Letter | Published:

An African HIV-1 sequence from 1959 and implications for the origin of the epidemic

Nature volume 391, pages 594597 (05 February 1998) | Download Citation

Subjects

Abstract

There is considerable genetic diversity among viruses of different subtypes (designated A to J) in the major group of human immunodeficiency virus type 1 (HIV-1), the form of HIV that is dominant in the global epidemic1,2,3. If available, HIV-1 sequences pre-dating the recognition of AIDS could be crucial in defining the time of origin and the subsequent evolution of these viruses in humans. The oldest known case of HIV-1 infection was reported to be that of a sailor from Manchester who died of an AIDS-like illness in 1959 (4,​5,​6); however, the authenticity of this case has not been confirmed7,8. Genetic analysis of sequences from clinical materials obtained from 1971 to 1976 from members of a Norwegian family infected earlier than 1971 showed that they carried viruses of the HIV-1 outlier group9,10, a variant form that is mainly restricted to West Africa1. Here we report the amplification and characterization of viral sequences from a 1959 African plasma sample that was previously found to be HIV-1 seropositive11. Multiple phylogenetic analyses not only authenticate this case as the oldest known HIV-1 infection, but also place its viral sequence near the ancestral node of subtypes B and D in the major group, indicating that these HIV-1 subtypes, and perhaps all major-group viruses, may have evolved from a single introduction into the African population not long before 1959.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    , , & Origins and diversity of human immunodeficiency viruses. AIDS 8, S27–S43 (1994).

  2. 2.

    et al. Molecular cloning and analysis of functional envelope genes from human immunodeficiency virus type 1 sequence subtypes A through G. J. Virol. 70, 1651–1667 (1996).

  3. 3.

    et al. Phylogenetic analysis of gag genes from 70 international HIV-1 isolates provides evidence for multiple genotypes. AIDS 7, 769–780 (1993).

  4. 4.

    , & Cytomegalic inclusion disease and pneumocystis carinii infection in an adult. Lancet ii, 951–955 (1960).

  5. 5.

    , & AIDS in 1959? Lancet ii, 1136 (1983).

  6. 6.

    , & HIV infection in Manchester, 1959. Lancet 336, 51 (1990).

  7. 7.

    & Was HIV present in 1959? Nature 374, 503–504 (1995).

  8. 8.

    & 1959 Manchester case of syndrome resembling AIDS. Lancet 348, 1363–1365 (1996).

  9. 9.

    et al. HIV-1 infection in Norwegian family before 1970. Lancet i, 1344–1345 (1988).

  10. 10.

    et al. Sequence analysis of HIV-1 group O from Norwegian patients infected in the 1960s. Virology 231, 43–47 (1997).

  11. 11.

    et al. Evidence for human infection with an HTLV-III/LAV-like virus in central Africa, 1959. Lancet i, 1279–1280 (1986).

  12. 12.

    et al. Population genetic studies in the Congo. 1. Glucose-6-phosphate dehydrogenase deficiency, hemoglobin S, and malaria. Am. J. Hum. Genet. 18, 514–537 (1966).

  13. 13.

    & Multiple aligned sequence editor (MASE). Trends Biochem. Sci. 13, 321–322 (1988).

  14. 14.

    , , & Basic local alignment search tool (BLAST). J. Mol. Biol. 215, 403–410 (1990).

  15. 15.

    , , & Recombination in HIV-1. Nature 374, 124–126 (1995).

  16. 16.

    , , & Acomputer program designed to rapidly screen for HIV-1 intersubtype recombinant sequences. AIDS Res. Hum. Retroviruses 11, 1413–1416 (1995).

  17. 17.

    , & Rates and dates of divergence between AIDS-virus nucleotide sequences. Mol. Biol. Evol. 5, 313–330 (1988).

  18. 18.

    An application of population genetic theory to synonymous gene sequence evolution in the human immunodeficiency virus (HIV). Genet. Res. 64, 1–9 (1994).

  19. 19.

    , & Intrahost human immunodeficiency virus type 1 evolution is related to length of the immunocompetent period. J. Virol. 69, 6911–6916 (1995).

  20. 20.

    et al. Adaptive evolution of human immunodeficiency virus type 1 during the natural course of infection. Science 277, 537–542 (1996).

  21. 21.

    & Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J. Mol. Evol. 29, 170–179 (1989).

  22. 22.

    , , , & Accurate reconstruction of a known HIV-1 transmission history by phylogenetic tree analysis. Proc. Natl Acad. Sci. USA 93, 10864–10869 (1996).

  23. 23.

    Viral Sex: the Nature of AIDS. (Oxford Univ. Press, 1997).

  24. 24.

    , & Tempo and mode of nucleotide substitutions in gag and env gene fragments in human immunodeficiency virus type 1 populations with a known transmission history. J. Virol. 71, 4761–4770 (1997).

  25. 25.

    , , , & The phylogenetic history of immunodeficiency viruses. Nature 333, 573–575 (1988).

  26. 26.

    & Understanding the origins of AIDS viruses. Nature 336, 315 (1988).

  27. 27.

    & How old is the immunodeficiency virus? AIDS 4 (suppl.)S85–S93 (1990).

  28. 28.

    et al. Evolutionary origin of human and simian immunodeficiency viruses. Proc. Natl Acad. Sci. USA 87, 4108–4111 (1990).

  29. 29.

    , , & fastDNAml: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput. Appl. Biosci. 10, 41–48 (1994).

  30. 30.

    Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17, 368–376 (1981).

Download references

Acknowledgements

We thank J. Felsenstein for an early release of PHYLIP 3.6 and for helpful suggestions, T. Leitner for advice, and G. Olsen for providing DNA rates and a preprint describing a method for estimating the relative rates of variation at each site. This study was supported by grants from the NIH, the Magic Johnson Foundation and the Irene Diamond Fund, and by donations from D. Pels, A.Gund and V. D. Adler.

Author information

Author notes

    • Tuofu Zhu

    Present address: University of Washington, Health Sciences Building, Room T239X, 1959 NE Pacific Avenue, Seattle, Washington DC 98195, USA.

Affiliations

  1. *Aaron Diamond AIDS Research Center, The Rockefeller University, 455 First Avenue, New York, New York 10016, USA

    • Tuofu Zhu
    •  & David D. Ho
  2. ‡Theoretical Division, Los Alamos National Laboratory, Los Alamos, New Mexico 87545, USA

    • Bette T. Korber
  3. §The Santa Fe Institute, Santa Fe, New Mexico 87501, USA

    • Bette T. Korber
  4. Department of Pediatrics, Emory University School of Medicine, Atlanta, Georgia 30303, USA

    • Andre J. Nahmias
  5. ¶PO Box 4087, Worthing BN14 7LQ, UK

    • Edward Hooper
  6. #Department of Genetics, University of Nottingham, Queens Medical Centre, Nottingham NG7 2UH, UK

    • Paul M. Sharp

Authors

  1. Search for Tuofu Zhu in:

  2. Search for Bette T. Korber in:

  3. Search for Andre J. Nahmias in:

  4. Search for Edward Hooper in:

  5. Search for Paul M. Sharp in:

  6. Search for David D. Ho in:

Corresponding author

Correspondence to David D. Ho.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/35400

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.