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The Chimpanzee Model

Contributions and Considerations for Studies of Hepatitis B Virus

  • Protocol
Hepatitis B and D Protocols

Part of the book series: Methods in Molecular Medicine™ ((MIMM,volume 96))

Abstract

Efforts to control the global pandemic of human hepatitis B virus (hHBV) infection have been hampered by incomplete understanding of viral-host interactions in this disease. This situation has been confounded by the fact that hHBV has a limited host range and cannot be propagated in simple cell culture (1). Reproducible experimental infection with determination of infectivity was demonstrated in chimpanzees (Pan troglodytes), but not other primates (2–4), long before other animal models such as the woodchuck were identified. After successful inoculation of chimpanzees was reported in 1972, multiple institutions, including a multigroup collaboration between the FDA, CDC, and NIH, initiated studies to evaluate them as a model for the study of HBV. For the majority of studies only chimpanzees “with no prior exposure” to virus were used because those with positive serology [either from exposure to hHBV or chimpanzee HBV (chHBV)], with an estimated prevalence of 3–6% in Africa (5), were not reproducibly susceptible to infection (3). It has been widely reported that the effects of HBV infection in chimpanzees are milder than in humans, that is, few have developed fulminant hepatitis, and inoculated chimpanzees exhibit few symptoms or signs of infection. Furthermore, the incidence of chronic infection with HBV (see Table 2) and horizontal and vertical transmission (from mother to offspring) in chimpanzees is lower than in humans (6,7). Chimpanzees have been the cornerstone of all research on infectivity of HBV and safety and efficacy of vaccines.

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References

  1. Deinhardt, F. (1976) Hepatitis in primates. Adv. Virus Res. 20, 113–57.

    Article  PubMed  CAS  Google Scholar 

  2. Prince, A.M. (1972) Infection of chimpanzees with hepatitis B virus, in Hepatitis and Blood Transfusion (Vyas, G. N., Perkins, H. A., and Schmid, R. S., eds.) Grune and Stratton, New York.

    Google Scholar 

  3. Maynard, J.E., Berquist, K.R., and Krushak, D.H. (1972) Experimental infection of chimpanzees with the virus of hepatitis B. Nature 237, 514–515.

    Article  PubMed  CAS  Google Scholar 

  4. Barker, L.F., Chisari, F. V., McGrath, P. P., et al. (1973) Transmission of type B viral hepatitis to chimpanzees. J. Infect. Dis. 127, 648–662.

    Article  PubMed  CAS  Google Scholar 

  5. Desmyter, J., Liu, W. T., de Somer, P., and Mortelmans, J. (1973) Primates as model for human viral hepatitis: transmission of infection by human hepatitis B virus. Vox Sang. 24, 17–26.

    Article  PubMed  Google Scholar 

  6. Prince, A. M., Goodall, J., Brotman, B., Dienske, H., and Schellekens, H., and Eichberg, J. W. (1989) Appropriate conditions for maintenance of chimpanzees in studies with blood-borne viruses: an epidemiologic and psychosocial perspective. J. Med. Primatol. 18, 27–42.

    PubMed  CAS  Google Scholar 

  7. Pancholi, P., Lee, D. H., Liu, Q., et al. (2001) DNA prime/canarypox boost-based immunotherapy of chronic hepatitis B virus infection in a chimpanzee. Hepatology 33, 448–454.

    Article  PubMed  CAS  Google Scholar 

  8. Tabor, E. (1985) Chimpanzee model for the study of hepatitis B, in Hepatitis B (Gerety, R. J., ed.), Academic Press, Orlando, FL.

    Google Scholar 

  9. Karasawa, T., Shikata, T., Abe, K., Kondo, R., Noro, M., and Oda, T. (1985) Ultrastructural studies on liver cell necrosis and lymphocytes in experimental hepatitis B. Acta Pathol. Jpn. 35, 1359–1374.

    PubMed  CAS  Google Scholar 

  10. Karasawa, T., Shikata, T., Abe, K., Kanayama, S., Kondo, R., and Oda, T. (1985) Ultrastructural changes of the bile secretory apparatus and bile ductule in experimental hepatitis B with neither apparent biochemical nor light-microscopic cholestasis. Acta Pathol. Jpn. 35, 1343–1358.

    PubMed  CAS  Google Scholar 

  11. Karasawa, T., Shikata, T., Abe, K., Kanayama, S., Noro, M., and Oda, T. (1985) HBV-associated ultrastructures in the chimpanzees’ livers with experimental hepatitis B. Acta Pathol. Jpn. 35, 1333–1342.

    PubMed  CAS  Google Scholar 

  12. Krawczynski, K., Prince, A.M., and Nowoslawski, A. (1979) Immunopathologic aspects of the HBsAg carrier state in chimpanzees. J. Med. Primatol. 8, 222–232.

    PubMed  CAS  Google Scholar 

  13. Shouval, D., Chakraborty, P. R., Ruiz-Opazo, N., et al. (1980) Chronic hepatitis in chimpanzee carriers of hepatitis B virus: morphologic, immunologic, and viral DNA studies. Proc. Natl. Acad. Sci. USA 77, 6147–6151.

    Article  PubMed  CAS  Google Scholar 

  14. Dienes, H. P., Purcell, R.H., Popper, H., and Ponzetto, A. (1990) The significance of infections with two types of viral hepatitis demonstrated by histologic features in chimpanzees. J. Hepatol. 10, 77–84.

    Article  PubMed  CAS  Google Scholar 

  15. Omata, M. (1990) Significance of extrahepatic replication of hepatitis B virus. Hepatology 12, 364–366.

    Article  PubMed  CAS  Google Scholar 

  16. Lieberman, H. M., Tung, W. W., and Shafritz, D. A. (1987) Splenic replication of hepatitis B virus in the chimpanzee chronic carrier. J. Med. Virol. 21, 347–359.

    Article  PubMed  CAS  Google Scholar 

  17. Penna, A., Artini, M., Cavalli, A., et al. (1996) Long-lasting memory T cell responses following self-limited acute hepatitis B. J. Clin. Invest. 98, 1185–1194.

    Article  PubMed  CAS  Google Scholar 

  18. Tabor, E., Hsia, C.C., and Muchmore, E. (1996) Histochemical and immunohistochemical similarities between hepatic tumors in two chimpanzees and man. J. Med. Primatol. 23, 271–279.

    Article  Google Scholar 

  19. Millman, I., Loeb, L.A., Bayer, M.E., and Blumberg, B. S. (1970) Australia antigen (a hepatitis-associated antigen): purification and physical properties. J. Exp. Med. 131, 1190–1199.

    Article  PubMed  CAS  Google Scholar 

  20. Smetana, H. F. and Felsenfeld, A. D. (1969) Viral hepatitis in subhuman primates and its relationship to human viral hepatitis. Virchows Arch. A Pathol. Pathol. Anat. 348, 309–327.

    Article  PubMed  CAS  Google Scholar 

  21. Hillis, W.D. (1971) An outbreak of infectious hepatitis among chimpanzee handlers at a United States Air Force base. Am. J. Hyg. 73, 316–328.

    Google Scholar 

  22. Deinhardt, F. (1976) Hepatitis in primates. Adv. Virus Res. 20, 113–157.

    Article  PubMed  CAS  Google Scholar 

  23. Rivers, S.L. and Keeling, M. (1970) A study of the incidence of Australia antigen and antibody in nonhuman primates. Vox Sang. 19, 270–272.

    Article  PubMed  CAS  Google Scholar 

  24. Morin, P. A., Moore, J.J., Chakraborty, R., Jin, L., Goodall, J., and Woodruff, D.S. (1994) Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265, 1193–1201.

    Article  PubMed  CAS  Google Scholar 

  25. Hu, X., Javadian, A, Gagneux, P., and Robertson, B.H. (2001) Paired chimpanzee hepatitis B virus (ChHBV) and mtDNA sequences suggest different ChHBV genetic variants are found in geographically distinct chimpanzee subspecies. Virus Res. 79, 103–108.

    Article  PubMed  CAS  Google Scholar 

  26. Gagneux, P., Gonder, M.K., Goldberg TL, Morin PA. (2001) Gene flow in wild chimpanzee populations: what genetic data tell us about chimpanzee movement over space and time. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 889–897.

    Article  PubMed  CAS  Google Scholar 

  27. Rahm, U. (1967) Observations during chimpanzee captures in the Congo. In Neue Ergebnisse der Primatologie-Progress in Primatology. (Starck, D., Schneider, R., and Kuhn, H. J., eds.), Fischer, Stuttgart, pp. 195–207.

    Google Scholar 

  28. Krugman, S. (1971) Experiments at the Willowbrook State School. Lancet 1, 966–967.

    Article  PubMed  CAS  Google Scholar 

  29. Barker, L. F., Maynard, J.E., Purcell, R. H., Hoofnagle, J.H., Berquist, K. R., and London, W. T. (1975) Viral hepatitis, type B, in experimental animals. Am. J. Med. Sci. 270, 189–195.

    Article  PubMed  CAS  Google Scholar 

  30. Liang, T. J., Blum, H. E., and Wands, J. R. (1990) Characterization and biological properties of a hepatitis B virus isolated from a patient without hepatitis B virus serologic markers. Hepatology 2, 204–212.

    Article  Google Scholar 

  31. Chen, P.J., Chen, M.L., and Chen, D.S. (1994) A viral mechanism in acute exacerbations of chronic type B hepatitis: hepatitis B virus reinfection and subsequent reactivation of two viral strains. J. Biomed. Sci. 1, 7–12.

    Article  PubMed  CAS  Google Scholar 

  32. Deinhardt, F., Courtois, G., Oberle, P., et al. (1962) Studies on liver function tests in chimpanzees after inoculation with infectious hepatitis virus. Am. J. Hyg. 75, 311–321.

    PubMed  CAS  Google Scholar 

  33. Ogata, N., Miller, R. H., Ishak, K.G., and Purcell, R. H. (1993) The complete nucleotide sequence of a pre-core mutant of hepatitis B virus implicated in fulminant hepatitis and its biological characterization in chimpanzees. Virology 194, 263–276.

    Article  PubMed  CAS  Google Scholar 

  34. Lanford, R. E., Bigger, C., Bassett, S., and Klimpel, G. (2001) The chimpanzee model of hepatitis C virus infections. ILAR J. 42, 117–126.

    PubMed  CAS  Google Scholar 

  35. Tabor, E., Aronson, D. L., and Gerety, R. J. (1980) Removal of hepatitis-B-virus infectivity from factor-IX complex by hepatitis-B immune-globulin. Experiments in chimpanzees. Lancet 2, 68–70.

    Article  PubMed  CAS  Google Scholar 

  36. Brummelhuis, H. G., Over, J., Duivis-Vorst, C. C., et al. (1983) Contributions to the optimal use of human blood. IX. Elimination of hepatitis B transmission by (potentially) infectious plasma derivatives. Vox Sang. 45, 205–216.

    Article  PubMed  CAS  Google Scholar 

  37. Stephan, W., Berthold, H., and Prince, A.M. (1981) Effect of combined treatment of serum containing hepatitis B virus with beta-propiolactone and ultraviolet irradiation. Vox Sang. 41, 134–138.

    Article  PubMed  CAS  Google Scholar 

  38. Tabor, E., Buynak, E., Smallwood, L. A., Snoy, P., Hilleman, M., and Gerety, R.J. (1983) Inactivation of hepatitis B virus by three methods: treatment with pepsin, urea, or formalin. J. Med. Virol. 11, 1–9.

    Article  PubMed  CAS  Google Scholar 

  39. Vnek, J., Prince, A.M., Hashimoto, N., and Ikram, H. (1978) Association of normal serum protein antigens with chimpanzee hepatitis B surface antigen particles. J. Med. Virol. 2, 319–333.

    Article  PubMed  CAS  Google Scholar 

  40. Prince, A. M., Stephan, W., Kotitschke, R., and Brotman, B. (1983) Inactivation of hepatitis B and non-A, non-B viruses by combined use of Tween 80, beta-propiolactone, and ultraviolet irradiation. Thromb. Haemost. 50, 534–536.

    PubMed  CAS  Google Scholar 

  41. Prince, A. M., Stephan, W., and Brotman, B. (1983) Beta-propiolactone/ultraviolet irradiation: a review of its effectiveness for inactivation of viruses in blood derivatives. Rev. Infect. Dis. 5, 92–107.

    Article  PubMed  CAS  Google Scholar 

  42. Feinstone, S. M., Mihalik, K. B., Kamimura, T., Alter, H. J., London, W. T., and Purcell, R. H. (1983) Inactivation of hepatitis B virus and non-A, non-B hepatitis by chloroform. Infect. Immun. 41, 816–821.

    PubMed  CAS  Google Scholar 

  43. Prince, A.M., Horowitz, B., Brotman, B., Huima, T., Richardson, L., and van den Ende, M. C. (1984) Inactivation of hepatitis B and Hutchinson strain non-A, non-B hepatitis viruses by exposure to Tween 80 and ether. Vox Sang. 46, 36–43.

    Article  PubMed  CAS  Google Scholar 

  44. Kobayashi, H., Tsuzuki, M., Koshimizu, K., et al. (1984) Susceptibility of hepatitis B virus to disinfectants or heat. J. Clin. Microbiol. 20, 214–216.

    PubMed  CAS  Google Scholar 

  45. Hollinger, F. B., Dolana, G., Thomas, W., and Gyorkey, F. (1984) Reduction in risk of hepatitis transmission by heat-treatment of a human factor VIII concentrate. J. Infect. Dis. 150, 250–262.

    Article  PubMed  CAS  Google Scholar 

  46. Purcell, R.H., Gerin, J. L., Popper, H., et al. (1985) Hepatitis B virus, hepatitis non-A, non-B virus and hepatitis delta virus in lyophilized antihemophilic factor: relative sensitivity to heat. Hepatology 5, 1091–1099.

    Article  PubMed  CAS  Google Scholar 

  47. Lelie, P.N., Reesink, H. W., Niessen, J., Brotman, B., and Prince, A. M. (1987) Inactivation of 10(15) chimpanzee-infectious doses of hepatitis B virus during preparation of a heatinactivated hepatitis B vaccine. J. Med. Virol. 23, 289–295.

    Article  PubMed  CAS  Google Scholar 

  48. Zolton, R. P., Padvelskis, J. V., and Kaplan, P.M. (1985) Removal of hepatitis B virus infectivity from human gamma-globulin prepared by ion-exchange chromatography. Vox Sang. 49, 381–389.

    Article  PubMed  CAS  Google Scholar 

  49. Alter, H.J., Creagan, R. P., Morel, P. A., et al. (1988) Photochemical decontamination of blood components containing hepatitis B and non-A, non-B virus. Lancet 2, 1446–1450.

    Article  PubMed  CAS  Google Scholar 

  50. Prince, D.L., Prince, H. N., Thraenhart, O., Muchmore, E., Bonder, E., and Pugh, J. (1993) Methodological approaches to disinfection of human hepatitis B virus. J. Clin. Microbiol. 31, 3296–3304.

    PubMed  CAS  Google Scholar 

  51. Maynard, J.E., Krushak, D. H., Bradley, D. W., and Berquist, K.R. (1975) Infectivity studies of hepatitis A and B in non-human primates. Dev. Biol. Stand. 30, 229–235.

    PubMed  CAS  Google Scholar 

  52. Krugman, S. (1975) Viral hepatitis type B: prospects for active immunization. Am. J. Med. Sci. 270, 391–393.

    Article  PubMed  CAS  Google Scholar 

  53. Drucker, J., Tabor, E., Gerety, R. J., Jackson, D., and Barker L. F. (1979) Simultaneous acute infections with hepatitis A and hepatitis B virus viruses in a chimpanzee. J. Infect. Dis. 139, 338–342.

    Article  PubMed  CAS  Google Scholar 

  54. Bradley, D.W., Maynard, J.E., McCaustland, K.A., Murphy, B.L., Cook, E.H., and Ebert, J. W. (1983) Non-A, non-B hepatitis in chimpanzees: interference with acute hepatitis A virus and chronic hepatitis B virus infections. J. Med. Virol. 11, 207–213.

    Article  PubMed  CAS  Google Scholar 

  55. Brotman, B., Prince, A.M., Huima, T., Richardson, L., van den Ende, M. C., and Pfeifer, U. (1983) Interference between non-A, non-B and hepatitis B virus infection in chimpanzees. J. Med. Virol. 11, 191–205.

    Article  PubMed  CAS  Google Scholar 

  56. Kos, T., Molijn, A., van Doorn, L.J., van Belkum, A., Dubbeld, M., and Schellekens, H. (1991) Hepatitis delta virus cDNA sequence from an acutely HBV-infected chimpanzee: sequence conservation in experimental animals. J. Med. Virol. 34, 268–279.

    Article  PubMed  CAS  Google Scholar 

  57. Wilson, S. and Logan, L.M. (1975) Hepatitis B core antigen in the immunosuppressed chimpanzee. Dev. Biol. Stand. 30, 240–243.

    PubMed  CAS  Google Scholar 

  58. Trepo, C., Vnek, J., and Prince, A. M. (1975) Delayed hypersensitivity and Arthus reaction to purified hepatitis B surface antigen (HBsAg) in immunized chimpanzees. Clin. Immunol. Immunopathol. 4, 528–537.

    Article  PubMed  CAS  Google Scholar 

  59. Negro, F., Shapiro, M., Satterfield, W. C., Gerin, J.L., and Purcell, R. H. (1989) Reappearance of hepatitis D virus (HDV) replication in chronic hepatitis B virus carrier chimpanzees rechallenged with HDV. J. Infect. Dis. 160, 567–571.

    Article  PubMed  CAS  Google Scholar 

  60. Ruiz-Opazo, N., Chakraborty, P. R., and Shafritz, D. A. (1982) Characterization of viral genomes in the liver and serum of chimpanzee long-term hepatitis B virus carriers: a possible role for supercoiled HBV-DNA in persistent HBV infection. J. Cell. Biochem. 19, 281–292.

    Article  PubMed  CAS  Google Scholar 

  61. Abe, K., Kagei, N., Teramura, Y., and Ejima, H. (1993) Hepatocellular carcinoma associated with chronic Schistosoma mansoni infection in a chimpanzee. J. Med. Primatol. 22, 237–239.

    PubMed  CAS  Google Scholar 

  62. Lubeck, M.D., Davis, A.R., Chengalvala, M., et al. (1989) Immunogenicity and efficacy testing in chimpanzees of an oral hepatitis B vaccine based on live recombinant adenovirus. Proc. Natl. Acad. Sci. USA 86, 6763–6767.

    Article  PubMed  CAS  Google Scholar 

  63. Fujisawa, Y., Kuroda, S., Van Eerd, P.A.C.M., Schellekens, H., and Kakinuma, A. (1990) Protective efficacy of a novel hepatitis B vaccine consisting of M (pre S2+S) protein particles (a third generation vaccine). Vaccine 8, 192–198.

    Article  PubMed  CAS  Google Scholar 

  64. Purcell, R. H., Gerin, J.L. (1975) Hepatitis B subunit vaccine: a preliminary report of safety and efficacy tests in chimpanzees. Am. J. Med. Sci. 270, 395–399.

    Article  PubMed  CAS  Google Scholar 

  65. Purcell, R. H., London, W. T., McAuliffe, V.J., et al. (1976) Modification of chronic hepatitis-B virus infection in chimpanzees by administration of an interferon inducer. Lancet 2, 757–761.

    Article  PubMed  CAS  Google Scholar 

  66. Hilleman, M.R., Buynak, E.B., Roehm, R.R., et al. (1975) Purified and inactivated human hepatitis B vaccine: progress report. Am. J. Med. Sci. 270, 401–404.

    Article  PubMed  CAS  Google Scholar 

  67. Gerety, R. J., Tabor, E., Purcell R. H., and Tyeryar, F.J. (1979) Summary of an international workshop on hepatitis B vaccines. J. Infect. Dis. 140, 642–648.

    Article  PubMed  CAS  Google Scholar 

  68. Iwarson, S., Tabor, E., Thomas, H. C., et al. (1985) Neutralization of hepatitis B virus infectivity by a murine monoclonal antibody: an experimental study in the chimpanzee. J. Med. Virol. 16, 89–96.

    Article  PubMed  CAS  Google Scholar 

  69. Davis, H.L., McCluskie, M.J., Gerin, J. L., and Purcell, R.H. (1996) DNA vaccine for hepatitis B: evidence for immunogenicity in chimpanzees and comparison with other vaccines. Proc. Natl. Acad. Sci. USA 93, 7213–7218.

    Article  PubMed  CAS  Google Scholar 

  70. Pancholi, P., Lee, D. H., Liu, Q., et al. (2001) DNA prime/canarypox boost-based immunotherapy of chronic hepatitis B virus infection in a chimpanzee. Hepatology 33, 448–454.

    Article  PubMed  CAS  Google Scholar 

  71. Sällberg, M., Hughes, J., Javadian, A., et al. (1998) Genetic immunization of chimpanzees chronically infected with the hepatitis B virus, using a recombinant retroviral vector encoding the hepatitis B virus core antigen. Hum. Gene Ther. 9, 1719–1729.

    Article  PubMed  Google Scholar 

  72. Prince, A. M., Lee, D. H., and Brotman, B. (2001) Infectivity of blood from PCR-positive, HBsAg-negative, anti-HBs-positive cases of resolved hepatitis B infection. Transfusion (3), 329–332.

    Article  Google Scholar 

  73. Kremsdorf, D., Garreau, F., Duclos, H., et al. (1993) Complete nucleotide sequence and viral envelope protein expression of a hepatitis B virus DNA derived from a hepatitis B surface antigen-seronegative patient. J. Hepatol. 18, 244–250.

    Article  PubMed  CAS  Google Scholar 

  74. Bock, C-T., Tillman, H.L., Maschek, H-J., Manns, M.P., and Trautwein, C. (1982) A PreS mutation isolated from a patient with chronic hepatitis B infection leads to virus retention and misassembly. Gastroenterology 113, 1996–1982.

    Google Scholar 

  75. Shikata, T., Karasawa, T., and Abe, K. (1980) Two distinct types of hepatitis in experimental hepatitis B virus infection. Am. J. Pathol. 99, 353–363.

    PubMed  CAS  Google Scholar 

  76. Federal News Service, (2000) Hearing of the Health and Environment Subcommittee of the House Commerce Committee: Chimpanzees and Biomedical Research, chaired by Rep. Michael Bilirakis (18 May).

    Google Scholar 

  77. Hu, X., Margolis, H.S., Purcell, R. H., Ebert, J., and Robertson, B.H. (2000) Identification of hepatitis B virus indigenous to chimpanzees. Proc. Natl. Acad. Sci. USA 97, 1661–1664.

    Article  PubMed  CAS  Google Scholar 

  78. Takahashi, K., Brotman, B., Usuda, S., Mishiro, S., and Prince, A. M. (2000) Full-genome sequence analyses of hepatitis B virus (HBV) strains recovered from chimpanzees infected in the wild: implications for an origin of HBV. Virology 267, 58–64.

    Article  PubMed  CAS  Google Scholar 

  79. MacDonald, D.M., Holmes, E.C., Lewis, J.C., and Simmonds, P. (2000) Detection of hepatitis B virus infection in wild-born chimpanzees (Pan troglodytes verus): phylogenetic relationships with human and other primate genotypes. J. Virol. 74, 4253–4257.

    Article  PubMed  CAS  Google Scholar 

  80. Vartanian, J-P., Pineau, P., Henry, M., et al. (2002) Identification of a hepatitis B virus genome in wild chimpanzees (Pan troglodytes schweinfurth:) from East Africa indicates a wide geographical dispersion among equatorial African primates. J. Virol. 76, 11,155–11,158.

    Article  PubMed  CAS  Google Scholar 

  81. Zuckerman, A.J., Thornton, A., Howard, C.R., Tsiquaye, K.N., Jones, D.M., and Brambell, M. R. (1978) Hepatitis B outbreak among chimpanzees at the London Zoo. Lancet 2, 652–654.

    Article  PubMed  CAS  Google Scholar 

  82. Vaudin, M., Wolstenholme, A. J., Tsiquaye, K.N., Zuckerman, A. J., and Harrison, T.J. (1989) The complete nucleotide sequence of the genome of a hepatitis B virus isolated from a naturally infected chimpanzee. J. Gen. Virol. 69, 1383–1389.

    Article  Google Scholar 

  83. Grethe, S., Heckel, J.O., Rietschel, W., and Hufert, F.T. (2000) Molecular epidemiology of hepatitis B virus variants in nonhuman primates. J. Virol. 74, 5377–5381.

    Article  PubMed  CAS  Google Scholar 

  84. Norder, H., Ebert, J.W., Fields, H.A., Mushahwar, I.K., and Magnius, L.O. (1996) Complete sequencing of a gibbon hepatitis B virus genome reveals a unique genotype distantly related to the chimpanzee hepatitis B virus. Virology 218, 214–223.

    Article  PubMed  CAS  Google Scholar 

  85. Fares, M.A., and Holmes, E. C. (2002) A revised evolutionary history of hepatitis B virus (HBV) J. Mol. Evol. 54, 807–814.

    Article  PubMed  CAS  Google Scholar 

  86. Lanford, R. E., Chavez, D., Brasky, K. M., Burns, R. B. 3rd, and Rico-Hesse, R. (1998) Isolation of a hepadnavirus from the woolly monkey, a New World primate. Proc. Natl. Acad. Sci. USA 95, 5757–5761.

    Article  PubMed  CAS  Google Scholar 

  87. Ghany, M.G., Ayola, B., Villamil, F. G., et al. (1998) Hepatitis B virus S mutants in liver transplant recipients who were reinfected despite hepatitis B immune globulin prophylaxis. Hepatology 27, 213–222.

    Article  PubMed  CAS  Google Scholar 

  88. Bowyer, S.M., and Sim, J.G. (2000) Relationships within and between genotypes of hepatitis B virus at points across the genome: footprints of recombination in certain isolates. J. Gen. Virol. 81(Pt 2), 379–392.

    PubMed  CAS  Google Scholar 

  89. Hannoun, C., Norder, H., and Lindh, M.(2000) An aberrant genotype revealed in recombinant hepatitis B virus strains from Vietnam. J. Gen. Virol. 81(Pt 9), 2267–2272.

    PubMed  CAS  Google Scholar 

  90. Kils-Hutten, L., Cheynier, R., Wain-Hobson, S., and Meyerhans, A. (2001) Phylogenetic reconstruction of intrapatient evolution of human immunodeficiency virus type 1: predominance of drift and purifying selection. J. Gen. Virol. 82(Pt 7), 1621–1627.

    PubMed  CAS  Google Scholar 

  91. Bollyky, P.L. and Holmes, E. C. (1999) Reconstructing the complex evolutionary history of hepatitis B virus. J. Mol. Evol. 49, 130–141.

    Article  PubMed  CAS  Google Scholar 

  92. Sibley, C.G., and Ahlquist, J. E. (1984) The phylogeny of the hominoid primates, as indicated by DNA-DNA hybridization. J. Mol. Evol. 20, 2–15.

    Article  PubMed  CAS  Google Scholar 

  93. Chen, F.C., and Li, W.H. (2001) Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am. J. Hum. Genet. 68, 444–456.

    Article  PubMed  CAS  Google Scholar 

  94. Hodson, H. H., Jr., Lee, B.D., Wisecup, W. G., and Fineg, J. (1967) Baseline blood values of the chimpanzee. I. The relationship of age and sex and hematological values. Folia Primatol. (Basel) 7, 1–11.

    Article  Google Scholar 

  95. Adams, E.J., and Parham, P. (2001) Species-specific evolution of MHC class I genes in the higher primates. Immunol. Rev. 183, 41–64.

    Article  PubMed  CAS  Google Scholar 

  96. Adams, E.J., Cooper, S., Thomson, G., and Parham, P. (2000) Common chimpanzees have greater diversity than humans at two of the three highly polymorphic MHC class I genes. Immunogenetics 51, 410–424.

    Article  PubMed  CAS  Google Scholar 

  97. McAdam, S.N., Boyson, J.E., Liu, X., et al. (1995) Chimpanzee MHC class I A locus alleles are related to only one of the six families of human A locus alleles. J. Immunol. 154, 6421–6429.

    PubMed  CAS  Google Scholar 

  98. de Groot, N. G., Otting, N., Arguello, R., et al. (2000) Major histocompatibility complex class I diversity in a West African chimpanzee population: implications for HIV research. Immunogenetics 51, 398–409.

    Article  PubMed  Google Scholar 

  99. de Groot, N. G., Otting, N., Doxiadis, G. G. M., et al. (2002) An ancient selective sweep in the MHC class I gene repertoire of chimpanzees. Proc. Natl. Acad. Sci. USA 99, 11748–11753.

    Article  PubMed  CAS  Google Scholar 

  100. Bertoni, R., Sette, A., Sidney, J., et al. (1998) Human class I supertypes and CTL repertoires extend to chimpanzees. J. Immunol. 161, 4447–4455.

    PubMed  CAS  Google Scholar 

  101. Bontrop, R.E., Otting, N., de Groot, N. G., and Doxiadis, G. G. (1999) Major histocompatibility complex class II polymorphisms in primates. Immunol Rev. 167, 339–350.

    Article  PubMed  CAS  Google Scholar 

  102. Balla-Jhagjhoorsingh, S.S., Koopman, G., Mooij, P., et al. (1999) Conserved CTL epitopes shared between HIV-infected human long-term survivors and chimpanzees. J. Immunol. 162, 2308–2314.

    PubMed  CAS  Google Scholar 

  103. Andrieu, M., Chassin, D., Desoutter, J. F., et al. (2001) Downregulation of major histocom-patibility class I on human dendritic cells by HIV Nef impairs antigen presentation to HIV-specific CD8+ T lymphocytes. AIDS Res. Hum. Retroviruses 17, 1365–1370.

    Article  PubMed  CAS  Google Scholar 

  104. Adams E.J., Cooper, S., and Parham, P. (2001) A novel, nonclassical MHC class I molecule specific to the common chimpanzee. J. Immunol. 167, 3858–3869.

    PubMed  CAS  Google Scholar 

  105. Khakoo, S.I., Rajalingam, R., Shum, B. P., et al. (2000) Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12, 687–698.

    Article  PubMed  CAS  Google Scholar 

  106. Muchmore, E. A., Diaz, S., and Varki, A. (1998) A structural difference between the cell surfaces of humans and the great apes. Am. J. Phys. Anthropol. 107, 187–198.

    Article  PubMed  CAS  Google Scholar 

  107. Brinkman-Van der Linden, E. C., Sjoberg, E.R., Juneja, L. R., Crocker, P. R., Varki, N., and Varki, A. (2000) Loss of N-glycolylneuraminic acid in human evolution. Implications for sialic acid recognition by siglecs. J. Biol. Chem. 275, 8633–8640.

    Google Scholar 

  108. Angata, T., Varki, N.M., and Varki, A. (2001) A second uniquely human mutation affecting sialic acid biology. J. Biol. Chem. 276, 40282–40287.

    PubMed  CAS  Google Scholar 

  109. Crocker, P.R. and Varki, A. (2001) Siglecs in the immune system. Immunology 103, 137–145.

    Article  PubMed  CAS  Google Scholar 

  110. Mehta, A., Block, T.M., and Dwek, R.A. (1998) The role of N-linked glycosylation in the secretion of hepatitis B virus. Adv. Exp. Med. Biol. 435, 195–205.

    Article  PubMed  CAS  Google Scholar 

  111. Rother, R. P. and Galili, U. (1999) Alpha-Gal epitopes on viral glycoproteins. Subcell. Biochem. 32, 143–172.

    Article  PubMed  CAS  Google Scholar 

  112. Atkins, G.J., Qiao, M., Coombe, D.R., Gowans, E.J., and Ashman, L.K. (1997) Hepatitis B virus binding to leucocyte plasma membranes utilizes a different region of the preS1 domain to the hepatocyte receptor binding site and does not require receptors for opsonins. Immunol. Cell Biol. 75, 259–266.

    Article  PubMed  CAS  Google Scholar 

  113. Budkowska, A., Quan, C., Groh, F., et al. (1993) Hepatitis B virus (HBV) binding factor in human serum: candidate for a soluble form of hepatocyte HBV receptor. J. Virol. 67, 4316–4322.

    PubMed  CAS  Google Scholar 

  114. Neurath, A. R., Kent, S.B., Strick, N., and Parker, K.(1986) Identification and chemical synthesis of a host cell receptor binding site on hepatitis B virus. Cell 46, 429–436.

    Article  PubMed  CAS  Google Scholar 

  115. Check, E. (2002) Bank wants money back from troubled chimp facility. Nature 415, 248.

    Article  PubMed  CAS  Google Scholar 

  116. Santiago, M.L., Rodenburg, C.M., Kamenya, S., et al. (2002) SIVcpz in wild chimpanzees. Science 295, 465.

    Article  PubMed  CAS  Google Scholar 

  117. Lichter, E.A. (1969) Chimpanzee antibodies to Australia antigen. Nature 224, 810–811

    Article  PubMed  CAS  Google Scholar 

  118. Maynard, J. E., Hartwell, W.V., and Berquist, K.R. (1971) Hepatitis-associated antigen in chimpanzees. J. Infect. Dis. 123, 660–664.

    Article  PubMed  CAS  Google Scholar 

  119. Lander, H.J., Holland, P. V., Alter, H. J., Chanock, R.M., and Purcell, R. H. (1972) Antibody to hepatitis-associated antigen. Frequency and pattern of response as detected by radioimmunoprecipitation. JAMA 220, 1079–1082.

    Article  PubMed  CAS  Google Scholar 

  120. Eichberg, J. W. and Kalter, S. S. (1980) Hepatitis A and B: serologic survey of human and nonhuman primate sera. Lab. Anim. Sci. 30, 541–543.

    PubMed  CAS  Google Scholar 

  121. Murphy, B.L., Maynard, J.E., and Le Bouvier, G.L. (1974) Viral subtypes and cross-protection in hepatitis B virus infections of chimpanzees. Intervirology 3, 378–81

    Article  PubMed  CAS  Google Scholar 

  122. Bradley, D.W., Maynard, J.E., Berquist, K.R., and Krushak, D.H. (1974) Hepatitis B and serum DNA polymerase activities in chimpanzees. Nature 251, 356–357.

    Article  PubMed  CAS  Google Scholar 

  123. Markenson, J.A., Gerety, R. J., Hoofnagle, J. H., and Barker, L. F. (1975) Effects of cyclophosphamide on hepatitis B virus infection and challenge in chimpanzees. J. Infect. Dis. 131, 79–87.

    Article  PubMed  CAS  Google Scholar 

  124. Berquist, K. R., Peterson, J. M., Murphy, B.L., Ebert, J. W., Maynard, J. E., and Purcell, R. H. (1975) Hepatitis B antigens in serum and liver of chimpanzees acutely infected with hepatitis B virus. Infect. Immun. 12, 602–605.

    PubMed  CAS  Google Scholar 

  125. Alter, H. J., Purcell, R. H., Gerin, J. L., et al. (1977) Transmission of hepatitis B to chimpanzees by hepatitis B surface antigen-positive saliva and semen. Infect. Immun. 16, 928–933.

    PubMed  CAS  Google Scholar 

  126. Shikata, T., Karasawa, T., Abe, K., et al. (1977) Hepatitis B e antigen and infectivity of hepatitis B virus. J. Infect. Dis. 136, 571–576.

    Article  PubMed  CAS  Google Scholar 

  127. Tabor, E., Gerety, R. J., Barker, L.F., Howard, C. R., and Zuckerman, A.J. (1978) Effect of ethanol during hepatitis B virus infection in chimpanzees. J. Med. Virol. 2, 295–303.

    Article  PubMed  CAS  Google Scholar 

  128. Ling, C. M., Mushahwar, I.K., Overby, L. R., Berquist, K. R., Maynard, J.E. (1979) Hepatitis B e-antigen and its correlation with other serological markers in chimpanzees. Infect. Immun. 24, 352–356.

    PubMed  CAS  Google Scholar 

  129. Sly, D.L., London, W.T., and Purcell, R.H. (1979) Illness in a chimpanzee inoculated with hepatitis B virus. J. Am. Vet. Med. Assoc. 175, 987–988.

    PubMed  CAS  Google Scholar 

  130. Takahashi, K., Miyakawa, Y., Gotanda, T., Mishiro, S., Imai, M., and Mayumi, M. (1979) Shift from free “small” hepatitis B e antigen to IgG-bound “large” form in the circulation of human beings and a chimpanzee acutely infected with hepatitis B virus. Gastroenterology 77, 1193–1199

    PubMed  CAS  Google Scholar 

  131. Tabor, E., Frosner, G., Deinhardt, F., and Gerety, R.J. (1980) Hepatitis B e antigen and antibody: detection by radioimmunoassay in chimpanzees during experimental hepatitis Br. J. Med. Virol. 6, 91–99

    Article  CAS  Google Scholar 

  132. Bond, W.W., Peterson, N. J., Favero, M. S., Ebert, J. W., Maynard, J. E. (1982) Transmission of type B viral hepatitis via eye inoculation of a chimpanzee. J. Clin. Microbiol. 15, 533–534.

    PubMed  CAS  Google Scholar 

  133. Will, H., Darai, G., Deinhardt, F., Schellekens, H., and Schaller, H. (1983) Hepatitis B after infection of a chimpanzee with cloned HBV DNA. Dev. Biol. Stand. 54, 131–133.

    PubMed  CAS  Google Scholar 

  134. Will, H., Cattaneo, R., Darai, G., Deinhardt, F., Schellekens, H., and Schaller, H. (1985) Infectious hepatitis B virus from cloned DNA of known nucleotide sequence. Proc. Natl. Acad. Sci. USA 82, 891–895.

    Article  PubMed  CAS  Google Scholar 

  135. Wands, J. R., Fujita, Y. K., Isselbacher, K. J., et al. (1986) Identification and transmission of hepatitis B virus-related variants. Proc. Natl. Acad. Sci. USA 83, 6608–6612

    Article  PubMed  CAS  Google Scholar 

  136. Acs, G., Sells, M.A., Purcell, R.H., et al. (1987) Hepatitis B virusvirus produced by trans-fected Hep G2 cells causes hepatitis in chimpanzees. Proc. Natl. Acad. Sci. USA 84, 4641–4644.

    Article  PubMed  CAS  Google Scholar 

  137. Sureau, C., Eichberg, J.W., Hubbard, G.B., Romet-Lemonne, J.L., and Essex, M. (1988) A molecularly cloned hepatitis B virus produced in vitro is infectious in a chimpanzee. J. Virol. 62, 3064–3067.

    PubMed  CAS  Google Scholar 

  138. Thiers, V., Nakajima, E., Kremsdorf, D., et al. (1988) Transmission of hepatitis B from hepatitis-B-seronegative subjects. Lancet 2, 1273–1276.

    Article  PubMed  CAS  Google Scholar 

  139. Shih, C., Yu, M. Y., Li, L. S., and Shih, J.W. (1990) Hepatitis B virus propagated in a rat hepatoma cell line is infectious in a primate model. Virology 179, 871–873.

    Article  PubMed  CAS  Google Scholar 

  140. Ogata, N., Zanetti, A.R., Yu, M., Miller, R. H., and Purcell, R.H. (1997) Infectivity and pathogenicity in chimpanzees of a surface gene mutant of hepatitis B virus that emerged in a vaccinated infant. J. Infect. Dis. 175, 511–523

    Article  PubMed  CAS  Google Scholar 

  141. Ibrahim, A. B., Vyas, G. N., and Prince, A.M. (1974) Studies on delayed hypersensitivity to hepatitis B antigen in chimpanzees. Clin. Exp. Immunol. 17, 311–318.

    PubMed  CAS  Google Scholar 

  142. Buynak, E.B., Roehm, R.R., Tytell, A.A., Bertland, A.U, 2nd, Lampson, G.P., and Hilleman, M.R. (1976) Vaccine against human hepatitis B. JAMA 235, 2832–2834.

    Article  PubMed  CAS  Google Scholar 

  143. Hollinger, F. B., Gitnick, G.L., Aach, R. D., et al. (1978) Non-A, non-B hepatitis transmission in chimpanzees: a project of the transfusion-transmitted viruses study group. Intervirology 10, 60–68.

    Article  PubMed  CAS  Google Scholar 

  144. Prince, A. M. (1977) Prevention of hepatitis B infections by passive immunization. Ric. Clin. Lab. 7, 198–208.

    PubMed  CAS  Google Scholar 

  145. Hilleman, M.R., Provost, P.J., Villarejos, V. M., et al. Infectious hepatitis (hepatitis A) research in nonhuman primates. Bull. Pan Am. Health Org. 11, 140–152.

    Google Scholar 

  146. Purcell, R. H. and Gerin, J. L. (1978) Hepatitis B vaccines. On the threshold. Am. J. Clin. Pathol. 70(1 Suppl), 159–169.

    PubMed  CAS  Google Scholar 

  147. Prince, A. M., Ikram, H., and Hopp, T. P. (1982) Hepatitis B virus vaccine: identification of HBsAg/a and HBsAg/d but not HBsAg/y subtype antigenic determinants on a synthetic immunogenic peptide. Proc. Natl. Acad. Sci. USA 79, 579–583.

    Article  PubMed  CAS  Google Scholar 

  148. Prince, A.M., Vnek, J., and Stephan, W. (1983) A new hepatitis B vaccine containing HBeAg in addition to HBsAg. Dev. Biol. Stand. 54, 13–22.

    PubMed  CAS  Google Scholar 

  149. Karasawa, T., Shikata, T., Abe, K., et al. (1983) Efficacy of hepatitis B vaccine in chimpanzees given transfusions of highly infective blood. J. Infect. Dis. 147, 327–335.

    Article  PubMed  CAS  Google Scholar 

  150. Tabor, E., Purcell, R. H., and Gerety, R. J.(1983) Primate animal models and titered inocula for the study of human hepatitis A, hepatitis B, and non-A, non-B hepatitis. J. Med. Primatol. 12, 305–318.

    PubMed  CAS  Google Scholar 

  151. Berthelot, P., Courouce, A.M., Eyquem, A., et al. (1984) Hepatitis B vaccine safety monitoring in the chimpanzee: interpretation of results. J. Med. Primatol. 13, 119–133.

    PubMed  CAS  Google Scholar 

  152. Moss, B., Smith, G.L., Gerin, J. L., and Purcell, R. H. (1984) Live recombinant vaccinia virus protects chimpanzees against hepatitis B. Nature 311, 67–69.

    Article  PubMed  CAS  Google Scholar 

  153. Stephan, W., Prince, A. M., and Brotman, B. (1984) Modulation of hepatitis B infection by intravenous application of an immunoglobulin preparation that contains antibodies to hepatitis B e and core antigens but not to hepatitis B surface antigen. J. Virol. 51, 420–424.

    PubMed  CAS  Google Scholar 

  154. Ohmura, T., Ohmizu, A., Sumi, A., et al. (1987) Properties of recombinant hepatitis B vaccine. Biochem. Biophys. Res. Commun. 149, 1172–1178.

    Article  PubMed  CAS  Google Scholar 

  155. Bitter, G.A., Egan, K. M., Burnette, W. N., et al. (1988) Hepatitis B vaccine produced in yeast. J. Med. Virol. 25, 123–140.

    Article  PubMed  CAS  Google Scholar 

  156. Prince, A.M., Whalen, R., and Brotman, B. (1997) Successful nucleic acid based immunization of newborn chimpanzees against hepatitis B virus. Vaccine 15, 916–919.

    Article  PubMed  CAS  Google Scholar 

  157. Pride, M.W., Bailey, C.R., Muchmore, E., and Thanavala, Y. (1998) Evaluation of B and T-cell responses in chimpanzees immunized with Hepagene, a hepatitis B vaccine containing pre-S1, pre-S2 gene products. Vaccine 16, 543–550.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Departments of Medicine and Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA

    Pascal Gagneux

  2. San Diego Veterans Administration Medical Center and Department of Medicine, University of California, San Diego, La Jolla, CA

    Elaine A. Muchmore

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  1. Pascal Gagneux
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  2. Elaine A. Muchmore
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  1. Ribapharm Inc., Costa Mesa, CA

    Robert K. Hamatake PhD  & Johnson Y. N. Lau MD  & 

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Gagneux, P., Muchmore, E.A. (2004). The Chimpanzee Model. In: Hamatake, R.K., Lau, J.Y.N. (eds) Hepatitis B and D Protocols. Methods in Molecular Medicine™, vol 96. Humana Press. https://doi.org/10.1385/1-59259-670-3:289

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  • DOI: https://doi.org/10.1385/1-59259-670-3:289

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  • Print ISBN: 978-1-58829-108-0

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