Origin of the HIV-1 group O epidemic in western lowland gorillas

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 11; pp. E1343 - E1352
• Main Authors: D’arc, Mirela, Ayouba, Ahidjo, Esteban, Amandine, Learn, Gerald H., Boué, Vanina, Liegeois, Florian, Etienne, Lucie, Tagg, Nikki, Leendertz, Fabian H., Boesch, Christophe, Madinda, Nadège F., Robbins, Martha M., Gray, Maryke, Cournil, Amandine, Ooms, Marcel, Letko, Michael, Simon, Viviana A., Sharp, Paul M., Hahn, Beatrice H., Delaporte, Eric, Ngole, Eitel Mpoudi, Peeters, Martine
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 17.03.2015; National Acad Sciences
• Series: PNAS Plus
• Subjects: 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; Cameroon; Gabon; Uganda; Africa; HIV-1; gorilla; AIDS; SIVgor; zoonotic transmission
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1502022112

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.