1887

Abstract

A gammaherpesvirus related to Epstein–Barr virus (EBV; ) infects otherwise healthy common marmosets (). Long-term culture of common marmoset peripheral blood lymphocytes resulted in outgrowth of spontaneously immortalized lymphoblastoid cell lines, primarily of B cell lineage. Electron microscopy of cells and supernatants showed herpesvirus particles. There were high rates of serological cross-reactivity to other herpesviruses (68–86%), but with very low geometric mean antibody titres [1:12 to human herpesvirus 6 and 1:14 to Herpesvirus papio ()]. Sequence analysis of the conserved herpesvirus DNA polymerase gene showed that the virus is a member of the lymphocryptovirus subgroup and is most closely related to a lymphocryptovirus from rhesus macaques and is closely related to EBV and Herpesvirus papio. High seroprevalence (79%, with geometric mean antibody titre of 1:110) among 28 common marmosets from two geographically distinct colonies indicated that the virus is likely present in many common marmosets in captivity. A New World primate harbouring a lymphocryptovirus suggests that this subgroup arose much earlier than previously thought.

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2002-07-01
2024-12-09
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References

  1. Ablashi D. V., Pearson G., Rabin H., Armstrong G., Easton J., Valerio M., Cicmanec J. 1978; Experimental infection of Callithrix jacchus marmosets with Herpesvirus ateles, Herpesvirus saimiri, and Epstein Barr virus. Biomedicine 29:7–10
    [Google Scholar]
  2. Apolloni A., Sculley T. B. 1994; Detection of A-type and B-type Epstein-Barr virus in throat washings and lymphocytes. Virology 202:978–981
    [Google Scholar]
  3. Baer R., Bankier A. T., Biggin M. D., Deininger P. L., Farrell P. J., Gibson T. J., Hatfull G., Hudson G. S., Satchwell S. C., Séguin C., Tuffnell P. S., Barrell B. G. 1984; DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature 310:207–211
    [Google Scholar]
  4. Brown N. A., Kovacs A., Lui C. R., Hur C., Zaia J. A., Mosley J. W. 1988; Prevalence of antibody to human herpesvirus 6 among blood donors infected with HIV. Lancet ii:1146
    [Google Scholar]
  5. Cho Y., Ramer J., Rivailler P., Quink C., Garber R. L., Beier D. R., Wang F. 2001; An Epstein-Barr-related herpesvirus from marmoset lymphomas. Proceedings of the National Academy of Sciences, USA 98:1224–1229
    [Google Scholar]
  6. Cox C., Chang S., Karran L., Griffin B., Wedderburn N. 1996; Persistent Epstein–Barr virus infection in the common marmoset ( Callithrix jacchus ). Journal of General Virology 77:1173–1180
    [Google Scholar]
  7. Cox C., Naylor B. A., Mackett M., Arrand J. R., Griffin B. E., Wedderburn N. 1998; Immunization of common marmosets with Epstein-Barr virus (EBV) envelope glycoprotein gp340: effect on viral shedding following EBV challenge. Journal of Medical Virology 55:255–261
    [Google Scholar]
  8. Deinhardt F., Falk L., Wolfe L. G., Schudel A., Nonoyama M., Lai P., Lapin B., Yakovleva L. 1978; Susceptibility of marmosets to Epstein-Barr virus-like baboon herpesviruses. Primates in Medicine 10:163–170
    [Google Scholar]
  9. de-Thé G., Dubouch P., Fontaine C., Wedderburn N., Carter R. L., Edwards M. B., Cohen B. 1980; Natural antibodies to EBV-VCA antigens in common marmosets ( Callithrix jacchus ) and response after EBV inoculation. Intervirology 14:284–291
    [Google Scholar]
  10. Emini E. A., Luka J., Armstrong M. E., Banker F. S., Provost P. J., Pearson G. R. 1986; Establishment and characterization of a chronic infectious mononucleosislike syndrome in common marmosets. Journal of Medical Virology 18:369–379
    [Google Scholar]
  11. Epstein M. A., Hunt R. D., Rabin H. 1973; Pilot experiments with EB virus in owl monkeys ( Aotus trivirgatus ). I. Reticuloproliferative disease in an inoculated animal. International Journal of Cancer 12:309–318
    [Google Scholar]
  12. Epstein M. A., Morgan A. J., Finerty S., Randle B. J., Kirkwood J. K. 1985; Protection of cottontop tamarins against Epstein-Barr virus-induced malignant lymphoma by a prototype subunit vaccine. Nature 318:287–289
    [Google Scholar]
  13. Falk L., Deinhardt F., Nonoyama M., Wolfe L. G., Bergholz C. 1976; Properties of a baboon lymphotropic herpesvirus related to Epstein-Barr virus. International Journal of Cancer 18:798–807
    [Google Scholar]
  14. Falk L. A., Henle G., Henle W., Deinhardt F., Schudel A. 1977; Transformation of lymphocytes by Herpesvirus papio. International Journal of Cancer 20:219–226
    [Google Scholar]
  15. Farrell P. J., Hollyoake M., Niedobitek G., Agathanggelou A., Morgan A., Wedderburn N. 1997; Direct demonstration of persistent Epstein–Barr virus gene expression in peripheral blood of infected common marmosets and analysis of virus-infected tissues in vivo. Journal of General Virology 78:1417–1424
    [Google Scholar]
  16. Gerber P., Pritchett R. F., Kieff E. D. 1976; Antigens and DNA of a chimpanzee agent related to Epstein-Barr virus. Journal of Virology 19:1090–1099
    [Google Scholar]
  17. Hayashi K., Koirala T. R., Ino H., Chen H. L., Ohara N., Teramoto N., Yoshino T., Takahashi K., Yamada M., Nii S. and others 1995; Malignant lymphoma induction in rabbits by intravenous inoculation of Epstein-Barr-virus-related herpesvirus from HTLV-II-transformed cynomolgus leukocyte cell line (Si-IIA). International Journal of Cancer 63:872–880
    [Google Scholar]
  18. Hayashi K., Chen H. L., Yanai H., Koirala T. R., Ohara N., Teramoto N., Oka T., Yoshino T., Takahashi K., Miyamoto K., Fujimoto K., Yoshikawa Y., Akagi T. 1999; Cyno-EBV (EBV-related herpesvirus from cynomolgus macaques) induces rabbit malignant lymphomas and their tumor cell lines frequently show specific chromosomal abnormalities. Laboratory Investigation 79:823–835
    [Google Scholar]
  19. Higashi K., Asada H., Kurata T., Ishikawa K., Hayami M., Spriatna Y., Sutarman & Yamanishi K. 1989; Presence of antibody to human herpesvirus 6 in monkeys. Journal of General Virology 70:3171–3176
    [Google Scholar]
  20. Jenson H. B. 2000; Leiomyoma and leiomyosarcoma. In Infectious Causes of Cancer: Targets for Intervention. pp 145–159 Edited by Goedert J. J. Totowa, NJ: Humana Press;
  21. Jenson H. B., Ench Y. 2002; Epstein-Barr virus. In Manual of Clinical Laboratory Immunology pp 615–626 Edited by Rose N. R., Hamilton R. G., Detrick B. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  22. Jenson H. B., Montalvo E. A., McClain K. L., Ench Y., Heard P., Christy B. A., Dewalt-Hagan P. J., Moyer M. P. 1999; Characterization of natural Epstein-Barr virus infection and replication in smooth muscle cells from a leiomyosarcoma. Journal of Medical Virology 57:36–46
    [Google Scholar]
  23. Jenson H. B., Ench Y., Gao S. J., Rice K., Carey D., Kennedy R. C., Arrand J. R., Mackett M. 2000; Epidemiology of herpesvirus papio infection in a large captive baboon colony: similarities to Epstein-Barr virus infection in humans. Journal of Infectious Diseases 181:1462–1466
    [Google Scholar]
  24. Kalter S. S., Heberling R. L., Ratner J. J. 1972; EBV antibody in sera of non-human primates. Nature 238:353–354
    [Google Scholar]
  25. Katz B. Z., Salimi B., Saini U., McNamara J. G., Eisen R. 1994; Epstein-Barr virus-infected marmoset cells do not form lymphomas in mice with severe combined immunodeficiency. Pediatric Research 36:456–460
    [Google Scholar]
  26. Landon J. C., Ellis L. B., Zeve V. H., Fabrizio D. P. 1968; Herpes-type virus in cultured leukocytes from chimpanzees. Journal of the National Cancer Institute 40:181–192
    [Google Scholar]
  27. Lennette E. T. 1995; Epstein-Barr virus (EBV). In Diagnostic Procedures for Viral, Rickettsial, and Chlamydial Infections. pp 299–312 Edited by Lennette E. H., Lennette D. A., Lennette E. T. Washington, DC: American Public Health Association;
  28. Levy J. A., Levy S. B., Hirshaut Y., Kafuko G., Prince A. 1971; Presence of EBV antibodies in sera from wild chimpanzees. Nature 233:559–560
    [Google Scholar]
  29. Li S. L., Biberfeld P., Ernberg I. 1994; DNA of lymphoma-associated herpesvirus (HVMF1) in SIV-infected monkeys ( Macaca fascicularis ) shows homologies to EBNA-1, -2 and -5 genes. International Journal of Cancer 59:287–295
    [Google Scholar]
  30. McClain K. L., Leach C. T., Jenson H. B., Joshi V. V., Pollock B. H., Parmley R. T., DiCarlo F. J., Chadwick E. G., Murphy S. B. 1995; Association of Epstein-Barr virus with leiomyosarcomas in young people with AIDS. New England Journal of Medicine 332:12–18
    [Google Scholar]
  31. McGeoch D. J., Cook S., Dolan A., Jamieson F. E., Telford E. A. 1995; Molecular phylogeny and evolutionary timescale for the family of mammalian herpesviruses. Journal of Molecular Biology 247:443–458
    [Google Scholar]
  32. McGeoch D. J., Dolan A., Ralph A. C. 2000; Toward a comprehensive phylogeny for mammalian and avian herpesviruses. Journal of Virology 74:10401–10406
    [Google Scholar]
  33. Mackett M., Cox C., Pepper S. D., Lees J. F., Naylor B. A., Wedderburn N., Arrand J. R. 1996; Immunisation of common marmosets with vaccinia virus expressing Epstein-Barr virus (EBV) gp340 and challenge with EBV. Journal of Medical Virology 50:263–271
    [Google Scholar]
  34. Miller G., Shope T., Lisco H., Stitt D., Lipman M. 1972; Epstein-Barr virus: transformation, cytopathic changes, and viral antigens in squirrel monkey and marmoset leukocytes. Proceedings of the National Academy of Sciences, USA 69:383–387
    [Google Scholar]
  35. Moghaddam A., Rosenzweig M., Lee-Parritz D., Annis B., Johnson R. P., Wang F. 1997; An animal model for acute and persistent Epstein-Barr virus infection. Science 276:2030–2033
    [Google Scholar]
  36. Moghaddam A., Koch J., Annis B., Wang F. 1998; Infection of human B lymphocytes with lymphocryptoviruses related to Epstein-Barr virus. Journal of Virology 72:3205–3212
    [Google Scholar]
  37. Nemerow G. R., McNaughton M. E., Cooper N. R. 1985; Monoclonal antibody to the Epstein-Barr virus receptor induces human B lymphocyte activation and differentiation. Transactions of the Association of American Physicians 98:290–300
    [Google Scholar]
  38. Neubauer R. H., Rabin H., Strnad B. C., Nonoyama M., Nelson-Rees W. A. 1979; Establishment of a lymphoblastoid cell line and isolation of an Epstein-Barr-related virus of gorilla origin. Journal of Virology 31:845–848
    [Google Scholar]
  39. Niedobitek G., Meru N., Delecluse H. J. 2001; Epstein-Barr virus infection and human malignancies. International Journal of Experimental Pathology 82:149–170
    [Google Scholar]
  40. Rabin H., Neubauer R. H., Hopkins R. F., Dzhikidze E. K., Shevtsova Z. V., Lapin B. A. 1977; Transforming activity and antigenicity of an Epstein-Barr-like virus from lymphoblastoid cell lines of baboons with lymphoid disease. Intervirology 8:240–249
    [Google Scholar]
  41. Rabin H., Neubauer R. H., Hopkins R. F., Nonoyama M. 1978; Further characterization of a herpesvirus-positive orangutan cell line and comparative aspects of in vitro transformation with lymphotropic old world primate herpesviruses. International Journal of Cancer 21:762–767
    [Google Scholar]
  42. Ramer J. C., Garber R. L., Steele K. E., Boyson J. F., O′Rourke C., Thomson J. A. 2000; Fatal lymphoproliferative disease associated with a novel gammaherpesvirus in a captive population of common marmosets. Comparative Medicine 50:59–68
    [Google Scholar]
  43. Rangan S. R., Martin L. N., Bozelka B. E., Wang N., Gormus B. J. 1986; Epstein-Barr virus-related herpesvirus from a rhesus monkey ( Macaca mulatta ) with malignant lymphoma. International Journal of Cancer 38:425–432
    [Google Scholar]
  44. Rickinson A. B., Young L. S., Rowe M. 1987; Influence of the Epstein-Barr virus nuclear antigen EBNA 2 on the growth phenotype of virus-transformed B cells. Journal of Virology 61:1310–1317
    [Google Scholar]
  45. Rivadeneira E. D., Ferrari M. G., Jarrett R. F., Armstrong A. A., Markham P., Birkebak T., Takemoto S., Johnson-Delaney C., Pecon-Slattery J., Clark E. A., Franchini G. 1999; A novel Epstein-Barr virus-like virus, HVMNE, in a Macaca nemestrina with mycosis fungoides. Blood 94:2090–2101
    [Google Scholar]
  46. Rivailler P., Jiang H., Cho Y. G., Quink C., Wang F. 2002; Complete nucleotide sequence of the rhesus lymphocryptovirus: genetic validation for an Epstein-Barr virus animal model. Journal of Virology 76:421–426
    [Google Scholar]
  47. Rose T. M., Strand K. B., Schultz E. R., Schaefer G., Rankin G. W. J., Thouless M. E., Tsai C. C., Bosch M. L. 1997; Identification of two homologs of the Kaposi’s sarcoma-associated herpesvirus (human herpesvirus 8) in retroperitoneal fibromatosis of different macaque species. Journal of Virology 71:4138–4144
    [Google Scholar]
  48. Salahuddin S. Z., Ablashi D. V., Markham P. D., Josephs S. F., Sturzenegger S., Kaplan M., Halligan G., Biberfeld P., Wong-Staal F., Kramarsky B., Gallo R. C. 1986; Isolation of a new virus, HBLV, in patients with lymphoproliferative disorders. Science 234:596–601
    [Google Scholar]
  49. Sixbey J. W., Shirley P., Chesney P. J., Buntin D. M., Resnick L. 1989; Detection of a second widespread strain of Epstein-Barr virus. Lancet ii:761–765
    [Google Scholar]
  50. Thorley-Lawson D. A., Nadler L. M., Bhan A. K., Schooley R. T. 1985; BLAST-2 [EBVCS], an early cell surface marker of human B cell activation, is superinduced by Epstein Barr virus. Journal of Immunology 134:3007–3012
    [Google Scholar]
  51. Wedderburn N., Edwards J. M., Desgranges C., Fontaine C., Cohen B., de The G. 1984; Infectious mononucleosis-like response in common marmosets infected with Epstein-Barr virus. Journal of Infectious Diseases 150:878–882
    [Google Scholar]
  52. Wutzler P., Meerbach A., Farber I., Wolf H., Scheibner K. 1995; Malignant lymphomas induced by an Epstein-Barr virus-related herpesvirus from Macaca arctoides – a rabbit model. Archives of Virology 140:1979–1995
    [Google Scholar]
  53. zur Hausen H., O’Neill F. J., Freese U. K., Hecker E. 1978; Persisting oncogenic herpesvirus induced by the tumour promotor TPA. Nature 272:373–375
    [Google Scholar]
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