Origin of the HIV-1 group O epidemic in western lowland gorillas
Significance Understanding emerging disease origins is important to gauge future human infection risks. This is particularly true for the various forms of the AIDS virus, HIV-1, which were transmitted to humans on four independent occasions. Previous studies identified chimpanzees in southern Camero...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 11; pp. E1343 - E1352 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
17.03.2015
National Acad Sciences |
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Significance Understanding emerging disease origins is important to gauge future human infection risks. This is particularly true for the various forms of the AIDS virus, HIV-1, which were transmitted to humans on four independent occasions. Previous studies identified chimpanzees in southern Cameroon as the source of the pandemic M group, as well as the geographically more restricted N group. Here, we show that the remaining two groups also emerged in southern Cameroon but had their origins in western lowland gorillas. Although group P has only been detected in two individuals, group O has spread extensively throughout west central Africa. Thus, both chimpanzees and gorillas harbor viruses that are capable of crossing the species barrier to humans and causing major disease outbreaks.
HIV-1, the cause of AIDS, is composed of four phylogenetic lineages, groups M, N, O, and P, each of which resulted from an independent cross-species transmission event of simian immunodeficiency viruses (SIVs) infecting African apes. Although groups M and N have been traced to geographically distinct chimpanzee communities in southern Cameroon, the reservoirs of groups O and P remain unknown. Here, we screened fecal samples from western lowland ( n = 2,611), eastern lowland ( n = 103), and mountain ( n = 218) gorillas for gorilla SIV (SIVgor) antibodies and nucleic acids. Despite testing wild troops throughout southern Cameroon ( n = 14), northern Gabon ( n = 16), the Democratic Republic of Congo ( n = 2), and Uganda ( n = 1), SIVgor was identified at only four sites in southern Cameroon, with prevalences ranging from 0.8–22%. Amplification of partial and full-length SIVgor sequences revealed extensive genetic diversity, but all SIVgor strains were derived from a single lineage within the chimpanzee SIV (SIVcpz) radiation. Two fully sequenced gorilla viruses from southwestern Cameroon were very closely related to, and likely represent the source population of, HIV-1 group P. Most of the genome of a third SIVgor strain, from central Cameroon, was very closely related to HIV-1 group O, again pointing to gorillas as the immediate source. Functional analyses identified the cytidine deaminase APOBEC3G as a barrier for chimpanzee-to-gorilla, but not gorilla-to-human, virus transmission. These data indicate that HIV-1 group O, which spreads epidemically in west central Africa and is estimated to have infected around 100,000 people, originated by cross-species transmission from western lowland gorillas. |
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| AbstractList | Significance Understanding emerging disease origins is important to gauge future human infection risks. This is particularly true for the various forms of the AIDS virus, HIV-1, which were transmitted to humans on four independent occasions. Previous studies identified chimpanzees in southern Cameroon as the source of the pandemic M group, as well as the geographically more restricted N group. Here, we show that the remaining two groups also emerged in southern Cameroon but had their origins in western lowland gorillas. Although group P has only been detected in two individuals, group O has spread extensively throughout west central Africa. Thus, both chimpanzees and gorillas harbor viruses that are capable of crossing the species barrier to humans and causing major disease outbreaks.
HIV-1, the cause of AIDS, is composed of four phylogenetic lineages, groups M, N, O, and P, each of which resulted from an independent cross-species transmission event of simian immunodeficiency viruses (SIVs) infecting African apes. Although groups M and N have been traced to geographically distinct chimpanzee communities in southern Cameroon, the reservoirs of groups O and P remain unknown. Here, we screened fecal samples from western lowland ( n = 2,611), eastern lowland ( n = 103), and mountain ( n = 218) gorillas for gorilla SIV (SIVgor) antibodies and nucleic acids. Despite testing wild troops throughout southern Cameroon ( n = 14), northern Gabon ( n = 16), the Democratic Republic of Congo ( n = 2), and Uganda ( n = 1), SIVgor was identified at only four sites in southern Cameroon, with prevalences ranging from 0.8–22%. Amplification of partial and full-length SIVgor sequences revealed extensive genetic diversity, but all SIVgor strains were derived from a single lineage within the chimpanzee SIV (SIVcpz) radiation. Two fully sequenced gorilla viruses from southwestern Cameroon were very closely related to, and likely represent the source population of, HIV-1 group P. Most of the genome of a third SIVgor strain, from central Cameroon, was very closely related to HIV-1 group O, again pointing to gorillas as the immediate source. Functional analyses identified the cytidine deaminase APOBEC3G as a barrier for chimpanzee-to-gorilla, but not gorilla-to-human, virus transmission. These data indicate that HIV-1 group O, which spreads epidemically in west central Africa and is estimated to have infected around 100,000 people, originated by cross-species transmission from western lowland gorillas. Understanding emerging disease origins is important to gauge future human infection risks. This is particularly true for the various forms of the AIDS virus, HIV-1, which were transmitted to humans on four independent occasions. Previous studies identified chimpanzees in southern Cameroon as the source of the pandemic M group, as well as the geographically more restricted N group. Here, we show that the remaining two groups also emerged in southern Cameroon but had their origins in western lowland gorillas. Although group P has only been detected in two individuals, group O has spread extensively throughout west central Africa. Thus, both chimpanzees and gorillas harbor viruses that are capable of crossing the species barrier to humans and causing major disease outbreaks. HIV-1, the cause of AIDS, is composed of four phylogenetic lineages, groups M, N, O, and P, each of which resulted from an independent cross-species transmission event of simian immunodeficiency viruses (SIVs) infecting African apes. Although groups M and N have been traced to geographically distinct chimpanzee communities in southern Cameroon, the reservoirs of groups O and P remain unknown. Here, we screened fecal samples from western lowland ( n = 2,611), eastern lowland ( n = 103), and mountain ( n = 218) gorillas for gorilla SIV (SIVgor) antibodies and nucleic acids. Despite testing wild troops throughout southern Cameroon ( n = 14), northern Gabon ( n = 16), the Democratic Republic of Congo ( n = 2), and Uganda ( n = 1), SIVgor was identified at only four sites in southern Cameroon, with prevalences ranging from 0.8–22%. Amplification of partial and full-length SIVgor sequences revealed extensive genetic diversity, but all SIVgor strains were derived from a single lineage within the chimpanzee SIV (SIVcpz) radiation. Two fully sequenced gorilla viruses from southwestern Cameroon were very closely related to, and likely represent the source population of, HIV-1 group P. Most of the genome of a third SIVgor strain, from central Cameroon, was very closely related to HIV-1 group O, again pointing to gorillas as the immediate source. Functional analyses identified the cytidine deaminase APOBEC3G as a barrier for chimpanzee-to-gorilla, but not gorilla-to-human, virus transmission. These data indicate that HIV-1 group O, which spreads epidemically in west central Africa and is estimated to have infected around 100,000 people, originated by cross-species transmission from western lowland gorillas. HIV-1, the cause of AIDS, is composed of four phylogenetic lineages, groups M, N, O, and P, each of which resulted from an independent cross-species transmission event of simian immunodeficiency viruses (SIVs) infecting African apes. Although groups M and N have been traced to geographically distinct chimpanzee communities in southern Cameroon, the reservoirs of groups O and P remain unknown. Here, we screened fecal samples from western lowland ( n = 2,611), eastern lowland ( n = 103), and mountain ( n = 218) gorillas for gorilla SIV (SIVgor) antibodies and nucleic acids. Despite testing wild troops throughout southern Cameroon ( n = 14), northern Gabon ( n = 16), the Democratic Republic of Congo ( n = 2), and Uganda ( n = 1), SIVgor was identified at only four sites in southern Cameroon, with prevalences ranging from 0.8–22%. Amplification of partial and full-length SIVgor sequences revealed extensive genetic diversity, but all SIVgor strains were derived from a single lineage within the chimpanzee SIV (SIVcpz) radiation. Two fully sequenced gorilla viruses from southwestern Cameroon were very closely related to, and likely represent the source population of, HIV-1 group P. Most of the genome of a third SIVgor strain, from central Cameroon, was very closely related to HIV-1 group O, again pointing to gorillas as the immediate source. Functional analyses identified the cytidine deaminase APOBEC3G as a barrier for chimpanzee-to-gorilla, but not gorilla-to-human, virus transmission. These data indicate that HIV-1 group O, which spreads epidemically in west central Africa and is estimated to have infected around 100,000 people, originated by cross-species transmission from western lowland gorillas. HIV-1, the cause of AIDS, is composed of four phylogenetic lineages, groups M, N, O, and P, each of which resulted from an independent cross-species transmission event of simian immunodeficiency viruses (SIVs) infecting African apes. Although groups M and N have been traced to geographically distinct chimpanzee communities in southern Cameroon, the reservoirs of groups O and P remain unknown. Here, we screened fecal samples from western lowland (n = 2,611), eastern lowland (n = 103), and mountain (n = 218) gorillas for gorilla SIV (SIVgor) antibodies and nucleic acids. Despite testing wild troops throughout southern Cameroon (n = 14), northern Gabon (n = 16), the Democratic Republic of Congo (n = 2), and Uganda (n = 1), SIVgor was identified at only four sites in southern Cameroon, with prevalences ranging from 0.8-22%. Amplification of partial and full-length SIVgor sequences revealed extensive genetic diversity, but all SIVgor strains were derived from a single lineage within the chimpanzee SIV (SIVcpz) radiation. Two fully sequenced gorilla viruses from southwestern Cameroon were very closely related to, and likely represent the source population of, HIV-1 group P. Most of the genome of a third SIVgor strain, from central Cameroon, was very closely related to HIV-1 group O, again pointing to gorillas as the immediate source. Functional analyses identified the cytidine deaminase APOBEC3G as a barrier for chimpanzee-to-gorilla, but not gorilla-to-human, virus transmission. These data indicate that HIV-1 group O, which spreads epidemically in west central Africa and is estimated to have infected around 100,000 people, originated by cross-species transmission from western lowland gorillas.HIV-1, the cause of AIDS, is composed of four phylogenetic lineages, groups M, N, O, and P, each of which resulted from an independent cross-species transmission event of simian immunodeficiency viruses (SIVs) infecting African apes. Although groups M and N have been traced to geographically distinct chimpanzee communities in southern Cameroon, the reservoirs of groups O and P remain unknown. Here, we screened fecal samples from western lowland (n = 2,611), eastern lowland (n = 103), and mountain (n = 218) gorillas for gorilla SIV (SIVgor) antibodies and nucleic acids. Despite testing wild troops throughout southern Cameroon (n = 14), northern Gabon (n = 16), the Democratic Republic of Congo (n = 2), and Uganda (n = 1), SIVgor was identified at only four sites in southern Cameroon, with prevalences ranging from 0.8-22%. Amplification of partial and full-length SIVgor sequences revealed extensive genetic diversity, but all SIVgor strains were derived from a single lineage within the chimpanzee SIV (SIVcpz) radiation. Two fully sequenced gorilla viruses from southwestern Cameroon were very closely related to, and likely represent the source population of, HIV-1 group P. Most of the genome of a third SIVgor strain, from central Cameroon, was very closely related to HIV-1 group O, again pointing to gorillas as the immediate source. Functional analyses identified the cytidine deaminase APOBEC3G as a barrier for chimpanzee-to-gorilla, but not gorilla-to-human, virus transmission. These data indicate that HIV-1 group O, which spreads epidemically in west central Africa and is estimated to have infected around 100,000 people, originated by cross-species transmission from western lowland gorillas. |
| Author | Robbins, Martha M. Boesch, Christophe Esteban, Amandine Letko, Michael Ngole, Eitel Mpoudi Tagg, Nikki Peeters, Martine Simon, Viviana A. Liegeois, Florian Leendertz, Fabian H. Hahn, Beatrice H. Ooms, Marcel Sharp, Paul M. Etienne, Lucie Madinda, Nadège F. D’arc, Mirela Boué, Vanina Learn, Gerald H. Gray, Maryke Cournil, Amandine Delaporte, Eric Ayouba, Ahidjo |
| Author_xml | – sequence: 1 givenname: Mirela surname: D’arc fullname: D’arc, Mirela organization: Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France; Laboratory of Human Virology, Universidade Federal do Rio de Janeiro, 21949-570 Rio de Janeiro, Brazil – sequence: 2 givenname: Ahidjo surname: Ayouba fullname: Ayouba, Ahidjo organization: Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France – sequence: 3 givenname: Amandine surname: Esteban fullname: Esteban, Amandine organization: Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France – sequence: 4 givenname: Gerald H. surname: Learn fullname: Learn, Gerald H. organization: Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104 – sequence: 5 givenname: Vanina surname: Boué fullname: Boué, Vanina organization: Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France; Centre International de Recherches Médicales, Franceville, Gabon – sequence: 6 givenname: Florian surname: Liegeois fullname: Liegeois, Florian organization: Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France; Centre International de Recherches Médicales, Franceville, Gabon – sequence: 7 givenname: Lucie surname: Etienne fullname: Etienne, Lucie organization: Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France – sequence: 8 givenname: Nikki surname: Tagg fullname: Tagg, Nikki organization: Projet Grands Singes, Center for Research and Conservation, Royal Zoological Society of Antwerp, 2018 Antwerp, Belgium – sequence: 9 givenname: Fabian H. surname: Leendertz fullname: Leendertz, Fabian H. organization: Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, 13353 Berlin, Germany – sequence: 10 givenname: Christophe surname: Boesch fullname: Boesch, Christophe organization: Department of Primatology, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany – sequence: 11 givenname: Nadège F. surname: Madinda fullname: Madinda, Nadège F. organization: Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, 13353 Berlin, Germany; Department of Primatology, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany; Institut de Recherche en Ecologie Tropicale, Libreville, Gabon – sequence: 12 givenname: Martha M. surname: Robbins fullname: Robbins, Martha M. organization: Department of Primatology, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany – sequence: 13 givenname: Maryke surname: Gray fullname: Gray, Maryke organization: International Gorilla Conservation Programme, Kigali, Rwanda – sequence: 14 givenname: Amandine surname: Cournil fullname: Cournil, Amandine organization: Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France – sequence: 15 givenname: Marcel surname: Ooms fullname: Ooms, Marcel organization: Department of Microbiology, Global Health and Emerging Pathogens Institute, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029 – sequence: 16 givenname: Michael surname: Letko fullname: Letko, Michael organization: Department of Microbiology, Global Health and Emerging Pathogens Institute, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029 – sequence: 17 givenname: Viviana A. surname: Simon fullname: Simon, Viviana A. organization: Department of Microbiology, Global Health and Emerging Pathogens Institute, Division of Infectious Diseases, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029 – sequence: 18 givenname: Paul M. surname: Sharp fullname: Sharp, Paul M. organization: Institute of Evolutionary Biology, and Center for Immunity, Infection, and Evolution, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom – sequence: 19 givenname: Beatrice H. surname: Hahn fullname: Hahn, Beatrice H. organization: Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104 – sequence: 20 givenname: Eric surname: Delaporte fullname: Delaporte, Eric organization: Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France – sequence: 21 givenname: Eitel Mpoudi surname: Ngole fullname: Ngole, Eitel Mpoudi organization: Institut de Recherches Médicales et d’Études des Plantes Médicinales, Prévention du Sida au Cameroun, Yaoundé, Cameroon – sequence: 22 givenname: Martine surname: Peeters fullname: Peeters, Martine organization: Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France; Computational Biology Institute, 34095 Montpellier, France |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25733890$$D View this record in MEDLINE/PubMed https://hal.umontpellier.fr/hal-02057839$$DView record in HAL |
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| Copyright_xml | – notice: Volumes 1–89 and 106–112, copyright as a collective work only; author(s) retains copyright to individual articles – notice: Copyright National Academy of Sciences Mar 17, 2015 – notice: Distributed under a Creative Commons Attribution 4.0 International License |
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| DOI | 10.1073/pnas.1502022112 |
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| DocumentTitleAlternate | Gorilla origin of the HIV-1 group O |
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| Keywords | HIV-1 gorilla AIDS SIVgor zoonotic transmission |
| Language | English |
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| Notes | http://dx.doi.org/10.1073/pnas.1502022112 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 PMCID: PMC4371950 1Present address: International Center for Infectiology Research, INSERM U1111 and Ecole Normale Supérieure de Lyon and Université Claude Bernard Lyon 1 and CNRS UMR 5308, 69364 Lyon, France. Contributed by Beatrice H. Hahn, February 2, 2015 (sent for review December 16, 2014; reviewed by Catherine A. Brennan and Tony L. Goldberg) Reviewers: C.A.B., Abbott Diagnostics; and T.L.G., University of Wisconsin. Author contributions: M.D., A.A., P.M.S., B.H.H., E.D., E.M.N., and M.P. designed research; M.D., A.A., A.E., V.B., F.L., L.E., M.O., M.L., and V.A.S. performed research; V.B., F.L., N.T., F.H.L., C.B., N.F.M., M.M.R., M.G., and E.M.N. contributed new reagents/analytic tools; M.D., A.A., G.H.L., A.C., M.O., M.L., V.A.S., and M.P. analyzed data; and M.D., A.A., P.M.S., B.H.H., and M.P. wrote the paper. |
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| Snippet | Significance Understanding emerging disease origins is important to gauge future human infection risks. This is particularly true for the various forms of the... HIV-1, the cause of AIDS, is composed of four phylogenetic lineages, groups M, N, O, and P, each of which resulted from an independent cross-species... Understanding emerging disease origins is important to gauge future human infection risks. This is particularly true for the various forms of the AIDS virus,... |
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| SubjectTerms | Acquired immune deficiency syndrome AIDS Animals Animals, Wild - virology Antibodies, Viral - immunology Biological Evolution Biological Sciences Cameroon Cameroon - epidemiology crossing Cytidine Deaminase - metabolism emerging diseases Epidemics Feces - virology Genetic diversity Genetic Variation Genome - genetics Geography Gorilla Gorilla gorilla - virology Gorillas HIV HIV-1 - physiology human diseases Human immunodeficiency virus Human immunodeficiency virus 1 Humans Life Sciences Molecular Sequence Data Nucleic acids Pan troglodytes pandemic Phylogenetics Phylogeny PNAS Plus Proteolysis risk Santé publique et épidémiologie Sequence Analysis, DNA Simian Acquired Immunodeficiency Syndrome - epidemiology Simian Acquired Immunodeficiency Syndrome - immunology Simian Acquired Immunodeficiency Syndrome - virology Simian immunodeficiency virus Simian Immunodeficiency Virus - immunology viruses |
| Title | Origin of the HIV-1 group O epidemic in western lowland gorillas |
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