Letter

Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes

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Abstract

The human AIDS viruses human immunodeficiency virus type 1 (HIV-1) and type 2 (HIV-2) represent cross-species (zoonotic) infections1,2,3,4. Although the primate reservoir of HIV-2 has been clearly identified as the sooty mangabey (Cercocebus atys)2,4,5,6,7, the origin of HIV-1 remains uncertain. Viruses related to HIV-1 have been isolated from the common chimpanzee (Pan troglodytes)8,9, but only three such SIVcpz infections have been documented1,10,11, one of which involved a virus so divergent11 that it might represent a different primate lentiviral lineage. In a search for the HIV-1 reservoir, we have now sequenced the genome of a new SIVcpz strain (SIVcpzUS) and have determined, by mitochondrial DNA analysis, the subspecies identity of all known SIVcpz-infected chimpanzees. We find that two chimpanzee subspecies in Africa, the central P. t. troglodytes and the eastern P. t. schweinfurthii, harbour SIVcpz and that their respective viruses form two highly divergent (but subspecies-specific) phylogenetic lineages. All HIV-1 strains known to infect man, including HIV-1 groups M, N and O, are closely related to just one of these SIVcpz lineages, that found in P. t. troglodytes. Moreover, we find that HIV-1 group N is a mosaic of SIVcpzUS- and HIV-1-related sequences, indicating an ancestral recombination event in a chimpanzee host. These results, together with the observation that the natural range of P. t. troglodytes coincides uniquely with areas of HIV-1 group M, N and O endemicity, indicate that P. t. troglodytes is the primary reservoir for HIV-1 and has been the source of at least three independent introductions of SIVcpz into the human population.

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References

  1. 1.

    , , , & Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature 345, 356–359 (1990).

  2. 2.

    , , , & An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339, 389–392 (1989).

  3. 3.

    , & Cross-species transmission and recombination of AIDS viruses. Phil. Trans. R. Soc. Lond. B 349, 41–47 (1995).

  4. 4.

    et al. Human infection by genetically-diverse SIVsm-related HIV-2 in west Africa. Nature 358, 495– 499 (1992).

  5. 5.

    et al. Genetic diversity of human immunodeficiency virus type 2: evidence for distinct sequence subtypes with differences in virus biology. J. Virol. 68, 7433–7447 (1994).

  6. 6.

    et al. Genetic characterization of a new west African simian immunodeficiency virus SIVsm: geographic clustering of household-derived SIV strains with human immunodeficiency virus type 2 subtypes and genetically diverse viruses from a single feral sooty mangabey troop. J. Virol. 70, 3617–3627 (1996).

  7. 7.

    et al. Human immunodeficiency virus type 2 (HIV-2) seroprevalence and characterization of a distinct HIV-2 genetic subtype from the natural range of SIV infected sooty mangabeys. J. Virol. 71, 3953–3960 (1997).

  8. 8.

    et al. Isolation and partial characterization of an HIV-related virus occurring naturally in chimpanzees in Gabon. AIDS 3 , 625–630 (1989).

  9. 9.

    et al. Isolation and characterization of a new chimpanzee lentivirus (simian immunodeficiency virus isolate cpz-ant) from a wild-captured chimpanzee. AIDS 6, 447–451 (1992).

  10. 10.

    et al. Phylogenetic analysis of a new chimpanzee lentivirus SIVcpz-gab2 from a wild-captured chimpanzee from Gabon. AIDS Res. Hum. Retroviruses 10, 1191–1192 (1994).

  11. 11.

    et al. Sequence analysis of a highly divergent HIV-1 related lentivirus isolated from a wild captured chimpanzee. Virology 221, 346–350 (1996).

  12. 12.

    et al. HTLV-III antibody in a breeding chimpanzee not experimentally exposed to the virus (letter). Lancet i, 678–679 (1986).

  13. 13.

    in Understanding Chimpanzees (eds Heltne, P. G. & Marquardt, L. A.) 312–353 (Harvard Univ. Press, London, (1989)).

  14. 14.

    et al. in Human Retroviruses and AIDS 1997: A Compilation and Analysis of Nucleic Acid and Amino Acid Sequences (Theoretical Biology and Biophysics Group, Los Alamos, New Mexico, (1997)).

  15. 15.

    et al. Identification of a new subgroup of SIVagm in tantalus monkeys. Virology 197, 426–430 (1993).

  16. 16.

    et al. Simian immunodeficiency viruses from central and western Africa: evidence for a new species-specific lentivirus in tantalus monkeys. J. Virol. 67, 1227–1235 (1993).

  17. 17.

    et al. Mosaic genome structure of simian immunodeficiency virus from west African green monkeys. EMBO J. 13, 2935–2947 (1994).

  18. 18.

    in Mammalian Species of World: A Taxonomic and Geographic Reference (eds Wilson, D. E. & Reader, D. M.) 243–277 (Smithsonian Institution Press, Washington DC, (1993)).

  19. 19.

    et al. Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265, 1193– 1201 (1994).

  20. 20.

    et al. Anew west African chimpanzee subspecies? Nature 388, 337 (1997).

  21. 21.

    , , & Origins and diversity of human immunodeficiency viruses. AIDS 8, S27–S42 (1994).

  22. 22.

    et al. HIV-1 subtype O: epidemiology, pathogenesis, diagnosis, and perspectives of the evolution of HIV. Arch. Virol. Suppl. 11, 195–202 (1996).

  23. 23.

    et al. Identification of a new human immunodeficiency virus type 1 distinct from group M and group O. Nature Med. 4, 1032–1037 (1998).

  24. 24.

    et al. An African HIV-1 sequence from 1959 and implications for the origin of the epidemic. Nature 391, 594– 597 (1998).

  25. 25.

    et al. Sequence and organization of the human mitochondrial genome. Nature 290, 457–465 (1981).

  26. 26.

    , , , & The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24, 4876– 4882 (1997).

  27. 27.

    & The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425 (1987).

  28. 28.

    & MOLPHY (a program package for MOLecular PHYlogenetics), version 2.2 (Institute of Statistical Mathematics, 4-6-7 Minami-Azabu, Minato-ku, Tokyo 106, Japan, (1994)).

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Acknowledgements

We thank P. Gagneux for mtDNA primer sequences; A. L. Rose, J. Moore and K.Ammann for information concerning chimpanzee hunting practices in west equatorial Africa; T.Goldberg, C. Boesch, R. W. Wrangham, J. Fritz and L. Brent for discussion; B. Jian for technical assistance; and W. J. Abbott and J. B. Wilson for artwork and manuscript preparation. This work was supported by grants from the National Institutes of Health, by shared facilities of the UAB Center for AIDS Research, and by the Birmingham Veterans Administration Medical Center.

Author information

Author notes

    • Scott F. Michael

    Present address: Department of Tropical Medicine, Tulane University, New Orleans, Louisiana 70112, USA.

Affiliations

  1. *Departments of Medicine and Microbiology, University of Alabama at Birmingham, 701 S. 19th Street, LHRB 613, Birmingham, Alabama 35294, USA

    • Feng Gao
    • , Yalu Chen
    • , Cynthia M. Rodenburg
    • , Scott F. Michael
    • , George M. Shaw
    •  & Beatrice H. Hahn
  2. †Institute of Genetics, University of Nottingham, Queens Medical Centre, Nottingham NG7 2UH , UK

    • Elizabeth Bailes
    •  & Paul M. Sharp
  3. ‡Laboratory of Structural and Genetic Information, CNRS, Marseilles 13402, France

    • David L. Robertson
  4. Southwest Foundation for Biomedical Research, San Antonio, Texas 78245, USA

    • Larry B. Cummins
  5. ¶AIDS Vaccine Program, National Cancer Institute-Frederick Cancer Research and Development Center, SAIC Frederick , Frederick, Maryland 21702, USA

    • Larry O. Arthur
  6. #Laboratoire Retrovirus, ORSTOM, BP 5045, Montpellier 34032, France

    • Martine Peeters
  7. Howard Hughes Medical Institute, University of Alabama at Birmingham, Birmingham, Alabama 35294, USA

    • George M. Shaw

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