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. 1997 Dec;71(12):9764–9769. doi: 10.1128/jvi.71.12.9764-9769.1997

A herpesvirus of rhesus monkeys related to the human Kaposi's sarcoma-associated herpesvirus.

R C Desrosiers 1, V G Sasseville 1, S C Czajak 1, X Zhang 1, K G Mansfield 1, A Kaur 1, R P Johnson 1, A A Lackner 1, J U Jung 1
PMCID: PMC230286  PMID: 9371642

Abstract

A herpesvirus that is related to but distinct from the Kaposi's sarcoma-associated herpesvirus (KSHV, or human herpesvirus 8) was isolated from rhesus monkeys. The sequence of 10.6 kbp from virion DNA revealed the presence of an interleukin-6 homolog similar to what is present in KSHV and a closer relatedness of the DNA polymerase and glycoprotein B reading frames to those of KSHV than to those of any other herpesvirus. This rhesus monkey herpesvirus replicated lytically and to high titers in cultured rhesus monkey fibroblasts. Antibody testing revealed a high prevalence for at least 10 years in our rhesus monkey colony and a high prevalence in two other colonies that were tested. Thus, rhesus monkeys naturally harbor a virus related to KSHV, which we have called RRV, for rhesus monkey rhadinovirus.

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Selected References

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  1. Albrecht J. C., Nicholas J., Biller D., Cameron K. R., Biesinger B., Newman C., Wittmann S., Craxton M. A., Coleman H., Fleckenstein B. Primary structure of the herpesvirus saimiri genome. J Virol. 1992 Aug;66(8):5047–5058. doi: 10.1128/jvi.66.8.5047-5058.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ambroziak J. A., Blackbourn D. J., Herndier B. G., Glogau R. G., Gullett J. H., McDonald A. R., Lennette E. T., Levy J. A. Herpes-like sequences in HIV-infected and uninfected Kaposi's sarcoma patients. Science. 1995 Apr 28;268(5210):582–583. doi: 10.1126/science.7725108. [DOI] [PubMed] [Google Scholar]
  3. Boshoff C., Schulz T. F., Kennedy M. M., Graham A. K., Fisher C., Thomas A., McGee J. O., Weiss R. A., O'Leary J. J. Kaposi's sarcoma-associated herpesvirus infects endothelial and spindle cells. Nat Med. 1995 Dec;1(12):1274–1278. doi: 10.1038/nm1295-1274. [DOI] [PubMed] [Google Scholar]
  4. Cesarman E., Chang Y., Moore P. S., Said J. W., Knowles D. M. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med. 1995 May 4;332(18):1186–1191. doi: 10.1056/NEJM199505043321802. [DOI] [PubMed] [Google Scholar]
  5. Cesarman E., Moore P. S., Rao P. H., Inghirami G., Knowles D. M., Chang Y. In vitro establishment and characterization of two acquired immunodeficiency syndrome-related lymphoma cell lines (BC-1 and BC-2) containing Kaposi's sarcoma-associated herpesvirus-like (KSHV) DNA sequences. Blood. 1995 Oct 1;86(7):2708–2714. [PubMed] [Google Scholar]
  6. Chalifoux L. V., Simon M. A., Pauley D. R., MacKey J. J., Wyand M. S., Ringler D. J. Arteriopathy in macaques infected with simian immunodeficiency virus. Lab Invest. 1992 Sep;67(3):338–349. [PubMed] [Google Scholar]
  7. Chang Y., Cesarman E., Pessin M. S., Lee F., Culpepper J., Knowles D. M., Moore P. S. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science. 1994 Dec 16;266(5192):1865–1869. doi: 10.1126/science.7997879. [DOI] [PubMed] [Google Scholar]
  8. Daniel M. D., Letvin N. L., King N. W., Kannagi M., Sehgal P. K., Hunt R. D., Kanki P. J., Essex M., Desrosiers R. C. Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science. 1985 Jun 7;228(4704):1201–1204. doi: 10.1126/science.3159089. [DOI] [PubMed] [Google Scholar]
  9. Daniel M. D., Letvin N. L., Sehgal P. K., Schmidt D. K., Silva D. P., Solomon K. R., Hodi F. S., Jr, Ringler D. J., Hunt R. D., King N. W. Prevalence of antibodies to 3 retroviruses in a captive colony of macaque monkeys. Int J Cancer. 1988 Apr 15;41(4):601–608. doi: 10.1002/ijc.2910410421. [DOI] [PubMed] [Google Scholar]
  10. Desrosiers R. C., Bakker A., Kamine J., Falk L. A., Hunt R. D., King N. W. A region of the Herpesvirus saimiri genome required for oncogenicity. Science. 1985 Apr 12;228(4696):184–187. doi: 10.1126/science.2983431. [DOI] [PubMed] [Google Scholar]
  11. Desrosiers R. C., Daniel M. D., Butler C. V., Schmidt D. K., Letvin N. L., Hunt R. D., King N. W., Barker C. S., Hunter E. Retrovirus D/New England and its relation to Mason-Pfizer monkey virus. J Virol. 1985 May;54(2):552–560. doi: 10.1128/jvi.54.2.552-560.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Desrosiers R. C. Safety issues facing development of a live-attenuated, multiply deleted HIV-1 vaccine. AIDS Res Hum Retroviruses. 1994 Apr;10(4):331–332. doi: 10.1089/aid.1994.10.331. [DOI] [PubMed] [Google Scholar]
  13. Desrosiers R. C. The value of specific pathogen-free rhesus monkey breeding colonies for AIDS research. AIDS Res Hum Retroviruses. 1997 Jan 1;13(1):5–6. doi: 10.1089/aid.1997.13.5. [DOI] [PubMed] [Google Scholar]
  14. Duboise S. M., Guo J., Desrosiers R. C., Jung J. U. Use of virion DNA as a cloning vector for the construction of mutant and recombinant herpesviruses. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11389–11394. doi: 10.1073/pnas.93.21.11389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Foreman K. E., Friborg J., Jr, Kong W. P., Woffendin C., Polverini P. J., Nickoloff B. J., Nabel G. J. Propagation of a human herpesvirus from AIDS-associated Kaposi's sarcoma. N Engl J Med. 1997 Jan 16;336(3):163–171. doi: 10.1056/NEJM199701163360302. [DOI] [PubMed] [Google Scholar]
  16. Gao S. J., Kingsley L., Hoover D. R., Spira T. J., Rinaldo C. R., Saah A., Phair J., Detels R., Parry P., Chang Y. Seroconversion to antibodies against Kaposi's sarcoma-associated herpesvirus-related latent nuclear antigens before the development of Kaposi's sarcoma. N Engl J Med. 1996 Jul 25;335(4):233–241. doi: 10.1056/NEJM199607253350403. [DOI] [PubMed] [Google Scholar]
  17. Giddens W. E., Jr, Tsai C. C., Morton W. R., Ochs H. D., Knitter G. H., Blakley G. A. Retroperitoneal fibromatosis and acquired immunodeficiency syndrome in macaques. Pathologic observations and transmission studies. Am J Pathol. 1985 May;119(2):253–263. [PMC free article] [PubMed] [Google Scholar]
  18. Honess R. W., Bodemer W., Cameron K. R., Niller H. H., Fleckenstein B., Randall R. E. The A+T-rich genome of Herpesvirus saimiri contains a highly conserved gene for thymidylate synthase. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3604–3608. doi: 10.1073/pnas.83.11.3604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jung J. U., Desrosiers R. C. Distinct functional domains of STP-C488 of herpesvirus saimiri. Virology. 1994 Nov 1;204(2):751–758. doi: 10.1006/viro.1994.1590. [DOI] [PubMed] [Google Scholar]
  20. Kaur A., Daniel M. D., Hempel D., Lee-Parritz D., Hirsch M. S., Johnson R. P. Cytotoxic T-lymphocyte responses to cytomegalovirus in normal and simian immunodeficiency virus-infected rhesus macaques. J Virol. 1996 Nov;70(11):7725–7733. doi: 10.1128/jvi.70.11.7725-7733.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kedes D. H., Operskalski E., Busch M., Kohn R., Flood J., Ganem D. The seroepidemiology of human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus): distribution of infection in KS risk groups and evidence for sexual transmission. Nat Med. 1996 Aug;2(8):918–924. doi: 10.1038/nm0896-918. [DOI] [PubMed] [Google Scholar]
  22. Kodama T., Silva D. P., Daniel M. D., Phillips-Conroy J. E., Jolly C. J., Rogers J., Desrosiers R. C. Prevalence of antibodies to SIV in baboons in their native habitat. AIDS Res Hum Retroviruses. 1989 Jun;5(3):337–343. doi: 10.1089/aid.1989.5.337. [DOI] [PubMed] [Google Scholar]
  23. Moore P. S., Boshoff C., Weiss R. A., Chang Y. Molecular mimicry of human cytokine and cytokine response pathway genes by KSHV. Science. 1996 Dec 6;274(5293):1739–1744. doi: 10.1126/science.274.5293.1739. [DOI] [PubMed] [Google Scholar]
  24. Moore P. S., Chang Y. Detection of herpesvirus-like DNA sequences in Kaposi's sarcoma in patients with and without HIV infection. N Engl J Med. 1995 May 4;332(18):1181–1185. doi: 10.1056/NEJM199505043321801. [DOI] [PubMed] [Google Scholar]
  25. Murthy S. C., Trimble J. J., Desrosiers R. C. Deletion mutants of herpesvirus saimiri define an open reading frame necessary for transformation. J Virol. 1989 Aug;63(8):3307–3314. doi: 10.1128/jvi.63.8.3307-3314.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Naidu Y. M., Kestler H. W., 3rd, Li Y., Butler C. V., Silva D. P., Schmidt D. K., Troup C. D., Sehgal P. K., Sonigo P., Daniel M. D. Characterization of infectious molecular clones of simian immunodeficiency virus (SIVmac) and human immunodeficiency virus type 2: persistent infection of rhesus monkeys with molecularly cloned SIVmac. J Virol. 1988 Dec;62(12):4691–4696. doi: 10.1128/jvi.62.12.4691-4696.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Neipel F., Albrecht J. C., Ensser A., Huang Y. Q., Li J. J., Friedman-Kien A. E., Fleckenstein B. Human herpesvirus 8 encodes a homolog of interleukin-6. J Virol. 1997 Jan;71(1):839–842. doi: 10.1128/jvi.71.1.839-842.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Renne R., Zhong W., Herndier B., McGrath M., Abbey N., Kedes D., Ganem D. Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture. Nat Med. 1996 Mar;2(3):342–346. doi: 10.1038/nm0396-342. [DOI] [PubMed] [Google Scholar]
  30. Roizmann B., Desrosiers R. C., Fleckenstein B., Lopez C., Minson A. C., Studdert M. J. The family Herpesviridae: an update. The Herpesvirus Study Group of the International Committee on Taxonomy of Viruses. Arch Virol. 1992;123(3-4):425–449. doi: 10.1007/BF01317276. [DOI] [PubMed] [Google Scholar]
  31. Rose T. M., Strand K. B., Schultz E. R., Schaefer G., Rankin G. W., Jr, Thouless M. E., Tsai C. C., Bosch M. L. Identification of two homologs of the Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in retroperitoneal fibromatosis of different macaque species. J Virol. 1997 May;71(5):4138–4144. doi: 10.1128/jvi.71.5.4138-4144.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Russo J. J., Bohenzky R. A., Chien M. C., Chen J., Yan M., Maddalena D., Parry J. P., Peruzzi D., Edelman I. S., Chang Y. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14862–14867. doi: 10.1073/pnas.93.25.14862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Said W., Chien K., Takeuchi S., Tasaka T., Asou H., Cho S. K., de Vos S., Cesarman E., Knowles D. M., Koeffler H. P. Kaposi's sarcoma-associated herpesvirus (KSHV or HHV8) in primary effusion lymphoma: ultrastructural demonstration of herpesvirus in lymphoma cells. Blood. 1996 Jun 15;87(12):4937–4943. [PubMed] [Google Scholar]
  34. Soulier J., Grollet L., Oksenhendler E., Cacoub P., Cazals-Hatem D., Babinet P., d'Agay M. F., Clauvel J. P., Raphael M., Degos L. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood. 1995 Aug 15;86(4):1276–1280. [PubMed] [Google Scholar]
  35. Staskus K. A., Zhong W., Gebhard K., Herndier B., Wang H., Renne R., Beneke J., Pudney J., Anderson D. J., Ganem D. Kaposi's sarcoma-associated herpesvirus gene expression in endothelial (spindle) tumor cells. J Virol. 1997 Jan;71(1):715–719. doi: 10.1128/jvi.71.1.715-719.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Thompson R., Honess R. W., Taylor L., Morran J., Davison A. J. Varicella-zoster virus specifies a thymidylate synthetase. J Gen Virol. 1987 May;68(Pt 5):1449–1455. doi: 10.1099/0022-1317-68-5-1449. [DOI] [PubMed] [Google Scholar]
  37. Trimble J. J., Murthy S. C., Bakker A., Grassmann R., Desrosiers R. C. A gene for dihydrofolate reductase in a herpesvirus. Science. 1988 Mar 4;239(4844):1145–1147. doi: 10.1126/science.2830673. [DOI] [PubMed] [Google Scholar]
  38. Tsai C. C., Giddens W. E., Jr, Morton W. R., Rosenkranz S. L., Ochs H. D., Benveniste R. E. Retroperitoneal fibromatosis and acquired immunodeficiency syndrome in macaques: epidemiologic studies. Lab Anim Sci. 1985 Oct;35(5):460–464. [PubMed] [Google Scholar]
  39. Tsai C. C., Warner T. F., Uno H., Giddens W. E., Jr, Ochs H. D. Subcutaneous fibromatosis associated with an acquired immune deficiency syndrome in pig-tailed macaques. Am J Pathol. 1985 Jul;120(1):30–37. [PMC free article] [PubMed] [Google Scholar]
  40. Whitby D., Howard M. R., Tenant-Flowers M., Brink N. S., Copas A., Boshoff C., Hatzioannou T., Suggett F. E., Aldam D. M., Denton A. S. Detection of Kaposi sarcoma associated herpesvirus in peripheral blood of HIV-infected individuals and progression to Kaposi's sarcoma. Lancet. 1995 Sep 23;346(8978):799–802. doi: 10.1016/s0140-6736(95)91619-9. [DOI] [PubMed] [Google Scholar]

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