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. 1985 Oct;56(1):60–65. doi: 10.1128/jvi.56.1.60-65.1985

Herpesvirus sylvilagus infects both B and T lymphocytes in vivo.

W J Kramp, P Medveczky, C Mulder, H C Hinze, J L Sullivan
PMCID: PMC252470  PMID: 2993667

Abstract

Herpesvirus sylvilagus infection of cottontail rabbits (Sylvilagus floridanus) was studied as a model of herpesvirus-induced lymphoproliferative disorders. Leukocytosis, splenomegaly, proliferation of T cells and virus production by lymphocytes characterized this infectious mononucleosis-like disease. Approximately two copies of circular herpesvirus sylvilagus genomes per cell were detected in spleen cells at 2 weeks postinfection, and circular genomes could still be observed after 4 months. Circular viral genomes were found in both B and T lymphocytes. Small amounts of linear viral DNA (0.1 to 0.3 copies per cell) were also detected in both B and T cells. These results indicated that the virus did not replicate in the majority of lymphocytes in vivo. Herpesvirus sylvilagus infection in cottontail rabbits could be useful as a model for studying the complex virus-host relationships of lymphotropic herpesviruses and perhaps as an animal model for Epstein-Barr virus infection in humans.

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Selected References

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  1. Adams A., Lindahl T. Epstein-Barr virus genomes with properties of circular DNA molecules in carrier cells. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1477–1481. doi: 10.1073/pnas.72.4.1477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barr I. G., Toh B. H. Routine flow cytometric diagnosis of lymphoproliferative disorders. J Clin Immunol. 1983 Apr;3(2):184–195. doi: 10.1007/BF00915491. [DOI] [PubMed] [Google Scholar]
  3. Bast B. J., Catty D., Manten-Slingerland R., Jansen J. T., Veldhuis D. H., Roholl P., Ballieux R. E. Surface Ig on rabbit lymphocytes. Rabbit B and T cells are distinct populations. Eur J Immunol. 1979 Dec;9(12):997–1003. doi: 10.1002/eji.1830091215. [DOI] [PubMed] [Google Scholar]
  4. Bayliss G. J., Wolf H. The regulated expression of Epstein-Barr virus. III. Proteins specified by EBV during the lytic cycle. J Gen Virol. 1981 Sep;56(Pt 1):105–118. doi: 10.1099/0022-1317-56-1-105. [DOI] [PubMed] [Google Scholar]
  5. Cleary M. L., Warnke R., Sklar J. Monoclonality of lymphoproliferative lesions in cardiac-transplant recipients. Clonal analysis based on immunoglobulin-gene rearrangements. N Engl J Med. 1984 Feb 23;310(8):477–482. doi: 10.1056/NEJM198402233100801. [DOI] [PubMed] [Google Scholar]
  6. Colby B. M., Shaw J. E., Elion G. B., Pagano J. S. Effect of acyclovir [9-(2-hydroxyethoxymethyl)guanine] on Epstein-Barr virus DNA replication. J Virol. 1980 May;34(2):560–568. doi: 10.1128/jvi.34.2.560-568.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Daniel M. D., Meléndez L. V., Hunt R. D., King N. W., Anver M., Fraser C. E., Barahona H., Baggs R. B. Herpesvirus saimiri: VII. Induction of malignant lymphoma in New Zealand white rabbits. J Natl Cancer Inst. 1974 Dec;53(6):1803–1807. [PubMed] [Google Scholar]
  8. Falk L., Johnson D., Deinhardt F. Transformation of marmoset lymphocytes in vitro with Herpesvirus ateles. Int J Cancer. 1978 May 15;21(5):652–657. doi: 10.1002/ijc.2910210517. [DOI] [PubMed] [Google Scholar]
  9. Gardella T., Medveczky P., Sairenji T., Mulder C. Detection of circular and linear herpesvirus DNA molecules in mammalian cells by gel electrophoresis. J Virol. 1984 Apr;50(1):248–254. doi: 10.1128/jvi.50.1.248-254.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gonzalez-Serva A., Hsiung G. D. Expression of herpesvirus in adherent cells derived from bone marrow of latently infected guinea pigs. Am J Pathol. 1978 Jun;91(3):483–496. [PMC free article] [PubMed] [Google Scholar]
  11. Griffith B. P., Hsiung G. D. Persistence and expression of herpes virus in guinea pig B and T spleen cells. Proc Soc Exp Biol Med. 1979 Oct;162(1):202–206. doi: 10.3181/00379727-162-40647. [DOI] [PubMed] [Google Scholar]
  12. Hanto D. W., Frizzera G., Gajl-Peczalska K. J., Sakamoto K., Purtilo D. T., Balfour H. H., Jr, Simmons R. L., Najarian J. S. Epstein-Barr virus-induced B-cell lymphoma after renal transplantation: acyclovir therapy and transition from polyclonal to monoclonal B-cell proliferation. N Engl J Med. 1982 Apr 15;306(15):913–918. doi: 10.1056/NEJM198204153061506. [DOI] [PubMed] [Google Scholar]
  13. Hinze H. C. Induction of lymphoid hyperplasia and lymphoma-like disease in rabbits by Herpesvirus sylvilagus. Int J Cancer. 1971 Nov 15;8(3):514–522. doi: 10.1002/ijc.2910080320. [DOI] [PubMed] [Google Scholar]
  14. Hinze H. C. New member of the herpesvirus group isolated from wild cottontail rabbits. Infect Immun. 1971 Feb;3(2):350–354. doi: 10.1128/iai.3.2.350-354.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hunt R. D., Meléndez L. V., García F. G., Trum B. F. Pathologic features of Herpesvirus ateles lymphoma in cotton-topped marmosets (Saguinus oedipus). J Natl Cancer Inst. 1972 Dec;49(6):1631–1639. doi: 10.1093/jnci/49.6.1631. [DOI] [PubMed] [Google Scholar]
  16. Hunt R. D., Meléndez L. V., King N. W., Gilmore C. E., Daniel M. D., Williamson M. E., Jones T. C. Morphology of a disease with features of malignant lymphoma in marmosets and owl monkeys inoculated with Herpesvirus saimiri. J Natl Cancer Inst. 1970 Feb;44(2):447–465. [PubMed] [Google Scholar]
  17. Jackson S., Chused T. M., Wilkinson J. M., Leiserson W. M., Kindt T. J. Differentiation antigens identify subpopulations of rabbit T and B lymphocytes. Definition by flow cytometry. J Exp Med. 1983 Jan 1;157(1):34–46. doi: 10.1084/jem.157.1.34. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jondal M., Klein G. Surface markers on human B and T lymphocytes. II. Presence of Epstein-Barr virus receptors on B lymphocytes. J Exp Med. 1973 Dec 1;138(6):1365–1378. doi: 10.1084/jem.138.6.1365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kaschka-Dierich C., Werner F. J., Bauer I., Fleckenstein B. Structure of nonintegrated, circular Herpesvirus saimiri and Herpesvirus ateles genomes in tumor cell lines and in vitro-transformed cells. J Virol. 1982 Oct;44(1):295–310. doi: 10.1128/jvi.44.1.295-310.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Medveczky P., Kramp W. J., Sullivan J. L. Circular Herpesvirus sylvilagus DNA in spleen cells of experimentally infected cottontail rabbits. J Virol. 1984 Nov;52(2):711–714. doi: 10.1128/jvi.52.2.711-714.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nazerian K., Elmubarak A., Sharma J. M. Establishment of B-lymphoblastoid cell lines from Marek's disease virus-induced tumors in turkeys. Int J Cancer. 1982 Jan 15;29(1):63–68. doi: 10.1002/ijc.2910290111. [DOI] [PubMed] [Google Scholar]
  22. Ooka T., Calender A., de Turenne M., Daillie J. Effect of arabinofuranosylthymine on the replication of Epstein-Barr virus and relationship with a new induced thymidine kinase activity. J Virol. 1983 Apr;46(1):187–195. doi: 10.1128/jvi.46.1.187-195.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pattengale P. K., Smith R. W., Perlin E. Atypical lymphocytes in acute infectious mononucleosis. Identification by multiple T and B lymphocyte markers. N Engl J Med. 1974 Nov 28;291(22):1145–1148. doi: 10.1056/NEJM197411282912201. [DOI] [PubMed] [Google Scholar]
  24. Rinaldo C. R., Jr, Black P. H., Hirsch M. S. Interaction of cytomegalovirus with leukocytes from patients with mononucleosis due to cytomegalovirus. J Infect Dis. 1977 Nov;136(5):667–678. doi: 10.1093/infdis/136.5.667. [DOI] [PubMed] [Google Scholar]
  25. Rziha H. J., Bauer B. Circular forms of viral DNA in Marek's disease virus-transformed lymphoblastoid cells. Arch Virol. 1982;72(3):211–216. doi: 10.1007/BF01348966. [DOI] [PubMed] [Google Scholar]
  26. Schirm S., Müller I., Desrosiers R. C., Fleckenstein B. Herpesvirus saimiri DNA in a lymphoid cell line established by in vitro transformation. J Virol. 1984 Mar;49(3):938–946. doi: 10.1128/jvi.49.3.938-946.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schubach W. H., Hackman R., Neiman P. E., Miller G., Thomas E. D. A monoclonal immunoblastic sarcoma in donor cells bearing Epstein-Barr virus genomes following allogeneic marrow grafting for acute lymphoblastic leukemia. Blood. 1982 Jul;60(1):180–187. [PubMed] [Google Scholar]
  28. Sell S., Skaletsky E., Holdbrook R., Linthicum D. S., Raffel C. Alternative hypotheses of lymphocyte surface immunoglobulin expression, B lymphocyte activation and B lymphocyte differentiation. Immunol Rev. 1980;52:141–179. doi: 10.1111/j.1600-065x.1980.tb00334.x. [DOI] [PubMed] [Google Scholar]
  29. Shek W. R., Calnek B. W., Schat K. A., Chen C. H. Characterization of Marek's disease virus-infected lymphocytes: discrimination between cytolytically and latently infected cells. J Natl Cancer Inst. 1983 Mar;70(3):485–491. [PubMed] [Google Scholar]
  30. Sixbey J. W., Pagano J. S. Epstein-Barr virus transformation of human B lymphocytes despite inhibition of viral polymerase. J Virol. 1985 Jan;53(1):299–301. doi: 10.1128/jvi.53.1.299-301.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Spieker J. O., Yuill T. M. Herpesvirus sylvilagus in cottontail rabbits: antibody prevalence and flea burden relationships. J Wildl Dis. 1976 Jul;12(3):310–314. doi: 10.7589/0090-3558-12.3.310. [DOI] [PubMed] [Google Scholar]
  32. Spieker J. O., Yuill T. M. Herpesvirus sylvilagus in cottontail rabbits: evidence of shedding but not transplacental transmission. J Wildl Dis. 1977 Jan;13(1):85–89. doi: 10.7589/0090-3558-13.1.85. [DOI] [PubMed] [Google Scholar]
  33. Sullivan J. L., Byron K. S., Brewster F. E., Baker S. M., Ochs H. D. X-linked lymphoproliferative syndrome. Natural history of the immunodeficiency. J Clin Invest. 1983 Jun;71(6):1765–1778. doi: 10.1172/JCI110932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sullivan J. L., Medveczky P., Forman S. J., Baker S. M., Monroe J. E., Mulder C. Epstein-Barr-virus induced lymphoproliferation. Implications for antiviral chemotherapy. N Engl J Med. 1984 Nov 1;311(18):1163–1167. doi: 10.1056/NEJM198411013111806. [DOI] [PubMed] [Google Scholar]
  35. Svedmyr E., Jondal M. Cytotoxic effector cells specific for B Cell lines transformed by Epstein-Barr virus are present in patients with infectious mononucleosis. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1622–1626. doi: 10.1073/pnas.72.4.1622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wegner D. L., Hinze H. C. Virus--host-cell relationship of Herpesvirus sylvilagus with cottontail rabbit leukocytes. Int J Cancer. 1974 Nov 15;14(5):567–575. doi: 10.1002/ijc.2910140502. [DOI] [PubMed] [Google Scholar]
  37. Werner F. J., Bornkamm G. W., Fleckenstein B. Episomal viral DNA in a Herpesvirus saimiri-transformed lymphoid cell line. J Virol. 1977 Jun;22(3):794–803. doi: 10.1128/jvi.22.3.794-803.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. zur Hausen H., O'Neill F. J., Freese U. K., Hecker E. Persisting oncogenic herpesvirus induced by the tumour promotor TPA. Nature. 1978 Mar 23;272(5651):373–375. doi: 10.1038/272373a0. [DOI] [PubMed] [Google Scholar]

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