Long-term persistence of infection in chimpanzees inoculated with an infectious hepatitis C virus clone is associated with a decrease in the viral amino acid substitution rate and low levels of heterogeneity

Journal of Virology

Volumn 78, Issue 18, 2004, Pages 9782-9789

  Fernandez, Javier ^a,c   Taylor, Deborah ^a   Morhardt, Duncan R ^a   Mihalik, Kathleen ^a   Puig, Montserrat ^a   Rice, Charles M ^b   Feinstone, Stephen M ^a   Major, Marian E ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c Ceregene Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; CHIMPANZEE; CLONE; GENE MUTATION; GENETIC HETEROGENEITY; HEPATITIS C VIRUS; INOCULATION; NONHUMAN; PERSISTENT VIRUS INFECTION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RNA TRANSCRIPTION; SINGLE STRAND CONFORMATION POLYMORPHISM; VIRUS GENE; VIRUS GENOME; VIRUS MUTATION;

AMINO ACID SUBSTITUTION; ANIMALS; APE DISEASES; GENOME, VIRAL; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; PAN TROGLODYTES; POLYMORPHISM, SINGLE-STRANDED CONFORMATIONAL; SELECTION (GENETICS); VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS;

EID: 4444261389     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.18.9782-9789.2004     Document Type: Article

References (31)

1. Bartosch, B., J. Dubuisson, and F. L. Cosset. 2003. Infectious hepatitis C virus pseudoparticles containing functional E1-E2 envelope protein complexes. J. Exp. Med. 197:633-642.
2. Blight, K. J., A. A. Kolykhalov, and C. M. Rice. 2000. Efficient initiation of HCV RNA replication in cell culture. Science 290:1972-1974.
3. Bukh, J., R. H. Miller, and R. H. Purcell. 1995. Genetic heterogeneity of hepatitis C virus: quasispecies and genotypes. Semin. Liver Dis. 15:41-63.
4. Chang, K. M., B. Rehermann, J. G. McHutchison, C. Pasquinelli, S. Southwood, A. Sette, and F. V. Chisari. 1997. Immunological significance of cytotoxic T lymphocyte epitope variants in patients chronically infected by the hepatitis C virus. J. Clin. Investig. 100:2376-2385.
5. Choo, Q. L., G. Kuo, R. Ralston, A. Weiner, D. Chien, G. Van Nest, J. Han, K. Berger, K. Thudium, C. Kuo, J. Kansopon, J. McFarland, A. Tabrizi, K. Ching, B. Moss, L. B. Cummins, M. Houghton, and E. Muchmore. 1994. Vaccination of chimpanzees against infection by the hepatitis C virus. Proc. Natl. Acad. Sci. USA 91:1294-1298.
6. 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.
7. Erickson, A. L., Y. Kimura, S. Igarashi, J. Eichelberger, M. Houghton, J. Sidney, D. McKinney, A. Sette, A. L. Hughes, and C. M. Walker. 2001. The outcome of hepatitis C virus infection is predicted by escape mutations in epitopes targeted by cytotoxic T lymphocytes. Immunity 15:883-895.
8. Farci, P., A. Shimoda, A. Coiana, G. Diaz, G. Peddis, J. C. Melpolder, A. Strazzera, D. Y. Chien, S. J. Munoz, A. Balestrieri, R. H. Purcell, and H. J. Alter. 2000. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288:339-344.
9. Farci, P., A. Shimoda, D. Wong, T. Cabezon, D. De Gioannis, A. Strazzera, Y. Shimizu, M. Shapiro, H. J. Alter, and R. H. Purcell. 1996. 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 93:15394-15399.
10. Forns, X., R. Thimme, S. Govindarajan, S. U. Emerson, R. H. Purcell, F. V. Chisari, and J. Bukh. 2000. Hepatitis C virus lacking the hypervariable region 1 of the second envelope protein is infectious and causes acute resolving or persistent infection in chimpanzees. Proc. Natl. Acad. Sci. USA 97:13318-13323.
11. Grakoui, A., N. H. Shoukry, D. J. Woollard, J. H. Han, H. L. Hanson, J. Ghrayeb, K. K. Murthy, C. M. Rice, and C. M. Walker. 2003. HCV persistence and immune evasion in the absence of memory T cell help. Science 302:659-662.
12. Hsu, M., J. Zhang, M. Flint, C. Logvinoff, C. Cheng-Mayer, C. M. Rice, and J. A. McKeating. 2003. Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. USA 100:7271-7276.
13. Kaneko, T., T. Moriyama, K. Udaka, K. Hiroishi, H. Kita, H. Okamoto, H. Yagita, K. Okumura, and M. Imawari. 1997. Impaired induction of cytotoxic T lymphocytes by antagonism of a weak agonist borne by a variant hepatitis C virus epitope. Eur. J. Immunol. 27:1782-1787.
14. Kolykhalov, A. A., E. V. Agapov, K. Blight, K. Mihalik, S. M. Feinstone, and C. M. Rice. 1997. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 277:570-574.
15. 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.
16. Major, M. E., K. Mihalik, J. Fernandez, J. Seidman, D. Kleiner, A. A. Kolykhalov, C. M. Rice, and S. M. Feinstone. 1999. Long-term follow-up of chimpanzees inoculated with the first infectious clone for hepatitis C virus. J. Virol. 73:3317-3325.
17. Major, M. E., B. Rehermann, and S. M. Feinstone. 2001. Hepatitis C viruses, p. 1127-1161. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
18. Ogata, N., H. J. Alter, R. H. Miller, and R. H. Purcell. 1991. Nucleotide sequence and mutation rate of the H strain of hepatitis C virus. Proc. Natl. Acad. Sci. USA 88:3392-3396.
19. Okada, S. I., Y. Akahane, H. Suzuki, H. Okamoto, and S. Mishiro. 1992. 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 16:619-624.
20. Penin, F., C. Combet, G. Germanidis, P. O. Frainais, G. Deleage, and J. M. Pawlotsky. 2001. Conservation of the conformation and positive charges of hepatitis C virus E2 envelope glycoprotein hypervariable region 1 points to a role in cell attachment. J. Virol. 75:5703-5710.
21. Puig, M., M. E. Major, K. Mihalik, M. Y. Yu, and S. M. Feinstone. 2004. Immunization of chimpanzees with an envelope protein-based vaccine enhances specific humoral and cellular immune responses that delay hepatitis C virus infection. Vaccine 22:991-1000,
22. Puig, M., K. Mihalik, M. Y. Yu, S. M. Feinstone, and M. E. Major. 2002. Sensitivity and reproducibility of HCV quantitation in chimpanzee sera using TaqMan real-time PCR assay. J. Virol. Methods 105:253-263.
23. Ray, S. C., Q. Mao, R. E. Lanford, S. Bassett, O. Laeyendecker, Y. M. Wang, and D. L. Thomas. 2000. Hypervariable region 1 sequence stability during hepatitis C virus replication in chimpanzees. J. Virol. 74:3058-3066.
24. 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.
25. Saito, I., T. Miyamura, A. Ohbayashi, H. Harada, T. Katayama, S. Kikuchi, Y. Watanabe, S. Koi, M. Onji, Y. Ohta, Q. L. Choo, M. Houghton, and G. Kuo. 1990. Hepatitis C virus infection is associated with the development of hepatocellular carcinoma. Proc. Natl. Acad. Sci. USA 87:6547-6549.
26. Shimizu, Y. K., M. Hijikata, A. Iwamoto, H. J. Alter, R. H. Purcell, and H. Yoshikura. 1994. Neutralizing antibodies against hepatitis C virus and the emergence of neutralization escape mutant viruses. J. Virol. 68:1494-1500.
27. Simmonds, P., A. Alberti, H. J. Alter, F. Bonino, D. W. Bradley, C. Brechot, J. T. Brouwer, S. W. Chan, K. Chayama, and D. S. Chen. 1994. A proposed system for the nomenclature of hepatitis C viral genotypes. Hepatology 19:1321-1324.
28. Smith, D. B. 1999. Evolution of the hypervariable region of hepatitis C virus. J. Viral Hepat, 6(Suppl. 1):41-46.
29. van Doorn, L., 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.
30. Wang, H., T. Bian, S. J. Merrill, and D. D. Eckels. 2002. Sequence variation in the gene encoding the nonstructural 3 protein of hepatitis C virus: evidence for immune selection. J. Mol. Evol. 54:465-473.
31. Wang, H., and D. D. Eckels. 1999. 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. 162:4177-4183.