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Phyloepidemiological Analysis Reveals that Viral Divergence Led to the Paucity of Simian Immunodeficiency Virus SIVmus/gsn/mon Infections in Wild Populations

Human immunodeficiency virus type 1 (HIV-1) is the result of cross-species transmission of simian immunodeficiency virus from chimpanzees (SIVcpz). SIVcpz is a chimeric virus which shares common ancestors with viruses infecting red-capped mangabeys and a subset of guenon species. The epidemiology of...

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Autores principales: Schmidt, Fabian, Liegeois, Florian, Greenwood, Edward J. D., LeBreton, Matthew, Lester, James, Deleplancque, Luc, Peeters, Martine, Aghokeng, Avelin, Tamoufe, Ubald, Diffo, Joseph L. D., Takuo, Jean M., Wolfe, Nathan D., Leroy, Eric, Rouet, François, Heeney, Jonathan L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5331790/
https://www.ncbi.nlm.nih.gov/pubmed/28077632
http://dx.doi.org/10.1128/JVI.01884-16
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author Schmidt, Fabian
Liegeois, Florian
Greenwood, Edward J. D.
LeBreton, Matthew
Lester, James
Deleplancque, Luc
Peeters, Martine
Aghokeng, Avelin
Tamoufe, Ubald
Diffo, Joseph L. D.
Takuo, Jean M.
Wolfe, Nathan D.
Leroy, Eric
Rouet, François
Heeney, Jonathan L.
author_facet Schmidt, Fabian
Liegeois, Florian
Greenwood, Edward J. D.
LeBreton, Matthew
Lester, James
Deleplancque, Luc
Peeters, Martine
Aghokeng, Avelin
Tamoufe, Ubald
Diffo, Joseph L. D.
Takuo, Jean M.
Wolfe, Nathan D.
Leroy, Eric
Rouet, François
Heeney, Jonathan L.
author_sort Schmidt, Fabian
collection PubMed
description Human immunodeficiency virus type 1 (HIV-1) is the result of cross-species transmission of simian immunodeficiency virus from chimpanzees (SIVcpz). SIVcpz is a chimeric virus which shares common ancestors with viruses infecting red-capped mangabeys and a subset of guenon species. The epidemiology of SIV infection in hominoids is characterized by low prevalences and an uneven geographic distribution. Surveys in Cameroon indicated that two closely related members of the guenon species subset, mustached guenons and greater spot-nosed guenons, infected with SIVmus and SIVgsn, respectively, also have low rates of SIV infections in their populations. Compared to that for other monkeys, including red-capped mangabeys and closely related guenon species, such an epidemiology is unusual. By intensifying sampling of geographically distinct populations of mustached and greater spot-nosed guenons in Gabon and including large sample sets of mona guenons from Cameroon, we add strong support to the hypothesis that the paucity of SIV infections in wild populations is a general feature of this monophyletic group of viruses. Furthermore, comparative phylogenetic analysis reveals that this phenotype is a feature of this group of viruses infecting phylogenetically disparate hosts, suggesting that this epidemiological phenotype results from infection with these HIV-1-related viruses rather than from a common host factor. Thus, these HIV-1-related viruses, i.e., SIVcpz and the guenon viruses which share an ancestor with part of the SIVcpz genome, have an epidemiology distinct from that found for SIVs in other African primate species. IMPORTANCE Stable virus-host relationships are established over multiple generations. The prevalence of viral infections in any given host is determined by various factors. Stable virus-host relationships of viruses that are able to cause persistent infections and exist with high incidences of infection are generally characterized by a lack of morbidity prior to host reproduction. Such is the case for cytomegalovirus (CMV) and Epstein-Barr virus (EBV) infections of humans. SIV infections of most African primate species also satisfy these criteria, with these infections found at a high prevalence and with rare cases of clinical disease. In contrast, SIVcpz, the ancestor of HIV-1, has a different epidemiology, and it has been reported that infected animals suffer from an AIDS-like disease in the wild. Here we conclusively demonstrate that viruses which are closely related to SIVcpz and infect a subset of guenon monkeys show an epidemiology resembling that of SIVcpz.
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spelling pubmed-53317902017-03-13 Phyloepidemiological Analysis Reveals that Viral Divergence Led to the Paucity of Simian Immunodeficiency Virus SIVmus/gsn/mon Infections in Wild Populations Schmidt, Fabian Liegeois, Florian Greenwood, Edward J. D. LeBreton, Matthew Lester, James Deleplancque, Luc Peeters, Martine Aghokeng, Avelin Tamoufe, Ubald Diffo, Joseph L. D. Takuo, Jean M. Wolfe, Nathan D. Leroy, Eric Rouet, François Heeney, Jonathan L. J Virol Genetic Diversity and Evolution Human immunodeficiency virus type 1 (HIV-1) is the result of cross-species transmission of simian immunodeficiency virus from chimpanzees (SIVcpz). SIVcpz is a chimeric virus which shares common ancestors with viruses infecting red-capped mangabeys and a subset of guenon species. The epidemiology of SIV infection in hominoids is characterized by low prevalences and an uneven geographic distribution. Surveys in Cameroon indicated that two closely related members of the guenon species subset, mustached guenons and greater spot-nosed guenons, infected with SIVmus and SIVgsn, respectively, also have low rates of SIV infections in their populations. Compared to that for other monkeys, including red-capped mangabeys and closely related guenon species, such an epidemiology is unusual. By intensifying sampling of geographically distinct populations of mustached and greater spot-nosed guenons in Gabon and including large sample sets of mona guenons from Cameroon, we add strong support to the hypothesis that the paucity of SIV infections in wild populations is a general feature of this monophyletic group of viruses. Furthermore, comparative phylogenetic analysis reveals that this phenotype is a feature of this group of viruses infecting phylogenetically disparate hosts, suggesting that this epidemiological phenotype results from infection with these HIV-1-related viruses rather than from a common host factor. Thus, these HIV-1-related viruses, i.e., SIVcpz and the guenon viruses which share an ancestor with part of the SIVcpz genome, have an epidemiology distinct from that found for SIVs in other African primate species. IMPORTANCE Stable virus-host relationships are established over multiple generations. The prevalence of viral infections in any given host is determined by various factors. Stable virus-host relationships of viruses that are able to cause persistent infections and exist with high incidences of infection are generally characterized by a lack of morbidity prior to host reproduction. Such is the case for cytomegalovirus (CMV) and Epstein-Barr virus (EBV) infections of humans. SIV infections of most African primate species also satisfy these criteria, with these infections found at a high prevalence and with rare cases of clinical disease. In contrast, SIVcpz, the ancestor of HIV-1, has a different epidemiology, and it has been reported that infected animals suffer from an AIDS-like disease in the wild. Here we conclusively demonstrate that viruses which are closely related to SIVcpz and infect a subset of guenon monkeys show an epidemiology resembling that of SIVcpz. American Society for Microbiology 2017-02-28 /pmc/articles/PMC5331790/ /pubmed/28077632 http://dx.doi.org/10.1128/JVI.01884-16 Text en Copyright © 2017 Schmidt et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Genetic Diversity and Evolution
Schmidt, Fabian
Liegeois, Florian
Greenwood, Edward J. D.
LeBreton, Matthew
Lester, James
Deleplancque, Luc
Peeters, Martine
Aghokeng, Avelin
Tamoufe, Ubald
Diffo, Joseph L. D.
Takuo, Jean M.
Wolfe, Nathan D.
Leroy, Eric
Rouet, François
Heeney, Jonathan L.
Phyloepidemiological Analysis Reveals that Viral Divergence Led to the Paucity of Simian Immunodeficiency Virus SIVmus/gsn/mon Infections in Wild Populations
title Phyloepidemiological Analysis Reveals that Viral Divergence Led to the Paucity of Simian Immunodeficiency Virus SIVmus/gsn/mon Infections in Wild Populations
title_full Phyloepidemiological Analysis Reveals that Viral Divergence Led to the Paucity of Simian Immunodeficiency Virus SIVmus/gsn/mon Infections in Wild Populations
title_fullStr Phyloepidemiological Analysis Reveals that Viral Divergence Led to the Paucity of Simian Immunodeficiency Virus SIVmus/gsn/mon Infections in Wild Populations
title_full_unstemmed Phyloepidemiological Analysis Reveals that Viral Divergence Led to the Paucity of Simian Immunodeficiency Virus SIVmus/gsn/mon Infections in Wild Populations
title_short Phyloepidemiological Analysis Reveals that Viral Divergence Led to the Paucity of Simian Immunodeficiency Virus SIVmus/gsn/mon Infections in Wild Populations
title_sort phyloepidemiological analysis reveals that viral divergence led to the paucity of simian immunodeficiency virus sivmus/gsn/mon infections in wild populations
topic Genetic Diversity and Evolution
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5331790/
https://www.ncbi.nlm.nih.gov/pubmed/28077632
http://dx.doi.org/10.1128/JVI.01884-16
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