Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1988 Jun;62(6):2134–2142. doi: 10.1128/jvi.62.6.2134-2142.1988

Distribution of a macaque immunosuppressive type D retrovirus in neural, lymphoid, and salivary tissues.

A A Lackner 1, M H Rodriguez 1, C E Bush 1, R J Munn 1, H S Kwang 1, P F Moore 1, K G Osborn 1, P A Marx 1, M B Gardner 1, L J Lowenstine 1
PMCID: PMC253311  PMID: 3285033

Abstract

Simian acquired immune deficiency syndrome (SAIDS) in rhesus macaques (Macaca mulatta) at the California Primate Research Center is caused by a type D retrovirus designated SAIDS retrovirus serotype 1 (SRV-1). This syndrome is characterized by profound immunosuppression and death associated with opportunistic infections. Neurologic signs and lesions have not been described as part of this syndrome. The distribution of SRV-1 in the salivary glands, lymph nodes, spleens, thymuses, and brains of eight virus-infected rhesus macaques was examined by immunohistochemistry. Electron microscopy, in situ RNA hybridization, and Southern blot hybridization were also performed on selected tissues to detect viral particles, RNA, and DNA, respectively. In seven of eight SRV-1-infected animals, the transmembrane envelope glycoprotein (gp20) of SRV-1 was present in three or more tissues, but never in the brain. In the remaining animal, no viral antigen was detected in any tissue. In this same group of animals, viral nucleic acid was detected in the lymph nodes of six of six animals by Southern blot hybridization, in the salivary glands of two of five animals by both Southern blot and in situ hybridizations, and, surprisingly, in the brains of three of three animals by Southern blot and of three of five animals by in situ hybridization, including the one animal in which viral gp20 was undetectable. None of these animals had neurologic signs or lesions. The detection of viral nucleic acid in the absence of viral antigen in the brain suggests latent SRV-1 infection of the central nervous system.

Full text

PDF

Images in this article

2137Image
on p.2137
2138Image
on p.2138
2139Image
on p.2139
2139Image
on p.2139

Selected References

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

  1. 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]
  2. Bryant M. L., Yamamoto J., Luciw P., Munn R., Marx P., Higgins J., Pedersen N., Levine A., Gardner M. B. Molecular comparison of retroviruses associated with human and simian AIDS. Hematol Oncol. 1985 Jul-Sep;3(3):187–197. doi: 10.1002/hon.2900030307. [DOI] [PubMed] [Google Scholar]
  3. Cork L. C., Narayan O. The pathogenesis of viral leukoencephalomyelitis-arthritis of goats. I. Persistent viral infection with progressive pathologic changes. Lab Invest. 1980 Jun;42(6):596–602. [PubMed] [Google Scholar]
  4. Daniel M. D., King N. W., Letvin N. L., Hunt R. D., Sehgal P. K., Desrosiers R. C. A new type D retrovirus isolated from macaques with an immunodeficiency syndrome. Science. 1984 Feb 10;223(4636):602–605. doi: 10.1126/science.6695172. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Fine D. L., Landon J. C., Pienta R. J., Kubicek M. T., Valerio M. G., Loeb W. F., Chopra H. C. Responses of infant rhesus monkeys to inoculation with Mason-Pfizer monkey virus materials. J Natl Cancer Inst. 1975 Mar;54(3):651–658. [PubMed] [Google Scholar]
  7. Francis D. P., Essex M., Hardy W. D., Jr Excretion of feline leukaemia virus by naturally infected pet cats. Nature. 1977 Sep 15;269(5625):252–254. doi: 10.1038/269252a0. [DOI] [PubMed] [Google Scholar]
  8. Gallo R. C., Gallagher R. E., Wong-Staal F., Aoki T., Markham P. D., Schetters H., Ruscetti F., Valerio M., Walling M. J., O'Keeffe R. T. Isolation and tissue distribution of type-C virus and viral components from a gibbon ape (Hylobates lar) with lymphocytic leukemia. Virology. 1978 Feb;84(2):359–373. doi: 10.1016/0042-6822(78)90255-6. [DOI] [PubMed] [Google Scholar]
  9. Gardner M. B. Retroviral spongiform polioencephalomyelopathy. Rev Infect Dis. 1985 Jan-Feb;7(1):99–110. doi: 10.1093/clinids/7.1.99. [DOI] [PubMed] [Google Scholar]
  10. Gardner M. B., Rongey R. W., Johnson E. Y., DeJournett R., Huebner R. J. C-type tumor virus particles in salivary tissue of domestic cats. J Natl Cancer Inst. 1971 Sep;47(3):561–568. [PubMed] [Google Scholar]
  11. Gravell M., London W. T., Lecatsas G., Hamilton R. S., Houff S. A., Sever J. L. Transmission of simian acquired immunodeficiency syndrome (SAIDS) with type D retrovirus isolated from saliva or urine. Proc Soc Exp Biol Med. 1984 Dec;177(3):491–494. doi: 10.3181/00379727-177-3-rc2. [DOI] [PubMed] [Google Scholar]
  12. Groopman J. E., Salahuddin S. Z., Sarngadharan M. G., Markham P. D., Gonda M., Sliski A., Gallo R. C. HTLV-III in saliva of people with AIDS-related complex and healthy homosexual men at risk for AIDS. Science. 1984 Oct 26;226(4673):447–449. doi: 10.1126/science.6093247. [DOI] [PubMed] [Google Scholar]
  13. Heidecker G., Lerche N. W., Lowenstine L. J., Lackner A. A., Osborn K. G., Gardner M. B., Marx P. A. Induction of simian acquired immune deficiency syndrome (SAIDS) with a molecular clone of a type D SAIDS retrovirus. J Virol. 1987 Oct;61(10):3066–3071. doi: 10.1128/jvi.61.10.3066-3071.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Henrickson R. V., Maul D. H., Osborn K. G., Sever J. L., Madden D. L., Ellingsworth L. R., Anderson J. H., Lowenstine L. J., Gardner M. B. Epidemic of acquired immunodeficiency in rhesus monkeys. Lancet. 1983 Feb 19;1(8321):388–390. doi: 10.1016/s0140-6736(83)91503-9. [DOI] [PubMed] [Google Scholar]
  15. Ho D. D., Rota T. R., Schooley R. T., Kaplan J. C., Allan J. D., Groopman J. E., Resnick L., Felsenstein D., Andrews C. A., Hirsch M. S. Isolation of HTLV-III from cerebrospinal fluid and neural tissues of patients with neurologic syndromes related to the acquired immunodeficiency syndrome. N Engl J Med. 1985 Dec 12;313(24):1493–1497. doi: 10.1056/NEJM198512123132401. [DOI] [PubMed] [Google Scholar]
  16. Kawakami T. G., Sun L., McDowell T. S. Infectious primate type-C virus shed by healthy gibbons. Nature. 1977 Aug 4;268(5619):448–450. doi: 10.1038/268448a0. [DOI] [PubMed] [Google Scholar]
  17. Kwang H. S., Pedersen N. C., Lerche N. W., Osborn K. G., Marx P. A., Gardner M. B. Viremia, antigenemia, and serum antibodies in rhesus macaques infected with simian retrovirus type 1 and their relationship to disease course. Lab Invest. 1987 Jun;56(6):591–597. [PubMed] [Google Scholar]
  18. Lerche N. W., Henrickson R. V., Maul D. H., Gardner M. B. Epidemiologic aspects of an outbreak of acquired immunodeficiency in rhesus monkeys (Macaca mulatta). Lab Anim Sci. 1984 Apr;34(2):146–150. [PubMed] [Google Scholar]
  19. Lerche N. W., Marx P. A., Osborn K. G., Maul D. H., Lowenstine L. J., Bleviss M. L., Moody P., Henrickson R. V., Gardner M. B. Natural history of endemic type D retrovirus infection and acquired immune deficiency syndrome in group-housed rhesus monkeys. J Natl Cancer Inst. 1987 Oct;79(4):847–854. [PubMed] [Google Scholar]
  20. Lerche N. W., Osborn K. G., Marx P. A., Prahalada S., Maul D. H., Lowenstine L. J., Munn R. J., Bryant M. L., Henrickson R. V., Arthur L. O. Inapparent carriers of simian acquired immune deficiency syndrome type D retrovirus and disease transmission with saliva. J Natl Cancer Inst. 1986 Aug;77(2):489–496. [PubMed] [Google Scholar]
  21. 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]
  22. Letvin N. L., Eaton K. A., Aldrich W. R., Sehgal P. K., Blake B. J., Schlossman S. F., King N. W., Hunt R. D. Acquired immunodeficiency syndrome in a colony of macaque monkeys. Proc Natl Acad Sci U S A. 1983 May;80(9):2718–2722. doi: 10.1073/pnas.80.9.2718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Levy J. A., Shimabukuro J., Hollander H., Mills J., Kaminsky L. Isolation of AIDS-associated retroviruses from cerebrospinal fluid and brain of patients with neurological symptoms. Lancet. 1985 Sep 14;2(8455):586–588. [PubMed] [Google Scholar]
  24. 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]
  25. Luciw P. A., Oppermann H., Bishop J. M., Varmus H. E. Integration and expression of several molecular forms of Rous sarcoma virus DNA used for transfection of mouse cells. Mol Cell Biol. 1984 Jul;4(7):1260–1269. doi: 10.1128/mcb.4.7.1260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lynn D. A., Angerer L. M., Bruskin A. M., Klein W. H., Angerer R. C. Localization of a family of MRNAS in a single cell type and its precursors in sea urchin embryos. Proc Natl Acad Sci U S A. 1983 May;80(9):2656–2660. doi: 10.1073/pnas.80.9.2656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. MacKenzie M., Lowenstine L., Lalchandani R., Lerche N., Osborn K., Spinner A., Bleviss M., Hendrickson R., Gardner M. Hematologic abnormalities in simian acquired immune deficiency syndrome. Lab Anim Sci. 1986 Feb;36(1):14–19. [PubMed] [Google Scholar]
  28. Marx P. A., Bryant M. L., Osborn K. G., Maul D. H., Lerche N. W., Lowenstine L. J., Kluge J. D., Zaiss C. P., Henrickson R. V., Shiigi S. M. Isolation of a new serotype of simian acquired immune deficiency syndrome type D retrovirus from Celebes black macaques (Macaca nigra) with immune deficiency and retroperitoneal fibromatosis. J Virol. 1985 Nov;56(2):571–578. doi: 10.1128/jvi.56.2.571-578.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Marx P. A., Maul D. H., Osborn K. G., Lerche N. W., Moody P., Lowenstine L. J., Henrickson R. V., Arthur L. O., Gilden R. V., Gravell M. Simian AIDS: isolation of a type D retrovirus and transmission of the disease. Science. 1984 Mar 9;223(4640):1083–1086. doi: 10.1126/science.6695196. [DOI] [PubMed] [Google Scholar]
  30. Marx P. A., Pedersen N. C., Lerche N. W., Osborn K. G., Lowenstine L. J., Lackner A. A., Maul D. H., Kwang H. S., Kluge J. D., Zaiss C. P. Prevention of simian acquired immune deficiency syndrome with a formalin-inactivated type D retrovirus vaccine. J Virol. 1986 Nov;60(2):431–435. doi: 10.1128/jvi.60.2.431-435.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Maul D. H., Lerche N. W., Osborn K. G., Marx P. A., Zaiss C., Spinner A., Kluge J. D., MacKenzie M. R., Lowenstine L. J., Bryant M. L. Pathogenesis of simian AIDS in rhesus macaques inoculated with the SRV-1 strain of type D retrovirus. Am J Vet Res. 1986 Apr;47(4):863–868. [PubMed] [Google Scholar]
  32. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Meyer P. R., Ormerod L. D., Osborn K. G., Lowenstine L. J., Hendrickson R. V., Modlin R. L., Smith R. E., Gardner M. B., Taylor C. R. An immunopathologic evaluation of lymph nodes from monkey and man with acquired immune deficiency syndrome and related conditions. Hematol Oncol. 1985 Jul-Sep;3(3):199–210. doi: 10.1002/hon.2900030308. [DOI] [PubMed] [Google Scholar]
  34. Munn R. J., Marx P. A., Yamamoto J. K., Gardner M. B. Ultrastructural comparison of the retroviruses associated with human and simian acquired immunodeficiency syndromes. Lab Invest. 1985 Aug;53(2):194–199. [PubMed] [Google Scholar]
  35. 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]
  36. Osborn K. G., Prahalada S., Lowenstine L. J., Gardner M. B., Maul D. H., Henrickson R. V. The pathology of an epizootic of acquired immunodeficiency in rhesus macaques. Am J Pathol. 1984 Jan;114(1):94–103. [PMC free article] [PubMed] [Google Scholar]
  37. Pétursson G., Nathanson N., Georgsson G., Panitch H., Pálsson P. A. Pathogenesis of visna. I. Sequential virologic, serologic, and pathologic studies. Lab Invest. 1976 Oct;35(4):402–412. [PubMed] [Google Scholar]
  38. Rojko J. L., Hoover E. A., Mathes L. E., Olsen R. G., Schaller J. P. Pathogenesis of experimental feline leukemia virus infection. J Natl Cancer Inst. 1979 Sep;63(3):759–768. doi: 10.1093/jnci/63.3.759. [DOI] [PubMed] [Google Scholar]
  39. Shaw G. M., Harper M. E., Hahn B. H., Epstein L. G., Gajdusek D. C., Price R. W., Navia B. A., Petito C. K., O'Hara C. J., Groopman J. E. HTLV-III infection in brains of children and adults with AIDS encephalopathy. Science. 1985 Jan 11;227(4683):177–182. doi: 10.1126/science.2981429. [DOI] [PubMed] [Google Scholar]
  40. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  41. Stowring L., Haase A. T., Petursson G., Georgsson G., Palsson P., Lutley R., Roos R., Szuchet S. Detection of visna virus antigens and RNA in glial cells in foci of demyelination. Virology. 1985 Mar;141(2):311–318. doi: 10.1016/0042-6822(85)90264-8. [DOI] [PubMed] [Google Scholar]
  42. Stromberg K., Benveniste R. E., Arthur L. O., Rabin H., Giddens W. E., Jr, Ochs H. D., Morton W. R., Tsai C. C. Characterization of exogenous type D retrovirus from a fibroma of a macaque with simian AIDS and fibromatosis. Science. 1984 Apr 20;224(4646):289–282. doi: 10.1126/science.6200929. [DOI] [PubMed] [Google Scholar]
  43. Tenner-Racz K., Racz P., Bofill M., Schulz-Meyer A., Dietrich M., Kern P., Weber J., Pinching A. J., Veronese-Dimarzo F., Popovic M. HTLV-III/LAV viral antigens in lymph nodes of homosexual men with persistent generalized lymphadenopathy and AIDS. Am J Pathol. 1986 Apr;123(1):9–15. [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES