Skip to main content
Log in

Infection of rhesus monkeys and chimpanzees with Epstein-Barr virus

  • Original Papers
  • Published:
Archives of Virology Aims and scope Submit manuscript

Summary

Seventy-two nonhuman primates were entered into a long-term study to evaluate the pathogenicity of Epstein-Barr virus (EBV). Infectious virus was inoculated into 42 rhesus monkeys, 4 chimpanzees and 1 cynomolgus monkey. Immunostimulation or immunosuppression was attempted in 34 of these animals to enhance the oncogenic potential of the virus. Eleven inoculated animals were followed for more than 3 years and two were observed for 8 years. No tumors were observed in any of the animals; however, serological evaluation of the 47 inoculated primates and 25 matched controls indicated that at least 14 rhesus monkeys and the cynomolgus monkey were successfully infected with EBV. The potential use of rhesus monkeys as a model for EBV-induced disease in humans is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Bell, T. M.: Isolation of reovirus type 3. In: Burkitt's Lymphoma, 222–230. London: E. & S. Livingstone 1970.

    Google Scholar 

  2. Burkitt, D. P.: Alymphoma syndrome in tropical Africa. Int. Rev. exp. Pathol.2, 69–126 (1963).

    Google Scholar 

  3. Churchill, A. E., Biggs, P. M.: Herpes-type virus isolated in cell culture from tumors of chickens with Marek's disease. II. Studiesin vivo. J. Natl. Cancer Inst.49, 951–956 (1968).

    Google Scholar 

  4. Cohen, M. H., Bernstein, A. D., Levine, P. H.: Hematological and serological effects of Rauscher leukemia virus and Epstein-Barr virus on immunosuppressed newborn subhuman primates. Oncology29, 353–363 (1974).

    Google Scholar 

  5. Deinhardt, F., Falk, L., Wolfe, L. G., Paciga, J., Johnson, D.: Response of marmosets to experimental infection with Epstein-Barr virus. In:Biggs, P. M., de-The, G., Payne, L. N. (eds.), Oncogenesis and Herpes viruses II, 161–167. Lyon, France: IARC Scientific Publication, No. 2 1975.

    Google Scholar 

  6. Epstein, M. A., Achong, B. G., Barr, Y. M.: Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet1, 702–703 (1964).

    Google Scholar 

  7. Epstein, M. A., Hunt, R. D., Rabin, H.: Pilot experiments with EB virus in owl monkeys (Aotus trivirgatus). I. Reticuloproliferative disease in an inoculated animal. Int. J. Cancer13, 309–318 (1973).

    Google Scholar 

  8. Falk, L., Deinhardt, F., Wolfe, L., Johnson, D., Hilgers, J., de-The, G.: Epstein-Barr virus: experimental infection ofCallithrix jacchus marmosets. Int. J. Cancer17, 785–788 (1976).

    Google Scholar 

  9. Gazdar, A. F., Russell, E., Bassin, R. H.:In vivo enhancement of a murine sarcoma virus by diethylaminoethyl-dextran. Proc. Soc. exp. Biol. Med.137, 310 to 314 (1971).

    Google Scholar 

  10. Gerber, P., Birch, S. M.: Complement-fixing antibodies in sera of human and non-human primates to viral antigens derived from Burkitt's lymphoma cells. Proc. Natl. Acad. Sci. (U.S.A.)58, 478–484 (1967).

    Google Scholar 

  11. Gerber, P., Branch, J. W., Rosenblum, E. N.: Attempts to transmit infectious mononucleosis to rhesus monkeys and marmosets and to isolate herpeslike virus. Proc. Soc. exp. Biol. Med.130, 14–19 (1969).

    Google Scholar 

  12. Gerber, P., Pritchett, R. F., Kieff, E. D.: Antigens and DNA of a chimpanzee agent related to Epstein-Barr virus. J. Virol.19, 1090–1099 (1976).

    Google Scholar 

  13. Granlund, D. J., Andrese, A. P.: Detection of Epstein-Barr virus antigens with enzyme-conjugated antibody. Int. J. Cancer20, 495–499 (1977).

    Google Scholar 

  14. Henle, G., Henle, W.: Immunofluorescence in cells derived from Burkitt's lymphoma. J. Bacteriol.91, 1248–1256 (1966).

    Google Scholar 

  15. Henle, G., Henle, W., Clifford, P.: Antibodies to Epstein-Barr virus in Burkitt's lymphoma and control groups. J. Natl. Cancer Inst.43, 1127–1157 (1969).

    Google Scholar 

  16. Henle, W., Henle, G.: Epstein-Barr virus: the cause of infectious mononucleosis—a review. In:Biggs, P. M., de-The, G., Payne, L. N. (eds.), Oncogenesis and Herpesviruses, 269–271. Lyon, France: IARC Scientific Publication, No. 2 1975.

    Google Scholar 

  17. Henle, W., Henle, G., Zajac, B. A., Pearson, G., Waubke, R., Scriba, M.: Differential reactivity of human serums with early antigens induced by Epstein-Barr virus. Science169, 180–190 (1970).

    Google Scholar 

  18. Hirshaut, Y.: Sarcoidosis, another disease associated with serologic evidence for herpes-like virus infection. New Eng. J. Med.283, 502–506 (1970).

    Google Scholar 

  19. Huang, D. P., Ho, J. H. C., Henle, W., Henle, G.: Demonstration of Epstein-Barr virus-associated nuclear antigen in nasopharyngeal carcinoma cells from fresh biopsies. Int. J. Cancer14, 580–588 (1974).

    Google Scholar 

  20. Johansson, B., Klein, G., Henle, W., Henle, G.: Epstein-Barr virus (EBV)-associated antibody patterns in malignant lymphoma and leukemia. I. Hodgkin's disease. Int. J. Cancer6, 450–462 (1970).

    Google Scholar 

  21. Kinard, R.: A program for inoculation of primates with potentially oncogenic viruses. In: Medical Primatology (2nd Conference on Experimental Medicine and Surgery in Primates, 1970), 895–902. New York-Basel: Karger 1971.

    Google Scholar 

  22. Klein, G.: The Epstein-Barr virus. In:Kaplan, A. S. (ed.), The Herpesviruses, 521–557. New York-London: Academic Press 1973.

    Google Scholar 

  23. Landon, J. C., Malan, L. B.: Seroepidemiologic studies of Epstein-Barr virus antibody in monkeys. J. Natl. Cancer Inst.46, 881–884 (1971).

    Google Scholar 

  24. Levine, P. H., Ablashi, D. V., Berard, C. W., Carbone, P. P., Waggoner, D. E., Malan, L.: Elevated antibody titers to Epstein-Barr virus in Hodgkin's disease. Cancer27, 416–421 (1971).

    Google Scholar 

  25. Levine, P. H., Merrill, D. A., Bethlenfalvey, N. C., Dabich, L., Stevens, D. A., Waggoner, D. E.: A longitudinal comparison of antibodies to Epstein-Barr virus and clinical parameters in chronic lymphocytic leukemia and chronic myelocytic leukemia. Blood38, 479–484 (1971).

    Google Scholar 

  26. Levine, P. H., O'Conor, G. T., Berard, C. W.: Antibodies to Epstein-Barr virus (EBV) in American patients with Burkitt's lymphoma. Cancer30, 610–615 (1972).

    Google Scholar 

  27. Maurer, B. A., Jones, J. A., Neefe, J. R.: Definition of 17 rhesus monkey histocompatibility antigens, including one new antigen. Tissue Antigens11, 1–19 (1978).

    Google Scholar 

  28. Miller, G., Robinson, J., Heston, L.: Immortalizing and nonimmortalizing laboratory strains of EBV. Cold Spring Harbor Symposium on Quantitative Biology39, 773–781 (1974).

    Google Scholar 

  29. Niederman, J. C., McCollum, R. W., Henle, G., Henle, W.: Infectious mononucleosis. Clinical manifestations in relation to EB virus antibodies. J.A.M.A.203, 205–209 (1968).

    Google Scholar 

  30. O'Conor, G. T.: Persistent immunologic stimulation as a factor in oncogenesis with special reference to Burkitt's tumor. Amer. J. Med.18, 279–285 (1970).

    Google Scholar 

  31. Penn, I.: Cancer in organ transplant recipients. Prog. Clin. Cancer6, 37–49 (1975).

    Google Scholar 

  32. Rabin, H., Neubauer, R. H., Hopkins, R. F., Levy, B. M.: Characterization of lymphoid cell lines established from multiple Epstein-Barr (EBV)-induced lymphomas in a cotton-topped marmoset. Int. J. Cancer20, 44–50 (1977).

    Google Scholar 

  33. Rabin, H., Neubauer, R. H., Pearson, G. R., Cicmanec, J. L., Wallen, W. C., Loeb, W. F., Valerio, M. G.: Spontaneous lymphoma associated with herpesvirus saimiri in owl monkeys. J. Natl. Cancer Inst.54, 499–501 (1975).

    Google Scholar 

  34. Reedman, B. M., Klein, G.: Cellular localization of an Epstein-Barr virus (EBV)-associated complement-fixing antigen in producer and non-producer lymphoblastoid cell lines. Int. J. Cancer11, 499–520 (1973).

    Google Scholar 

  35. Rocchi, G., Hewetson, J. F.: A practical and quantitative microtest for determination of neutralizing antibodies against Epstein-Barr virus. J. gen. Virol.18, 385–391 (1973).

    Google Scholar 

  36. Shope, T., de Chario, D., Miller, G.: Malignant lymphoma in cottontop marmosets after inoculation with Epstein-Barr virus. Proc. Natl. Acad. Sci (U.S.A.)70, 2487–2491 (1973).

    Google Scholar 

  37. Simons, M. J., Wee, G. B., Chan, S. H., Shanmugaratnam, K., Day, N. E., de-The, G. B.: Probable identification of an HLA second-locus antigen associated with a high risk of nasopharyngeal carcinoma. Lancet1, 142–143 (1975).

    Google Scholar 

  38. Stevens, D. A., Pry, T. W., Blackham, E. A., Manaker, R. A.: Comparison of antigens from human and chimpanzee herpes-type virus-defected hemic cell lines. Proc. Soc. exp. Biol. Med.133, 678–683 (1970).

    Google Scholar 

  39. Ziegler, J. L., Magrath, I. T., Gerber, P., Levine, P. H.: Epstein-Barr virus and human malignancy. Annals of Int. Med.86, 323–336 (1977).

    Google Scholar 

  40. Zur Hausen, H., Schulte-Holthausen, H., Klein, G., Henle, W., Henle, G., Clifford, P., Santesson, L.: EBV DNA in biopsies of Burkitt tumours and anaplastic carcinomas of the nasopharynx. Nature (London)228, 1056–1058 (1970).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

With 2 Figures

Supported in part by Contracts NO 1-CP-4333 and NO 1-CP-61029 with the Carcinogenesis Extramural Program, Division of Cancer Cause and Prevention.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Levine, P.H., Leiseca, S.A., Hewetson, J.F. et al. Infection of rhesus monkeys and chimpanzees with Epstein-Barr virus. Archives of Virology 66, 341–351 (1980). https://doi.org/10.1007/BF01320630

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01320630

Keywords

Navigation