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. 1996 Mar;70(3):1633–1639. doi: 10.1128/jvi.70.3.1633-1639.1996

Interspecies transmission of macaque simian T-cell leukemia/lymphoma virus type 1 in baboons resulted in an outbreak of malignant lymphoma.

A Voevodin 1, E Samilchuk 1, H Schätzl 1, E Boeri 1, G Franchini 1
PMCID: PMC189987  PMID: 8627684

Abstract

An outbreak of malignant lymphoma has been observed in one of the baboon (Papio hamadryas) stocks of Sukhumi Primate Center. More than 300 cases in this "high-lymphoma stock" have been registered since 1967. Human T-cell lymphotropic virus type 1 (HTLV-1)-related virus was implicated as the etiologic agent of Sukhumi baboon lymphoma. The origin of this virus remained unclear. Two possibilities were originally considered: the origin could be baboon simian T-cell leukemia/lymphoma virus type 1 (STLV-1) or HTLV-1 (before the outbreak started, some Sukhumi baboons were inoculated with human leukemic material). The third possibility entered recently: interspecies transmission of rhesus macaque STLV-1 to baboons. It was prompted by the finding of very close similarity between STLV-1 991-1cc (the strain isolated from a non-Sukhumi baboon inoculated with material from a Sukhumi lymphomatous baboon) and rhesus STLV-1. To test this hypothesis, we investigated 37 Sukhumi STLV-1 isolates from baboons of high-lymphoma stock by PCR discriminating rhesus type and baboon type STLV-1 isolates. All of them were proved to be rhesus type STLV-1. In contrast, all six STLV-1 isolates from baboons belonging to other stocks or populations were of baboon type. The PCR results were fully confirmed by DNA sequence data. The partial env gene gene sequences of all four STLV-1 isolates from Sukhumi lymphomatous baboons were 97 to 100% similar to the sequence of known rhesus STLV-1 and only 85% homologous with the sequence of conventional baboon STLV-1. Thus, interspecies transmission of STLV-1 from rhesus macaques (or closely related species) to baboons occurred at Sukhumi Primate Center. Most probably this event initiated the outbreak of lymphoma in Sukhumi baboons.

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Selected References

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  1. Chikobaeva M. G., Schatzl H., Rose D., Bush U., Iakovleva L. A., Deinhardt F., Helm K., Lapin B. A. Novyi variant obez'ian'ego T-limfotropnogo retrovirusa pervogo tipa (STLV-1F) v Sukhumskoi kolonii pavianov gamadrilov. Vopr Virusol. 1993 Nov-Dec;38(6):249–253. [PubMed] [Google Scholar]
  2. Crawford M. H., Devor E. J., O'Rourke D. H., Yakovleva L. A., Voevodin A. F., Lapin B. A. Genetics of primate lymphomas in a baboon (Papio hamadryas) colony of Sukhumi, USSR. Genetica. 1987 Aug 31;73(1-2):145–157. doi: 10.1007/BF00057445. [DOI] [PubMed] [Google Scholar]
  3. D'iachenko A. G., Kondzhariia I. G., Indzhiia E. V., Lapin B. A., Iakovleva L. A., Rudaia L. D., Dzhalagoniia B. L. Monoklonal'naia integratsiia virusa T-kletochnogo leikoza obez'ian u pavianov gamadrilov so zlokachestvennoi limfomoi. Eksp Onkol. 1990;12(3):15–18. [PubMed] [Google Scholar]
  4. 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]
  5. Gessain A., Boeri E., Yanagihara R., Gallo R. C., Franchini G. Complete nucleotide sequence of a highly divergent human T-cell leukemia (lymphotropic) virus type I (HTLV-I) variant from melanesia: genetic and phylogenetic relationship to HTLV-I strains from other geographical regions. J Virol. 1993 Feb;67(2):1015–1023. doi: 10.1128/jvi.67.2.1015-1023.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gessain A., Gallo R. C., Franchini G. Low degree of human T-cell leukemia/lymphoma virus type I genetic drift in vivo as a means of monitoring viral transmission and movement of ancient human populations. J Virol. 1992 Apr;66(4):2288–2295. doi: 10.1128/jvi.66.4.2288-2295.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Guo H. G., Wong-Stall F., Gallo R. C. Novel viral sequences related to human T-cell leukemia virus in T cells of a seropositive baboon. Science. 1984 Mar 16;223(4641):1195–1197. doi: 10.1126/science.6322297. [DOI] [PubMed] [Google Scholar]
  8. Hubbard G. B., Moné J. P., Allan J. S., Davis K. J., 3rd, Leland M. M., Banks P. M., Smir B. Spontaneously generated non-Hodgkin's lymphoma in twenty-seven simian T-cell leukemia virus type 1 antibody-positive baboons (Papio species). Lab Anim Sci. 1993 Aug;43(4):301–309. [PubMed] [Google Scholar]
  9. Kondzhariia I. G., D'iachenko A. G., Lapin B. A., Rudaia L. D. Analiz virusa T-kletochnogo leikoza obez'ian, klonal'no integrirovannogo pri zlokachestvennoi limfome pavianov. Vopr Virusol. 1990 May-Jun;35(3):211–213. [PubMed] [Google Scholar]
  10. Koralnik I. J., Boeri E., Saxinger W. C., Monico A. L., Fullen J., Gessain A., Guo H. G., Gallo R. C., Markham P., Kalyanaraman V. Phylogenetic associations of human and simian T-cell leukemia/lymphotropic virus type I strains: evidence for interspecies transmission. J Virol. 1994 Apr;68(4):2693–2707. doi: 10.1128/jvi.68.4.2693-2707.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kwok S., Higuchi R. Avoiding false positives with PCR. Nature. 1989 May 18;339(6221):237–238. doi: 10.1038/339237a0. [DOI] [PubMed] [Google Scholar]
  12. Lapin B. A., Iakovleva L. A., Asanov N. S., Kokosha L. V., Tsiripova G. S. Epidemiologicheskii aspekt vspyshki leikoza v stade pavianov gamadrilov Sukhumskogo pitomnika. Vopr Virusol. 1973 Jan-Feb;18(1):38–44. [PubMed] [Google Scholar]
  13. Lapin B. A. Possible ways viral leukemia spreads among the hamadryas baboons of the Sukhumi monkey colony. Bibl Haematol. 1975;(40):75–84. doi: 10.1159/000397520. [DOI] [PubMed] [Google Scholar]
  14. Lapin B. A., Voevodin A. F., Indzhiia L. V., Iakovleva L. Ia, Gallo R. Nekotorye aspekty étiologii leikozov primatov, vkliuchaia cheloveka. Biull Eksp Biol Med. 1983 Dec;96(12):14–16. [PubMed] [Google Scholar]
  15. Moné J., Whitehead E., Leland M., Hubbard G., Allan J. S. Simian T-cell leukemia virus type I infection in captive baboons. AIDS Res Hum Retroviruses. 1992 Sep;8(9):1653–1661. doi: 10.1089/aid.1992.8.1653. [DOI] [PubMed] [Google Scholar]
  16. Newton C. R., Graham A., Heptinstall L. E., Powell S. J., Summers C., Kalsheker N., Smith J. C., Markham A. F. Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS). Nucleic Acids Res. 1989 Apr 11;17(7):2503–2516. doi: 10.1093/nar/17.7.2503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Popovic M., Sarin P. S., Robert-Gurroff M., Kalyanaraman V. S., Mann D., Minowada J., Gallo R. C. Isolation and transmission of human retrovirus (human t-cell leukemia virus). Science. 1983 Feb 18;219(4586):856–859. doi: 10.1126/science.6600519. [DOI] [PubMed] [Google Scholar]
  18. Rabin H., Neubauer R. H., Hopkins R. F., 3rd, Dzhikidze E. K., Shevtsova Z. V., Lapin B. A. Transforming activity and antigenicity of an Epstein-Barr-like virus from lymphoblastoid cell lines of baboons with lymphoid disease. Intervirology. 1977;8(4):240–249. doi: 10.1159/000148899. [DOI] [PubMed] [Google Scholar]
  19. Rogers J., Kidd K. K. Nuclear DNA polymorphisms in a wild population of yellow baboons (Papio hamadryas cynocephalus) from Mikumi National Park, Tanzania. Am J Phys Anthropol. 1993 Apr;90(4):477–486. doi: 10.1002/ajpa.1330900407. [DOI] [PubMed] [Google Scholar]
  20. Rychlik W., Spencer W. J., Rhoads R. E. Optimization of the annealing temperature for DNA amplification in vitro. Nucleic Acids Res. 1990 Nov 11;18(21):6409–6412. doi: 10.1093/nar/18.21.6409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Saksena N. K., Herve V., Durand J. P., Leguenno B., Diop O. M., Digouette J. P., Mathiot C., Muller M. C., Love J. L., Dube S. Seroepidemiologic, molecular, and phylogenetic analyses of simian T-cell leukemia viruses (STLV-I) from various naturally infected monkey species from central and western Africa. Virology. 1994 Jan;198(1):297–310. doi: 10.1006/viro.1994.1033. [DOI] [PubMed] [Google Scholar]
  22. Saksena N. K., Hervé V., Sherman M. P., Durand J. P., Mathiot C., Müller M., Love J. L., LeGuenno B., Sinoussi F. B., Dube D. K. Sequence and phylogenetic analyses of a new STLV-I from a naturally infected tantalus monkey from Central Africa. Virology. 1993 Jan;192(1):312–320. doi: 10.1006/viro.1993.1035. [DOI] [PubMed] [Google Scholar]
  23. Schatzl H., Yakovleva L., Lapin B., Rose D., Inzhiia L., Gaedigk-Nitschko K., Deinhardt F., von der Helm K. Detection and characterization of T-cell leukemia virus-like proviral sequences in PBL and tissues of baboons by PCR. Leukemia. 1992;6 (Suppl 3):158S–160S. [PubMed] [Google Scholar]
  24. Schätzl H., Tschikobava M., Rose D., Voevodin A., Nitschko H., Sieger E., Busch U., von der Helm K., Lapin B. The Sukhumi primate monkey model for viral lymphomogenesis: high incidence of lymphomas with presence of STLV-I and EBV-like virus. Leukemia. 1993 Aug;7 (Suppl 2):S86–S92. [PubMed] [Google Scholar]
  25. Sherman M. P., Saksena N. K., Dube D. K., Yanagihara R., Poiesz B. J. Evolutionary insights on the origin of human T-cell lymphoma/leukemia virus type I (HTLV-I) derived from sequence analysis of a new HTLV-I variant from Papua New Guinea. J Virol. 1992 Apr;66(4):2556–2563. doi: 10.1128/jvi.66.4.2556-2563.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Song K. J., Nerurkar V. R., Saitou N., Lazo A., Blakeslee J. R., Miyoshi I., Yanagihara R. Genetic analysis and molecular phylogeny of simian T-cell lymphotropic virus type I: evidence for independent virus evolution in Asia and Africa. Virology. 1994 Feb 15;199(1):56–66. doi: 10.1006/viro.1994.1097. [DOI] [PubMed] [Google Scholar]
  27. Vandamme A. M., Liu H. F., Goubau P., Desmyter J. Primate T-lymphotropic virus type I LTR sequence variation and its phylogenetic analysis: compatibility with an African origin of PTLV-I. Virology. 1994 Jul;202(1):212–223. doi: 10.1006/viro.1994.1337. [DOI] [PubMed] [Google Scholar]
  28. Voevodin A. F., Lapin B. A., Tatosyan A. G., Hirsch I. Markers of HTLV-I-related virus in hamadryas baboon lymphoma. Haematol Blood Transfus. 1987;31:392–394. doi: 10.1007/978-3-642-72624-8_84. [DOI] [PubMed] [Google Scholar]
  29. Voevodin A. F., Lapin B. A., Yakovleva L. A., Ponomaryeva T. I., Oganyan T. E., Razmadze E. N. Antibodies reacting with human T-lymphotropic retrovirus (HTLV-I) or related antigens in lymphomatous and healthy hamadryas baboons. Int J Cancer. 1985 Nov 15;36(5):579–584. doi: 10.1002/ijc.2910360511. [DOI] [PubMed] [Google Scholar]
  30. Zil'ber L. A., Lapin B. A., Adzhigitov F. I., Shevliagin V. Ia, Iakovleva L. A. Induktsiia opukholei u obez'ian virusom rausa. Vopr Onkol. 1967;13(1):49–56. [PubMed] [Google Scholar]

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