Viral persistence, antibody to E1 and E2, and hypervariable region 1 sequence stability in hepatitis C virus-inoculated chimpanzees

Journal of Virology

Volumn 73, Issue 2, 1999, Pages 1118-1126

  Bassett, Suzanne E ^a,b   Thomas, David L ^c   Brasky, Kathleen M ^a   Lanford, Robert E ^a,b  

^a SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANTIBODY; ENVELOPE PROTEIN; NUCLEOTIDE; VIRUS RNA;

AMINO ACID SEQUENCE; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CHIMPANZEE; ENZYME LINKED IMMUNOSORBENT ASSAY; HEPATITIS C; HEPATITIS C VIRUS; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOBLOTTING; NONHUMAN; NUCLEOTIDE SEQUENCE; PERSISTENT VIRUS INFECTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 0032923618     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.2.1118-1126.1999     Document Type: Article

References (56)

1. Abe, K., G. Inchauspe, and K. Fujisawa. 1992. Genomic characterization and mutation rate of hepatitis C virus isolated from a patient who contracted hepatitis during an epidemic of non-A, non-B hepatitis in Japan. J. Gen. Virol. 73:2725-2729.
2. Abe, K., G. Inchauspe, T. Shikata, and A. M. Prince. 1992. Three different patterns of hepatitis C virus infection in chimpanzees. Hepatology 15:690-695.
3. Abrignani, S. 1997. Immune responses throughout hepatitis C virus (HCV) infection: HCV from the immune system point of view. Springer Semin. Immunopathol. 19:47-55.
4. Allander, T., A. Beyene, S. H. Jacobson, L. Grillner, and M. A. A. Persson. 1997. Patients infected with the same hepatitis C virus strain display different kinetics of the isolate-specific antibody response. J. Infect. Dis. 175:26-31.
5. Alter, H. J. 1995. To C or not to C: these are the questions. J. Am. Soc. Hematol. 85:1681-1695.
6. Alter, M. J., H. S. Margolis, K. Krawczynski, F. N. Judson, A. Mares, W. J. Alexander, P. Y. Hu, J. K. Miller, M. A. Gerber, R. E. Sampliner, E. L. Meeks, and M. J. Beach. 1992. The natural history of community-acquired hepatitis C in the United States. N. Engl. J. Med. 327:1899-1905.
7. Bassett, S. E., K. M. Brasky, and R. E. Lanford. 1998. Analysis of hepatitis C virus (HCV)-inoculated chimpanzees reveals unexpected clinical profiles. J. Virol. 72:2589-2599.
8. Booth, J. C., U. Kumar, D. Webster, J. Monjardino, and H. C. Thomas. 1998. 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 27:223-227.
9. 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.
10. Bukh, J., R. H. Purcell, and R. H. Miller. 1993. 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 90:8234-8238.
11. Cerino, A., M. Bissolati, A. Cividini, A. Nicosia, M. Esumi, N. Hayashi, K. Mizuno, R. Slobbe, P. Oudshoorn, E. Silini, M. Asti, and M. U. Mondelli. 1997. Antibody responses to the hepatitis C virus E2 protein: relationship, to viremia and prevalence in anti-HCV seronegative subjects. J. Med. Virol. 51:1-5.
12. Chang, K. M., B. Rehermann, and F. V. Chisari. 1997. Immunopathology of hepatitis C. Springer Semin. Immunopathol. 19:57-68.
13. Chien, D. Y., Q.-L. Choo, R. Ralston, R. Spaete, M. Tong, M. Houghton, and G. Kuo. 1993. Persistence of HCV despite antibodies to both putative envelope glycoproteins. Lancet 342:933. (Letter.)
14. 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.
15. Choo, Q.-L., K. H. Richman, J. H. Han, K. Berger, C. Lee, C. Dong, C. Gallegos, D. Corr, A. Medina-Selby, P. J. Barr, A. J. Weiner, D. W. Bradley, G. Kuo, and M. Houghton. 1991. Genetic organization and diversity of the hepatitis C virus. Pro. Natl. Acad. Sci. USA 88:2451-2455.
16. Eckels, D., P. Flamenberg, and J. C. Gill. 1996. Hepatitis C virus: models of immunopathogenesis and prophylaxis. Tranfusion 36:836-844.
17. Enomoto, N., C. Sato, M. Kurosaki, and F. Marumo. 1994. Hepatitis C virus after interferon treatment has the variation in the hypervariable region of envelope 2 gene. J. Hepatol. 20:252-261.
18. Farci, P., J. Bukh, and R. H. Purcell. 1997. The quasispecies of hepatitis C virus and the host immune response. Springer Semin. Immunopathol. 19:5-26.
19. 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.
20. Fong, T. L., S. R. Lee, W. K. Briggs, B. Valinluck, S. Govindarajan, A. Hoffman, B. Jaczko, and A. G. Redeker. 1996. Clinical significance of hepatitis C viral RNA status and its correlation to antibodies to structural HCV antigens in anti-HCV reactive patients with normal liver tests. J. Med. Virol. 49:253-258.
21. Harada, S., R. Suzuki, A. Ando, Y. Watanabe, S. Yagi, T. Miyamura, and I. Saito. 1995. Establishment of a cell line constitutively expressing E2 glycoprotein of hepatitis C virus and humoral response of hepatitis C patients to the expressed protein. J. Gen. Virol. 76:1223-1231.
22. Hilfenhaus, J., U. Krupka, T. Nowak, L. B. Cummins, K. Fuchs, and M. Roggendorf. 1992. Follow-up of hepatitis C virus infection in chimpanzees: determination of viraemia and specific humoral immune response. J. Gen. Virol. 73:1015-1019.
23. Houghton, M., A. Weiner, J. Han, G. Kuo, and Q.-L. Choo. 1991. Molecular biology of the hepatitis C viruses: implications for diagnosis, development and control of disease. Hepatology 14:381-388.
24. Hüssy, P., H. Faust, J.-C. Wagner, G. Schmid, J. Mous, and H. Jacobsen. 1997. Evaluation of hepatitis C virus envelope proteins expressed in E. coli and insect cells for use as tools for antibody screening. J. Hepatol. 26:1179-1186.
25. Kato, N., Y. Ootsuyama, T. Tanaka, M. Nakagawa, T. Nakazawa, K. Muraiso, S. Ohkoshi, M. Hijikata, and K. Shimotohno. 1992. Marked sequence diversity in the putative envelop proteins of hepatitis C viruses. Virus Res. 22:107-123.
26. 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.
27. 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.
28. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
29. Lanford, R. E., and J. S. Butel. 1979. Antigenic relationship of SV40 early proteins to purified large T polypeptide. Virology 97:295-306.
30. Lanford, R. E., K. D. Carey, L. E. Estlack, G. C. Smith, and R. V. Hay. 1989. Analysis of plasma protein and lipoprotein synthesis in long-term primary cultures of baboon nepatocytes maintained in serum-free medium. In vitro Cell. Dev. Biol. 25:174-182.
31. Lanford, R. E., L. Notvall, L. H. Barbosa, and J. W. Eichberg. 1991. Evaluation of a chimpanzee colony for antibodies to hepatitis C virus. J. Med. Virol. 34:148-153.
32. Lanford, R. E., L. Notvall, and B. Beames. 1995. Nucleotide priming and reverse transcriptase activity in hepatitis B virus polymerase expressed in insect cells. J. Virol. 69:4431-4439.
33. Lanford, R. E., L. Notvall, D. Chavez, R. White, G. Frenzel, C. Simonsen, and J. Kim. 1993. Analysis of hepatitis C virus capsid, E1, and E2/Ns1 proteins expressed in insect cells. Virology 197:225-235.
34. Lesniewski, R., G. Okasinski, R. Carrick, C. Van Sant, S. Desai, R. Johnson, J. Scheffel, B. Moore, and I. Mushahwar. 1995. Antibody to hepatitis C virus second envelope (HCV-E2) glycoprotein: a new marker of HCV infection closely associated with viremia. J. Med. Virol. 45:415-422.
35. Michalak, J. P., C. Wychowski, A. Choukhi, J. C. Meunier, S. Ung, C. M. Rice, and J. Dubuisson. 1997. Characterization of truncated forms of hepatitis C virus glycoproteins. J. Gen. Virol. 78:2299-2306.
36. Mink, M. A., S. Benichou, P. Madaule, P. Tiollais, A. M. Prince, and G. Inchauspe. 1994. Characterization and mapping of a B-cell immunogenic domain in hepatitis C virus E2 glycoprotein using a yeast peptide library. Virology 200:246-255.
37. National Institutes of Health. 1997. National Institutes of Health Consensus development conference panel statement: management of hepatitis C. Hepatology 26:2S-10S.
38. Nishihara, T., C. Nozaki, H. Nakatake, K. Hoshiko, M. Esumi, N. Hayashi, K. Hino, F. Hamada, K. Mizuno, and T. Shikata. 1993. Secretion and purification of hepatitis C virus NS1 glycoprotein produced by recombinant baculovirus-infected insect cells. Gene 129:207-214.
39. Odeberg, J., Z. B. Yun, A. Sönnerborg, K. Bjoro, M. Uhlén, and J. Lundeberg. 1997. Variation of hepatitis C virus hypervariable region 1 in immunocompromised patients. J. Infect. Dis. 175:938-943.
40. 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.
41. Okada, S.-I., Y. Akahane, H. Suzuki, H. Okamoto, and S. Mishiro. 1992. The degree of variability in the amimo terminal region of the E2/NS1 protein of hepatitis C virus correlates with responsiveness to interferon therapy in viremic patients. Hepatology 16:619-624.
42. Okamoto, H., M. Kojima, S.-I. Okada, H. Yoshizawa, H. Iizuka, T. Tanaka, E. E. Muchmore, D. A. Peterson, Y. Ito, and S. Mishiro. 1992. Genetic drift of hepatitis C virus during an 8.2-year infection in a chimpanzee: variability and stability. Virology 190:894-899.
43. Rosa, D., S. Campagnoli, C. Moretto, E. Guenzi, I. Cousens, M. Chin, C. Dong, A. J. Weiner, J. Y. N. Lau, Q. L. Choo, D. Chien, P. Pileri, M. Houghton, and S. Abrignani. 1996. A quantitative test to estimate neutralizing antibodies to the hepatitis C virus: cytofluorimetric assessment of envelope glycoprotein 2 binding to target cells. Proc. Natl. Acad. Sci. USA 93:1759-1763.
44. Summers, M. D., and G. E. Smith. 1987. A manual of methods for baculovirus vectors and insect cell culture procedures. Tex. Agric. Exp. Stn. Bull. 1555:1-48.
45. Thomas, D. L., D. Vlahov, L. Solomon, S. Cohn, E. Taylor, R. Garfein, and K. E. Nelson. 1995. Correlates of hepatitis C virus infections among injection drug users. Medicine (Baltimore) 74:212-220.
46. 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.
47. Van Doom, L.-J., K. van Hoek, G. de Martinoff, F. Bosman, L. Stuyver, T. Kos, I. Frantzen, P. Sillekens, G. Maertens, and W. Quint. 1997. Serological and molecular analysis of hepatitis C virus envelope regions 1 and 2 during acute and chronic infections in chimpanzees. J. Med. Virol. 52:441-450.
48. Walker, C. M. 1997. Comparative features of hepatitis C virus infection in humans and chimpanzees. Springer Semin. Immunopathol. 19:85-98.
49. Wang, Y. F., B. Brotman, L. Andrus, and A. M. Prince. 1996. Immune response to epitopes of hepatitis C virus (HCV) structural proteins in HCV-infected humans and chimpanzees. J. Infect. Dis. 173:808-821.
50. Weiner, A. J., M. J. Brauer, J. Rosenblatt, K. H. Richman, J. Tung, K. Crawford, F. Bonino, G. Saracco, Q. L. Choo, M. Houghton, et al. 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.
51. Wray, W., T. Boulikas, V. P. Wray, and R. Hancock. 1981. Silver staining of proteins in polyacrylamide gels. Anal. Biochem. 118:197-203.
52. Yeh, B. I., K. H. Han, S. H. Oh, H. S. Kim, S. H. Hong, 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.
53. Yoshioka, K., Y. Higashi, K. Tanaka, T. Aiyama, M. Takayanagi, A. Okumura, K. Iwata, Y. Nagai, and S. Kakumu. 1996. Deficiency of antibody response to hypervariable region of hepatitis C virus in patients with chronic hepatitis C. J. Hepatol. 24:649-657.
54. Yuki, N., N. Hayashi, A. Kasahara, H. Hagiwara, E. Mita, K. Ohkawa, K. Katayama, H. Fusamoto, and T. Kamada. 1996. Quantitative analysis of antibody to hepatitis C virus envelope 2 glycoprotein in patients with chronic hepatitis C virus infection. Hepatology 23:947-952.
55. Yuki, N., N. Hayashi, T. Moribe, Y. Matsushita, T. Tabala, T. Inoue, Y. Kanazawa, K. Ohkawa, A. Kasahara, H. Fusamoto, and T. Kamada. 1997. Relation of disease activity during chronic hepatitis C infection to complexity of hypervariable region 1 quasispecies. Hepatology 25:439-444.
56. Zibert, A., H. Meisel, W. Kraas, A. Schulz, G. Jung, and M. Roggendorf. 1997. Early antibody response against hypervariable region 1 is associated with acute self-limiting infections of hepatitis C virus. Hepatology 25:1245-1249.