Evolution of the hepatitis C virus second envelope protein hypervariable region in chronically infected patients receiving alpha interferon therapy

Journal of Virology

Volumn 73, Issue 8, 1999, Pages 6490-6499

  Pawlotsky, Jean Michel ^a   Germanidis, Georgios ^a   Frainais, Pierre Olivier ^a   Bouvier, Magali ^a   Soulier, Alexandre ^a   Pellerin, Muriel ^a   Dhumeaux, Daniel ^a  

^a HENRI MONDOR HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT ALPHA2A INTERFERON; VIRUS ENVELOPE PROTEIN;

ADULT; AGED; ARTICLE; CELL SURVIVAL; CHRONIC DISEASE; CYTOTOXIC T LYMPHOCYTE; DRUG EFFECT; ENVELOPE GENE; FEMALE; HEPATITIS C VIRUS; HUMAN; IMMUNOGLOBULIN VARIABLE REGION; MAJOR CLINICAL STUDY; MALE; MOLECULAR CLONING; PRIORITY JOURNAL; SINGLE STRAND CONFORMATION POLYMORPHISM; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS INFECTION; VIRUS REPLICATION;

EID: 0032795492     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.8.6490-6499.1999     Document Type: Article

References (70)

1. Alter, H. 1998. Natural history and clinical aspects of hepatitis C virus infection, p. 43-50. In R. F. Schinazi, J. P. Sommadossi, and H. C. Thomas (ed.), Therapies for viral hepatitis. International Medical Press, London, United Kingdom.
2. Baron, S., S. K. Tyring, W. R. Fleischmann, D. H. Coppenhaver, D. W. Niesel, G. R. Klimpel, G. J. Stanton, and T. K. Hughes. 1991. The interferons. Mechanisms of action and clinical applications. JAMA 266:1375-1383.
3. Barrera, J. M., M. Bruguera, M. G. Ercilla, C. Gil, R. Celis, M. P. Gil, M. del Valle Onorato, J. Rodes, and A. Ordinas. 1995. Persistent hepatitis C viremia after acute self-limiting posttransfusion hepatitis C. Hepatology 21:639-644.
4. Bennett, W. G., Y. Inoue, J. R. Beck, J. B. Wong, S. G. Pauker, and G. L. Davis. 1997. Estimates of the cost-effectiveness of a single course of interferon-α2b in patients with histologically mild chronic hepatitis C. Ann. Intern. Med. 127:855-865.
5. Carithers, R. L., Jr., and S. S. Emerson. 1997. Therapy of hepatitis C: meta-analysis of interferon alfa-2b trials. Hepatology 26(Suppl. 1):83S-88S.
6. Chang, K. M. 1998. The mechanisms of chronicity in hepatitis C virus infection. Gastroenterology 115:1015-1017.
7. Chazouillères, O., M. Kim, C. Combs, L. Ferrell, P. Bacchetti, J. Roberts, N. L. Ascher, P. Neuwald, J. Wilber, M. Urdea, S. Quan, R. Sanchez-Pescador, and T. L. Wright. 1994. Quantitation of hepatitis C virus RNA in liver transplant recipients. Gastroenterology 106:994-999.
8. Chemello, L., L. Cavalletto, C. Casarin, P. Bonetti, E. Bernardinello, P. Pontisso, C. Donada, F. Belussi, S. Martinelli, A. Alberti, and the TriVeneto Viral Hepatitis Group. 1996. Persistent hepatitis C viremia predicts late relapse after sustained response to interferon-α in chronic hepatitis C. Ann. Intern. Med. 124:1058-1060.
9. Choo, Q. L., G. Kuo, A. J. Weiner, L. R. Overby, D. W. Bradley, and M. Houghton. 1989. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244:359-362.
10. Devis, G. L., R. Esteban-Mur, V. Rustgi, J. Hoefs, S. C. Gordon, C. Trépo, M. L. Shiffman, S. Zeuzem, A. Craxi, M. H. Ling, and J. Albrecht. 1998. Interferon alfa-2b alone or in combination with ribavirin for the treatment of relapse of chronic hepatitis C. N. Engl. J. Med. 339:1493-1499.
11. Delwart, E. L., H. Pan, A. Neumann, and M. Markowitz. 1998. Rapid, transient changes at the env locus of plasma human immunodeficiency virus type 1 populations during the emergence of protease inhibitor resistance. J. Virol. 72:2416-2421.
12. Dhumeaux, D., M. Doffoël, and J. P. Galmiche. 1997. A French consensus conference on hepatitis C: screening and treatment. J. Hepatol. 27:941-944.
13. Domingo, E. 1996. Biological significance of viral quasispecies. Viral Hepatitis Rev. 2:247-261.
14. Duarte, E. A., I. S. Novella, S. C. Weaver, E. Domingo, S. Wain-Hobson, D. K. Clarke, A. Moya, S. F. Elena, J. C. de la Torre, and J. J. Holland. 1994. RNA virus quasispecies: significance for viral disease and epidemiology. Infect. Agents Dis. 3:201-214.
15. Duvoux, C., J. M. Pawlotsky, D. Cherqui, J. Tran van Nhieu, J. M. Métreau, P. L. Fagniez, J. Duval, E. S. Zafrani, and D. Dhumeaux. 1995. Serial quantitative determination of hepatitis C virus RNA levels after liver transplantation. A useful test for diagnosis of hepatitis C virus reinfection. Transplantation 60:457-461.
16. Enomoto, N., I. Sakuma, Y. Asahina, M. Kurosaki, T. Murakami, C. Yamamoto, N. Izumi, F. Marumo, and C. Sato. 1995. Comparison of full-length sequences of interferon-sensitive and resistant hepatitis C virus 1b. Sensitivity to interferon is conferred by amino acid substitutions in the NS5A region. J. Clin. Investig. 96:224-230.
17. Enomoto, N., M. Kurosaki, Y. Tanaka, F. Marumo, and S. Sato. 1994. Fluctuation of hepatitis C virus quasispecies in persistent infection and interferon treatment revealed by single-strand conformation polymorphism analysis. J. Gen. Virol. 75:1361-1369.
18. Farci, P., H. J. Alter, D. C. Wong, R. H. Miller, S. Govindarajan, R. Engle, M. Shapiro, and R. H. Purcell. 1994. Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc. Natl. Acad. Sci. USA 91:7792-7796.
19. Farrell, G. C., B. R. Bacon, R. D. Goldin, and the Clinical Advisory Group for the Hepatitis C Comparative Study. 1998. Lymphoblastoid interferon alfa-n1 improves the long-term response to a 6-month course of treatment in chronic hepatitis C compared with recombinant interferon alfa-2b: results of an international randomized controlled trial. Hepatology 27:1121-1127.
20. Felsenstein, J. 1985. Confidence limits on phytogenies: an approach using the bootstrap. Evolution 39:783-791.
21. Felsenstein, J. 1995. PHYLIP (phylogeny inference package), version 3.57. Distributed by the author. Department of Genetics, University of Washington, Seattle.
22. Gale, M., Jr., C. M. Blakely, B. Kwieciszewski, S. L. Tan, M. Dossett, N. M. Tang, M. J. Korth, S. J. Polyak, D. R. Gretch, and M. G. Katze. 1998. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol. Cell. Biol. 18:5208-5218.
23. Gale, M. J., Jr., M. J. Korth, N. M. Tang, S. L. Tan, D. A. Hopkins, T. E. Dever, S. J. Polyak, D. R. Gretch, and M. G. Katz. 1997. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230:217-227.
24. Heim, M. K., D. Moradpour, and H. E. Blum. 1998. Expression of hepatitis C virus proteins inhibits signal transduction through the Jak-Stat pathway. Hepatology 28:321A.
25. Jukes, T. H., and T. R. Cantor. 1969. Evolution of protein molecules, p. 21-132. In H. N. Munro (ed.), Mammalian protein metabolism. Academic Press, New York, N.Y.
26. Kao, J. H., P. J. Chen, M. Y. Lai, T. H. Wang, and D. S. Chen. 1994. Quasispecies of hepatitis C virus and genetic drift of the hypervariable region in chronic type C hepatitis. J. Infect. Dis. 172:261-264.
27. Kato, N., H. Sekiya, Y. Ootsuyama, T. Nakazawa, M. Hijikata, S. Ohkoshi, and K. Shimotohno. 1993. Humoral immune response to hypervariable region 1 of the putative envelope glycoprotein (gp70) of hepatitis C virus. J. Virol. 67:3923-3930.
28. Kato, N., Y. Ootsuyama, H. Sekiya, S. Ohkoshi, T. Nakazawa, M. Hijikata, and K. Shimotohno. 1994. Genetic drift in hypervariable region 1 of the viral genome in persistent hepatitis C virus infection. J. Virol. 68:4776-4784.
29. Knodell, R. G., K. G. Ishak, W. C. Black, T. S. Chen, R. Craig, N. Kaplowitz, T. W. Kiernan, and J. Wollman. 1981. Formulation and application of a numerical scoring system for assessing histological activity in asymptomatic chronic active hepatitis. Hepatology 1:431-435.
30. Kojima, M., T. Osuga, F. Tsuda, T. Tanaka, and H. Okamoto. 1994. Influence of antibodies to the hypervariable region of E2/NS1 glycoprotein on the selective replication of hepatitis C virus in chimpanzees. Virology 204:665-672.
31. Korenaga, M., K. Hino, M. Okazaki, M. Okuda, and K. Okita. 1997. Differences in hypervariable region 1 quasispecies between immune complexed and non-immune complexed hepatitis C virus particles. Biochem. Biophys. Res. Commun. 240:677-682.
32. Koziel, M. J. 1997. The role of the immune responses in the pathogenesis of hepatitis C virus infection. J. Viral Hepatitis 4(Suppl. 2):31-41.
33. Kumar, S., K. Tamura, and M. Nei. 1993. MEGA: molecular evolutionary genetic analysis for microcomputers. Comput. Appl. Biosci. 10:189-191.
34. Kumar, U., J. Monjardino, and H. C. Thomas. 1994. Hypervariable region of hepatitis C virus envelope glycoprotein (E2/NS1) in an agammaglobulinemic patient. Gastroenterology 106:1072-1075.
35. Kurosaki, M., N. Enomoto, F. Marumo, and C. Sato. 1993. Rapid sequence variation of the hypervariable region of hepatitis C virus during the course of chronic infection. Hepatology 18:1293-1299.
36. Lau, D. T. Y., D. E. Kleiner, M. G. Ghany, Y. Park, P. Schmid, and J. H. Hoofhagle. 1998. Ten-year follow-up after interferon-́ therapy for chronic hepatitis C. Hepatology 28:1121-1127.
37. Lindsay, K. L. 1997. Therapy of hepatitis C: overview. Hepatology 26(Suppl. 1):71S-77S.
38. Manzin, A., L. Solforosi, E. Petrelli, G. Macarri, G. Tosone, M. Piazza, and M. Clementi. 1998. Evolution of hypervariable region 1 of hepatitis C virus in primary infection. J. Virol. 72:6271-6276.
39. Marcellin, P., N. Boyer, A. Gervais, M. Martinot, M. Pouteau, C. Castelnau, A. Kilani, J. Areias, A. Auperin, J. P. Benhamou, C. Degott, and S. Erlinger. 1997. Long-term histologic improvement and loss of detectable intrahepatic HCV RNA in patients with chronic hepatitis C and sustained response to interferon-α therapy. Ann. Intern. Med. 127:875-581.
40. Martell, M., J. I. Esteban, J. Quer, J. Genesca, A. Weiner, R. Esteban, J. Guardia, and J. Gomez. 1992. Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: quasispecies nature of HCV genome distribution. J. Virol. 66:3225-3229.
41. McHutchison, J. G., S. C. Gordon, E. R. Schiff, M. L. Shiftman, W. M. Lee, V. K. Rustgl, Z. D. Goodman, M. H. Ling, S. Cort, and J. K. Albrecht. 1998. Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. N. Engl. J. Med. 339:1485-1492.
42. Nagasaka, A., S. Hige, I. Tsunematsu, J. Yoshida, Y. Sasaki, T. Matsushima, and M. Asaka. 1996. Changes in hepatitis C virus quasispecies and density populations in patients before and after interferon therapy. J. Med. Virol. 50:214-220.
43. Nowak, M. A., R. M. May, R. E. Phillips, S. Rowland-Jones, D. G. Lalloo, S. McAdam, P. Klenerman, B. Koppe, K. Sigmund, C. R. M. Bangham, and A. J. McMichael. 1995. Antigenic oscillations and shifting immunodominance in HIV-1 infections. Nature 375:606-611.
44. O'Connel, J. F. 1997. Mechanisms of action of interferon: potential role in hepatitis C. Viral Hepatitis Rev. 3:121-128.
45. Odeberg, J., Z. Yun, A. Sönnerborg, K. Bjoro, M. Uhlen, and J. Lundenberg. 1997. Variation of hepatitis C virus hypervariable region 1 in immunocompromised patients. J. Infect. Dis. 175:938-943.
46. Paterson, M., C. D. Laxton, R. Sully, H. C. Thomas, A. Ackrill, and G. R. Foster. 1998. The non-structural 5A protein of the hepatitis C virus blocks the antiviral effects triggered by IFN-α. Hepatology 28:370A.
47. Pawlotsky, J. M. 1998. Hepatitis C virus infection: virus/host interactions. J. Viral Hepatitis 5(Suppl. 1):3-8.
48. Pawlotsky, J. M., G. Germanidis, A. U. Neumann, M. Pellerin, P. O. Frainais, and D. Dhumeaux. 1998. Interferon resistance of hepatitis C virus genotype 1b: relationship to nonstructural 5A gene quasispecies mutations. J. Virol. 72:2795-2805.
49. Pawlotsky, J. M., M. Pellerin, M. Bouvier, F. Roudot-Thoraval, G. Germanidis, A. Bastie, F. Darthuy, J. Rémiré. C. J. Soussy, and D. Dhumeaux. 1998. Genetic complexity of the hypervariable region 1 (HVR1) of hepatitis C virus (HCV): influence on characteristics of HCV infection and responses to interferon alfa therapy in patients with chronic hepatitis C. J. Med. Virol. 54:256-264.
50. Pawlotsky, J. M., F. Roudot-Thoraval, A. Bastie, F. Darthuy, J. Rémiré, J. M. Métreau, E. S. Zafrani, J. Duval, and D. Dhumeaux. 1996. Factors affecting treatment responses to interferon-α in chronic hepatitis C. J. Infect. Dis. 174:1-7.
51. Peters, M. 1996. Actions of cytokines on the immune response and viral interactions: an overview. Hepatology 23:909-916.
52. Polyak, S. J., S. McArdle, S. L. Liu, D. G. Sullivan, M. Chung, W. T. Hofgärtner, R L. Carithers, B. J. McMahon, J. I. Mullins, L Corey, and D. R. Gretch. 1998. 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. 72:4288-4296.
53. Poynard, T., P. Marcellin, S. S. Lee, C. Niederau, G. S. Minuk, G. Ideo, V. Bain, J. Heathcote, S. Zeuzem, C. Trépo, and J. Albrecht. 1998. Randomised trial of interferon alpha-2b plus ribavirin for 48 weeks or for 24 weeks versus interferon alpha-2b plus placebo for 48 weeks for treatment of chronic infection with hepatitis C virus. Lancet 352:1426-1432.
54. Ray, S. C., Y. M. Wang, O. Laeyendecker, J. R. Ticehurst, S. A. Villano, and D. L. Thomas. 1999. Acute hepatitis C virus structural gene sequences as predictors of persistent viremia: hypervariable region 1 as a decoy. J. Virol. 73:2938-2946.
55. Roudot-Thoraval, F., A. Bastie, J. M. Pawlotsky, D. Dhumeaux, and the Study Group for the Prevalence and the Epidemiology of Hepatitis C Virus. 1997. Epidemiological factors affecting the severity of hepatitis C virus-related liver disease: a French survey of 6664 patients. Hepatology 26:485-490.
56. Saitou, N., and N. Mei. 1987. The neighbor-joining methods: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
57. Shimizu, V. K., M. Hijikata, A. Iwamoto, H. J. Alter, R. H. Purcell, and H. Voshikura. 1994. Neutralizing antibodies against hepatitis C virus and the emergence of neutralization escape mutant viruses. J. Virol. 68:1494-1500.
58. Shindo, M., A. M. Di Bisceglie, R. Biswas, K. Mihalik, and S. M. Feinstone. 1992. Hepatitis C virus replication during acute infection in the chimpanzee. J. Infect. Dis. 166:424-427.
59. Shindo, M., K. Hamada, S. Koya, K. Arai, Y. Sokawa, and T. Okuno. 1996. The clinical significance of changes in genetic heterogeneity of the hypervariable region 1 in chronic hepatitis C with interferon therapy. Hepatology 24:1018-1023.
60. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
61. Thomssen, R., S. Bonk, and A. Thiele. 1994. Density heterogeneities of hepatitis C virus in human sera due to the binding of β-lipoproteins and immunoglobulins. Med. Microbiol. Immunol. 182:329-334.
62. Tilg, H. 1997. New insights into the mechanisms of interferon alfa: an immunoregulatory and anti-inflammatory cytokine. Gastroenterology 112: 1017-1021.
63. Toyoda, H., T. Kumada, S. Nakano, I. Takeda, K. Sugiyama, T. Osada, S. Kiriyama, Y. Sone, M. Kinoshita, and T. Hadama. 1997. Quasispecies nature of hepatitis C virus and response to alpha interferon: significance as a predictor of direct response to interferon. J. Hepatol. 28:6-13.
64. Tsai, S. L., Y. M. Chen, M. H. Chen, C. Y. Huang, I. S. Sheen, C. T. Yen, J. H. Huang, G. C. Kuo, and Y. F. Liaw. 1998. Hepatitis C virus variants circumventing cytotoxic T lymphocyte activity as a mechanism of chronicity. Gastroenterology 115:954-965.
65. van Doorn, L. J., I. Capriles, G. Maertens, R. DeLeys, K. Murray, T. Kos, H. Schellekens, and W. Quint. 1995. Sequence evolution of the hypervariable region in the putative envelope region E2/NS1 of hepatitis C virus is correlated with specific humoral immune responses. J. Virol. 69:773-778.
66. van Doorn, L. J., W. Quint, K. Tsiquaye, J. Voermans, D. Paelinck, T. Kos, G. Maertens, H. Schellekens, and K. Murray. 1994. Longitudinal analysis of hepatitis C virus infection and genetic drift of the hypervariable region. J. Infect. Dis. 169:1226-1235.
67. Weiner, A. J., H. M. Geysen, C. Christopherson, J. E. Hall, T. J. Mason, G. Saracco, F. Bonino, K. Crawford, C. D. Marion, K. A. Crawford, M. Brunetto, P. J. Barr, T. Miyamura, J. McHutchison, and M. Houghton. 1992. Evidence for immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants: potential role in chronic HCV infections. Proc. Natl. Acad. Sci. USA 89:3468-3472.
68. Weiner, A. J., M. J. Brauer, J. Rosenblatt, K. H. Richman, J. Tung, K. Crawford, F. Bonino, G. Saracco, Q. L. Choo, and M. Houghton. 1991. 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 180:842-848.
69. Wyatt, C. A., L. Andrus, B. Brotman, F. Huang, D. H. Lee, and A. M. Prince. 1998. Immunity in chimpanzees chronically infected with hepatitis C virus: role of minor quasispecies in reinfection. J. Virol. 72:1725-1730.
70. Yen, B. I., K. H. Han, S. H. Oh, H. S. Kim, S. H. Hong, S. H. Oh, and Y. S. Kim. 1996. Nucleotide sequence variation in the hypervariable region of the hepatitis C virus in the sera of chronic hepatitis C patients undergoing controlled interferon-α therapy. J. Med. Virol. 49:95-102.