Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1991 Apr;65(4):2135–2140. doi: 10.1128/jvi.65.4.2135-2140.1991

Isolation from African Sykes' monkeys (Cercopithecus mitis) of a lentivirus related to human and simian immunodeficiency viruses.

P Emau 1, H M McClure 1, M Isahakia 1, J G Else 1, P N Fultz 1
PMCID: PMC240089  PMID: 1825855

Abstract

Analysis of serum samples from 100 wild-caught or colony-born Sykes' monkeys (Cercopithecus mitis) in Kenya revealed that 59 animals had antibodies cross-reactive to human immunodeficiency virus type 2 (HIV-2) and to simian immunodeficiency viruses (SIVs). A lentivirus, designated SIVsyk, was isolated from five of six seropositive asymptomatic Sykes' monkeys, but in four cases isolation was possible only after depletion of CD8+ lymphocytes and cocultivation of the CD4(+)-enriched cell population with peripheral blood mononuclear cells from seronegative Sykes' monkeys. SIVsyk resembled other SIVs and HIVs morphologically, had an Mg2(+)-dependent reverse transcriptase enzyme, and replicated in and was cytopathic for CEMx174 and Sup-T1 cells. SIVsyk differred substantially from other SIVs, however, in that it failed to replicate in normal human, mangabey, and macaque peripheral blood mononuclear cells and serum from seropositive Sykes' monkeys immunoprecipitated env antigens from HIV-1 as well as from HIV-2, SIVsmm, and SIVagm. These data demonstrate a high prevalence of natural infection in Sykes' monkeys in Kenya with a lentivirus that appears to be unique with respect to its host range and antigenic cross-reactivity.

Full text

PDF
2135

Images in this article

2138Image
on p.2138

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allan J. S., Kanda P., Kennedy R. C., Cobb E. K., Anthony M., Eichberg J. W. Isolation and characterization of simian immunodeficiency viruses from two subspecies of African green monkeys. AIDS Res Hum Retroviruses. 1990 Mar;6(3):275–285. doi: 10.1089/aid.1990.6.275. [DOI] [PubMed] [Google Scholar]
  2. Barré-Sinoussi F., Chermann J. C., Rey F., Nugeyre M. T., Chamaret S., Gruest J., Dauguet C., Axler-Blin C., Vézinet-Brun F., Rouzioux C. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science. 1983 May 20;220(4599):868–871. doi: 10.1126/science.6189183. [DOI] [PubMed] [Google Scholar]
  3. Benveniste R. E., Arthur L. O., Tsai C. C., Sowder R., Copeland T. D., Henderson L. E., Oroszlan S. Isolation of a lentivirus from a macaque with lymphoma: comparison with HTLV-III/LAV and other lentiviruses. J Virol. 1986 Nov;60(2):483–490. doi: 10.1128/jvi.60.2.483-490.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chakrabarti L., Guyader M., Alizon M., Daniel M. D., Desrosiers R. C., Tiollais P., Sonigo P. Sequence of simian immunodeficiency virus from macaque and its relationship to other human and simian retroviruses. Nature. 1987 Aug 6;328(6130):543–547. doi: 10.1038/328543a0. [DOI] [PubMed] [Google Scholar]
  5. Chesebro B., Buller R., Portis J., Wehrly K. Failure of human immunodeficiency virus entry and infection in CD4-positive human brain and skin cells. J Virol. 1990 Jan;64(1):215–221. doi: 10.1128/jvi.64.1.215-221.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Desrosiers R. C., Daniel M. D., Li Y. HIV-related lentiviruses of nonhuman primates. AIDS Res Hum Retroviruses. 1989 Oct;5(5):465–473. doi: 10.1089/aid.1989.5.465. [DOI] [PubMed] [Google Scholar]
  8. Franchini G., Gurgo C., Guo H. G., Gallo R. C., Collalti E., Fargnoli K. A., Hall L. F., Wong-Staal F., Reitz M. S., Jr Sequence of simian immunodeficiency virus and its relationship to the human immunodeficiency viruses. Nature. 1987 Aug 6;328(6130):539–543. doi: 10.1038/328539a0. [DOI] [PubMed] [Google Scholar]
  9. Fukasawa M., Miura T., Hasegawa A., Morikawa S., Tsujimoto H., Miki K., Kitamura T., Hayami M. Sequence of simian immunodeficiency virus from African green monkey, a new member of the HIV/SIV group. Nature. 1988 Jun 2;333(6172):457–461. doi: 10.1038/333457a0. [DOI] [PubMed] [Google Scholar]
  10. Fultz P. N., Gordon T. P., Anderson D. C., McClure H. M. Prevalence of natural infection with simian immunodeficiency virus and simian T-cell leukemia virus type I in a breeding colony of sooty mangabey monkeys. AIDS. 1990 Jul;4(7):619–625. doi: 10.1097/00002030-199007000-00002. [DOI] [PubMed] [Google Scholar]
  11. Fultz P. N., McClure H. M., Anderson D. C., Swenson R. B., Anand R., Srinivasan A. Isolation of a T-lymphotropic retrovirus from naturally infected sooty mangabey monkeys (Cercocebus atys). Proc Natl Acad Sci U S A. 1986 Jul;83(14):5286–5290. doi: 10.1073/pnas.83.14.5286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fultz P. N., McClure H. M., Swenson R. B., McGrath C. R., Brodie A., Getchell J. P., Jensen F. C., Anderson D. C., Broderson J. R., Francis D. P. Persistent infection of chimpanzees with human T-lymphotropic virus type III/lymphadenopathy-associated virus: a potential model for acquired immunodeficiency syndrome. J Virol. 1986 Apr;58(1):116–124. doi: 10.1128/jvi.58.1.116-124.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fultz P. N., Stricker R. B., McClure H. M., Anderson D. C., Switzer W. M., Horaist C. Humoral response to SIV/SMM infection in macaque and mangabey monkeys. J Acquir Immune Defic Syndr. 1990;3(4):319–329. [PubMed] [Google Scholar]
  14. Gallo R. C., Salahuddin S. Z., Popovic M., Shearer G. M., Kaplan M., Haynes B. F., Palker T. J., Redfield R., Oleske J., Safai B. Frequent detection and isolation of cytopathic retroviruses (HTLV-III) from patients with AIDS and at risk for AIDS. Science. 1984 May 4;224(4648):500–503. doi: 10.1126/science.6200936. [DOI] [PubMed] [Google Scholar]
  15. Hirsch V. M., Olmsted R. A., Murphey-Corb M., Purcell R. H., Johnson P. R. An African primate lentivirus (SIVsm) closely related to HIV-2. Nature. 1989 Jun 1;339(6223):389–392. doi: 10.1038/339389a0. [DOI] [PubMed] [Google Scholar]
  16. Hirsch V., Riedel N., Mullins J. I. The genome organization of STLV-3 is similar to that of the AIDS virus except for a truncated transmembrane protein. Cell. 1987 May 8;49(3):307–319. doi: 10.1016/0092-8674(87)90283-2. [DOI] [PubMed] [Google Scholar]
  17. Honjo S., Narita T., Kobayashi R., Hiyaoka A., Fujimoto K., Takasaka M., Sakakibara I., Mukai R., Ishikawa K., Ohta Y. Experimental infection of African green monkeys and cynomolgus monkeys with a SIVAGM strain isolated from a healthy African green monkey. J Med Primatol. 1990;19(1):9–20. [PubMed] [Google Scholar]
  18. Hoxie J. A., Haggarty B. S., Bonser S. E., Rackowski J. L., Shan H., Kanki P. J. Biological characterization of a simian immunodeficiency virus-like retrovirus (HTLV-IV): evidence for CD4-associated molecules required for infection. J Virol. 1988 Aug;62(8):2557–2568. doi: 10.1128/jvi.62.8.2557-2568.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Huet T., Cheynier R., Meyerhans A., Roelants G., Wain-Hobson S. Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature. 1990 May 24;345(6273):356–359. doi: 10.1038/345356a0. [DOI] [PubMed] [Google Scholar]
  20. Johnson P. R., Fomsgaard A., Allan J., Gravell M., London W. T., Olmsted R. A., Hirsch V. M. Simian immunodeficiency viruses from African green monkeys display unusual genetic diversity. J Virol. 1990 Mar;64(3):1086–1092. doi: 10.1128/jvi.64.3.1086-1092.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kanki P. J., Kurth R., Becker W., Dreesman G., McLane M. F., Essex M. Antibodies to simian T-lymphotropic retrovirus type III in African green monkeys and recognition of STLV-III viral proteins by AIDS and related sera. Lancet. 1985 Jun 8;1(8441):1330–1332. doi: 10.1016/s0140-6736(85)92818-1. [DOI] [PubMed] [Google Scholar]
  22. Kanki P. J., McLane M. F., King N. W., Jr, Letvin N. L., Hunt R. D., Sehgal P., Daniel M. D., Desrosiers R. C., Essex M. Serologic identification and characterization of a macaque T-lymphotropic retrovirus closely related to HTLV-III. Science. 1985 Jun 7;228(4704):1199–1201. doi: 10.1126/science.3873705. [DOI] [PubMed] [Google Scholar]
  23. Kannagi M., Yetz J. M., Letvin N. L. In vitro growth characteristics of simian T-lymphotropic virus type III. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7053–7057. doi: 10.1073/pnas.82.20.7053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Klatzmann D., Barré-Sinoussi F., Nugeyre M. T., Danquet C., Vilmer E., Griscelli C., Brun-Veziret F., Rouzioux C., Gluckman J. C., Chermann J. C. Selective tropism of lymphadenopathy associated virus (LAV) for helper-inducer T lymphocytes. Science. 1984 Jul 6;225(4657):59–63. doi: 10.1126/science.6328660. [DOI] [PubMed] [Google Scholar]
  25. Kraus G., Werner A., Baier M., Binniger D., Ferdinand F. J., Norley S., Kurth R. Isolation of human immunodeficiency virus-related simian immunodeficiency viruses from African green monkeys. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2892–2896. doi: 10.1073/pnas.86.8.2892. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Letvin N. L., Daniel M. D., Sehgal P. K., Desrosiers R. C., Hunt R. D., Waldron L. M., MacKey J. J., Schmidt D. K., Chalifoux L. V., King N. W. Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III. Science. 1985 Oct 4;230(4721):71–73. doi: 10.1126/science.2412295. [DOI] [PubMed] [Google Scholar]
  27. Li Y., Naidu Y. M., Daniel M. D., Desrosiers R. C. Extensive genetic variability of simian immunodeficiency virus from African green monkeys. J Virol. 1989 Apr;63(4):1800–1802. doi: 10.1128/jvi.63.4.1800-1802.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lowenstine L. J., Pedersen N. C., Higgins J., Pallis K. C., Uyeda A., Marx P., Lerche N. W., Munn R. J., Gardner M. B. Seroepidemiologic survey of captive Old-World primates for antibodies to human and simian retroviruses, and isolation of a lentivirus from sooty mangabeys (Cercocebus atys). Int J Cancer. 1986 Oct 15;38(4):563–574. doi: 10.1002/ijc.2910380417. [DOI] [PubMed] [Google Scholar]
  29. Maddon P. J., Dalgleish A. G., McDougal J. S., Clapham P. R., Weiss R. A., Axel R. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell. 1986 Nov 7;47(3):333–348. doi: 10.1016/0092-8674(86)90590-8. [DOI] [PubMed] [Google Scholar]
  30. McClure H. M., Anderson D. C., Fultz P. N., Ansari A. A., Lockwood E., Brodie A. Spectrum of disease in macaque monkeys chronically infected with SIV/SMM. Vet Immunol Immunopathol. 1989 May;21(1):13–24. doi: 10.1016/0165-2427(89)90126-8. [DOI] [PubMed] [Google Scholar]
  31. Miller M. D., Lord C. I., Stallard V., Mazzara G. P., Letvin N. L. The gag-specific cytotoxic T lymphocytes in rhesus monkeys infected with the simian immunodeficiency virus of macaques. J Immunol. 1990 Jan 1;144(1):122–128. [PubMed] [Google Scholar]
  32. Murphey-Corb M., Martin L. N., Rangan S. R., Baskin G. B., Gormus B. J., Wolf R. H., Andes W. A., West M., Montelaro R. C. Isolation of an HTLV-III-related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature. 1986 May 22;321(6068):435–437. doi: 10.1038/321435a0. [DOI] [PubMed] [Google Scholar]
  33. Nicol I., Flamminio-Zola G., Dubouch P., Bernard J., Snart R., Jouffre R., Reveil B., Fouchard M., Desportes I., Nara P. Persistent HIV-2 infection of rhesus macaque, baboon, and mangabeys. Intervirology. 1989;30(5):258–267. doi: 10.1159/000150101. [DOI] [PubMed] [Google Scholar]
  34. Ohta Y., Masuda T., Tsujimoto H., Ishikawa K., Kodama T., Morikawa S., Nakai M., Honjo S., Hayami M. Isolation of simian immunodeficiency virus from African green monkeys and seroepidemiologic survey of the virus in various non-human primates. Int J Cancer. 1988 Jan 15;41(1):115–122. doi: 10.1002/ijc.2910410121. [DOI] [PubMed] [Google Scholar]
  35. Peeters M., Honoré C., Huet T., Bedjabaga L., Ossari S., Bussi P., Cooper R. W., Delaporte E. Isolation and partial characterization of an HIV-related virus occurring naturally in chimpanzees in Gabon. AIDS. 1989 Oct;3(10):625–630. doi: 10.1097/00002030-198910000-00001. [DOI] [PubMed] [Google Scholar]
  36. Sattentau Q. J., Clapham P. R., Weiss R. A., Beverley P. C., Montagnier L., Alhalabi M. F., Gluckmann J. C., Klatzmann D. The human and simian immunodeficiency viruses HIV-1, HIV-2 and SIV interact with similar epitopes on their cellular receptor, the CD4 molecule. AIDS. 1988 Apr;2(2):101–105. doi: 10.1097/00002030-198804000-00005. [DOI] [PubMed] [Google Scholar]
  37. Spira T. J., Bozeman L. H., Holman R. C., Warfield D. T., Phillips S. K., Feorino P. M. Micromethod for assaying reverse transcriptase of human T-cell lymphotropic virus type III/lymphadenopathy-associated virus. J Clin Microbiol. 1987 Jan;25(1):97–99. doi: 10.1128/jcm.25.1.97-99.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tsoi M. S., Aprile J., Dobbs S., Goehle S., Storb R. Enrichment (and depletion) of human suppressor cells with monoclonal antibodies and immunoglobulin-coated plates. J Immunol Methods. 1982 Sep 30;53(3):293–305. doi: 10.1016/0022-1759(82)90176-4. [DOI] [PubMed] [Google Scholar]
  39. Tsubota H., Lord C. I., Watkins D. I., Morimoto C., Letvin N. L. A cytotoxic T lymphocyte inhibits acquired immunodeficiency syndrome virus replication in peripheral blood lymphocytes. J Exp Med. 1989 Apr 1;169(4):1421–1434. doi: 10.1084/jem.169.4.1421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tsujimoto H., Cooper R. W., Kodama T., Fukasawa M., Miura T., Ohta Y., Ishikawa K., Nakai M., Frost E., Roelants G. E. Isolation and characterization of simian immunodeficiency virus from mandrills in Africa and its relationship to other human and simian immunodeficiency viruses. J Virol. 1988 Nov;62(11):4044–4050. doi: 10.1128/jvi.62.11.4044-4050.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Tsujimoto H., Hasegawa A., Maki N., Fukasawa M., Miura T., Speidel S., Cooper R. W., Moriyama E. N., Gojobori T., Hayami M. Sequence of a novel simian immunodeficiency virus from a wild-caught African mandrill. Nature. 1989 Oct 12;341(6242):539–541. doi: 10.1038/341539a0. [DOI] [PubMed] [Google Scholar]
  42. Walker C. M., Moody D. J., Stites D. P., Levy J. A. CD8+ T lymphocyte control of HIV replication in cultured CD4+ cells varies among infected individuals. Cell Immunol. 1989 Apr 1;119(2):470–475. doi: 10.1016/0008-8749(89)90259-1. [DOI] [PubMed] [Google Scholar]
  43. Walker C. M., Moody D. J., Stites D. P., Levy J. A. CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science. 1986 Dec 19;234(4783):1563–1566. doi: 10.1126/science.2431484. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES