et al. Genetic diversity and tissue compartmentalization of the hepatitis C virus genome in blood mononuclear cells, liver, and serum from chronic hepatitis C patients. J Virol 1998;72:1640-1646
199. Maggi F, Fornai C, Morrica A, et al. Divergent evolution of hepatitis C virus in liver and peripheral blood mononuclear cells of infected patients. J Med Virol 1999;57:57-63
200. Okuda M, Hino K, Korenaga M, et al. Differences in hypervariable region 1 quasispecies of hepatitis C virus in human serum, peripheral blood mononuclear cells, and liver. Hepatology 1999;29:217-222
201. Fan X, Solomon H, Poulos JE, et al. Comparison of genetic heterogeneity of hepatitis C viral RNA in liver tissue and serum Am J Gastroenterol 1999;94:1347-1354
202. Jang SJ, Wang L-F, Radkowski M, et al. Differences between hepatitis C virus 5′untranslated region quasispecies in serum and liver. J Gen Virol 1999;80:711-716
203. Sakai A, Kaneko S, Masao H, et al. Quasispecies of hepatitis C virus in serum and in three different parts of the liver of patients with chronic hepatitis. Hepatology 1999;30:556-561
204. Kurosaki M, Enomoto N , Sakamoto N, et al. Detection and analysis of replication hepatitis C virus RNA in hepatocellular carcinoma tissues. J Hepatol 1995;22:527-535
205. Horie C, Iwahana H, Horie T, et al. Detection of different quasispecies of hepatitis C virus core region in cancerous and non-cancerous lesions. Biochem Biophys Res Commun 1996;26: 674-681
206. De Mitri MS, Mele L, Chen CH, et al. Comparison of serum and liver hepatitis C virus quasispecies in HCV-related hepatocellular carcinoma. J Hepatol 1998;29:887-892
207. Weiner AJ, Thaler MM, Crawford K, et al. A unique, predominant hepatitis C virus variant found in an infant born to a mother with multiple variants. J Virol 1993;67:4365-4368
208. Kudo T, Yanase Y, Ohshiro M, et al. Analysis of mother-to-infant transmission of hepatitis C virus: Quasispecies nature and buoyant densities of maternal virus populations. J Med Virol 1997;51:225-230
209. Sugitani M, Shikata T. Comparison of amino acid sequences in hypervariable region-1 of hepatitis C virus clones between human inocula and the infected chimpanzee sera. Virus Res 1998; 56:177-182.
210. Hijikata M, Mizuno K, Rikihisa T, et al. Selective transmission of hepatitis C virus in vivo and in vitro. Arch Virol 1995; 140:1623-1628
211. Kojima M, Osuga T, Tsuda F, et al. Influence of antibodies to the hypervariable region of E2/NS1 glycoprotein on the selective replication of hepatitis C virus in chimpanzees. Virology 1994,204:665-672
212. Fried MW, Hoofnagle JH. Therapy of hepatitis C. Semin Liver Dis 1995;15:82-91
213. Okada S, Akahane Y, Suzuki H, et al. The degree of variability in the amino terminal region of the E2/NS1 protein of hepatitis C virus correlates with responsiveness to interferon therapy in viremic patients. Hepatology 1992;16:619-624
214. Kanazawa Y, Hayashi N, Mita E, et al. Influence of viral quasispecies on effectiveness of interferon therapy in chronic hepatitis C patients. Hepatology 1994;20:1121-1130
215. Mizokami M, Lau JYN, Suzuki K, et al. Differential sensitivity of hepatitis C virus quasispecies to interferon-therapy. J Hepatol 1994;21:884-886
216. Yeh BI, Han KH, Oh SH, et al. Nucleotide sequence variation in the hypervariable region of the hepatitis C virus in the sera of chronic hepatitis C patients undergoing controlled interferon-therapy. J Med Virol 1996;49:95-102
217. González-Peralta RP, Qian K, She JY, et al. Clinical implications of viral quasispecies heterogeneity in chronic hepatitis C. J Med Virol 1996;49:242-247
218. Toyoda H, Kumada T, Nakano S, et al. Quasispecies nature of hepatitis C virus and response to alpha interferon: Significance as a predictor of direct response to interferon. J Hepatol 1997; 26:6-13
219. Le Guen B, Squadrito G, Nalpas B, et al. Hepatitis C virus genome complexity correlates with response to interferon therapy: A study in French patients with chronic hepatitis C. Hepatology 1997;25:1250-1254
220. Pawlotsky JM, Pellerin M, Bouvier M, et al. Genetic complexity of the hypervariable region 1 (HVR1) of hepatitis C virus (HCV): Influence on the characteristics of the infection and responses to interferon alfa therapy in patients with chronic hepatitis C. J Med Virol 1998;54:256-264
221. Hagiwara H, Hayashi N, Kasahara A, et al. Treatment with recombinant interferon-alpha 2a for patients with chronic hepatitis C: Predictive factors for biochemical and virologic response. Osaka Liver disease Study Group. Scand J Gastroenterol 1996; 31:1021-1026
222. Shindo M, Hamada K, Koya S, et al. The clinical significance of changes in genetic heterogeneity of the hypervariable region 1 in chronic hepatitis C with interferon therapy. Hepatology 1996; 24:1018-1023
223. Polyak SJ, Faulkner G, Carithers RL Jr, et al. Assessment of hepatitis C virus quasispecies heterogeneity by gel shift analysis: correlation with response to interferon therapy. J Infect Dis 1997;175:1101-1107
224. Yun ZB, Odeberg J, Lundeberg J, et al. Restriction of hepatitis C virus heterogeneity during prolonged interferon-alpha therapy in relation to changes in virus load. J Infect Dis 1996;173:992-996
225. Sakuma I, Enomoto N, Kurosaki M, et al. Selection of hepatitis C virus quasispecies during interferon treatment. Arch Virol 1996;141:1921-1932
226. Polyak SJ, McArdle S, Liu S-L, et al. Evolution of hepatitis C virus quasispecies in hypervariable region 1 and the putative interferon sensitivity-determining region during interferon therapy and natural infection. J Virol 1998;72:4288-4296
227. Pawlotsky JM, Germanidis G, Frainais PO, et al. Evolution of the hepatitis C virus second envelope protein hypervariable region in chronically infected patients receiving alpha interferon therapy. J Virol 1999;73:6490-6499
228. Farci P, Strazzera R, De Gioannis D, et al. Evolution of HCV quasispecies in the different patterns of response to interferon therapy in chronic hepatitis C. Proceedings of the 6th International Symposium on Hepatitis C and Related Viruses, Bethesda, MD, 6-9 June 1999, p. 80
229. Gerotto M, Sullivan DG, Polyak SJ, et al. Effect of retreatment with interferon alone or interferon plus ribavirin on hepatitis C virus quasispecies diversification in nonresponder patients with chronic hepatitis C. J Virol 1999;73:7241-7247
230. González-Peralta RP, Liu WZ, Davis GL, et al. Modulation of hepatitis C virus quasispecies heterogeneity by interferon-alpha and ribavirin therapy. J Viral Hepat 1997;4:99-106
231. Lee J-H, von Wagner M, Roth WK, et al. Effect of ribavirin on virus load and quasispecies distribution in patients infected with hepatitis C virus. J Hepatol 1998;29:29-35
232. Enomoto N, Sakuma I, Asahina Y, et al. Comparison of full-length sequences of interferon-sensitive and resistant hepatitis C virus 1b. J Clin Invest 1995;96:224-230
233. Enomoto N, Sakuma I, Asahina Y, et al. Mutations in the nonstructural protein 5A gene and response to interferon in patients with chronic hepatitis C virus 1b infection. N Engl J Med 1996;334:77-81
234. Tao Q, Wei L, Chang J, et al. Relationship between interferon therapy and variability in nonstructural gene 5b of hepatitis C virus. J Gastroenterol 1998;33:684-693
235. Saiz JC, Lopez-Labrador FX, Ampurdanes S, et al. The prognostic relevance of the nonstructural A gene interferon sensitivity determining region is different in infections with genotype 1b and 3a isolates of hepatitis C virus. J Infect Dis 1998;177: 839-847
236. Gale MJ, Jr., Korth MJ, Tang NM, et al. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural A protein. Virology 1997;230:217-227
237. Squadrito G, Leone F, Sartori M, et al. Mutations in the nonstructural A region of hepatitis C virus and response of chronic hepatitis C to interferon alfa. Gastroenterololy 1997;113: 67-72
238. Odeberg J, Yun Z, Sonnerborg A, et al. Variation in the hepatitis C virus NS5a region in relation to hypervariable region 1 heterogeneity during interferon treatment. J Med Virol 1998;6: 33-38
239. Pawlotsky JM, Germanidis G, Neumann AU, et al. Interferon resistance of hepatitis C virus genotype 1b: Relationship to nonstructural 5A gene quasispecies mutations. J Virol 1998;72: 279-280