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Non-human Primate Papillomaviruses Share Similar Evolutionary Histories and Niche Adaptation as the Human Counterparts
Given high genetic diversity of papillomaviruses (PV) and complex scenario of virus-host interaction, the genetic basis underlying the mechanisms of HPV carcinogenicity is not well understood. In an effort to evaluate the origin and evolution of PV pathogenicity, we collected paired oral, perianal,...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2019
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6747053/ https://www.ncbi.nlm.nih.gov/pubmed/31552003 http://dx.doi.org/10.3389/fmicb.2019.02093 |
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author | Chen, Zigui Long, Teng Wong, Po Yee Ho, Wendy C. S. Burk, Robert D. Chan, Paul K. S. |
author_facet | Chen, Zigui Long, Teng Wong, Po Yee Ho, Wendy C. S. Burk, Robert D. Chan, Paul K. S. |
author_sort | Chen, Zigui |
collection | PubMed |
description | Given high genetic diversity of papillomaviruses (PV) and complex scenario of virus-host interaction, the genetic basis underlying the mechanisms of HPV carcinogenicity is not well understood. In an effort to evaluate the origin and evolution of PV pathogenicity, we collected paired oral, perianal, and genital swabs from a wild macaque population. Of the 117 surveyed macaques, 88 (75.2%) were positive for PV DNA in one or more sites, mostly common from genital swabs, followed by oral and perianal sites. All putative macaque PV types phylogenetically clustered into the genera Alpha-, Beta-, and Gammapapillomavirus, with a strong phylogeny-tropism association as observed in HPVs. Using a Bayesian Markov Chain Monte Carlo framework, we demonstrated ancient intra-host divergence of primate PVs in which multiple ancestors had split and adapted to specific host ecosystems at least 41 million years ago, prior to the speciation events of primate host species. Following subsequent divergence and niche adaptation, distinct but phylogenetically related PV types were transmitted to similar host ecosystems by closely related host animals when host speciation occurred, which may explain in part the origin of carcinogenicity of HPV type 16 (HPV16) and Macaca fascicularis PV type 3 (MfPV3) that evolved from a most recent common ancestor containing the determinants for cervicovaginal colonization and cervical cancer. The findings identifying evolutionary and biological relatedness between human and non-human primate PVs lay a genetic foundation for research on parasite-host interactions and carcinogenic outcomes, which will prove useful in further study of viral pathogenesis and host specificity. STUDY IMPORTANCE: To better understand the origin and evolution of PV carcinogenicity associated with cervical cancer, we applied a combination of phylogenetic and bioinformatic analyses to investigate the genetic diversity of macaque papillomaviruses, and estimate divergence times of human and non-human primate PVs. The majority of both human and non-human primate PVs cluster into α-, β-, and γ-PVs, sharing similar evolutionary histories and biological properties to each other. The strong phylogeny-tropism association of primate PVs indicates an important role of niche adaptation and virus-host codivergence shaping the diversity of viral genomics, host specificity, immune exposure, and pathogenic property. Understanding the evolution of the family Papilloamviridae in general and the primate papillomaviruses in specific in relevant to virus-host interactions should provide important implications for viral pathogenesis and disease prevention. |
format | Online Article Text |
id | pubmed-6747053 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-67470532019-09-24 Non-human Primate Papillomaviruses Share Similar Evolutionary Histories and Niche Adaptation as the Human Counterparts Chen, Zigui Long, Teng Wong, Po Yee Ho, Wendy C. S. Burk, Robert D. Chan, Paul K. S. Front Microbiol Microbiology Given high genetic diversity of papillomaviruses (PV) and complex scenario of virus-host interaction, the genetic basis underlying the mechanisms of HPV carcinogenicity is not well understood. In an effort to evaluate the origin and evolution of PV pathogenicity, we collected paired oral, perianal, and genital swabs from a wild macaque population. Of the 117 surveyed macaques, 88 (75.2%) were positive for PV DNA in one or more sites, mostly common from genital swabs, followed by oral and perianal sites. All putative macaque PV types phylogenetically clustered into the genera Alpha-, Beta-, and Gammapapillomavirus, with a strong phylogeny-tropism association as observed in HPVs. Using a Bayesian Markov Chain Monte Carlo framework, we demonstrated ancient intra-host divergence of primate PVs in which multiple ancestors had split and adapted to specific host ecosystems at least 41 million years ago, prior to the speciation events of primate host species. Following subsequent divergence and niche adaptation, distinct but phylogenetically related PV types were transmitted to similar host ecosystems by closely related host animals when host speciation occurred, which may explain in part the origin of carcinogenicity of HPV type 16 (HPV16) and Macaca fascicularis PV type 3 (MfPV3) that evolved from a most recent common ancestor containing the determinants for cervicovaginal colonization and cervical cancer. The findings identifying evolutionary and biological relatedness between human and non-human primate PVs lay a genetic foundation for research on parasite-host interactions and carcinogenic outcomes, which will prove useful in further study of viral pathogenesis and host specificity. STUDY IMPORTANCE: To better understand the origin and evolution of PV carcinogenicity associated with cervical cancer, we applied a combination of phylogenetic and bioinformatic analyses to investigate the genetic diversity of macaque papillomaviruses, and estimate divergence times of human and non-human primate PVs. The majority of both human and non-human primate PVs cluster into α-, β-, and γ-PVs, sharing similar evolutionary histories and biological properties to each other. The strong phylogeny-tropism association of primate PVs indicates an important role of niche adaptation and virus-host codivergence shaping the diversity of viral genomics, host specificity, immune exposure, and pathogenic property. Understanding the evolution of the family Papilloamviridae in general and the primate papillomaviruses in specific in relevant to virus-host interactions should provide important implications for viral pathogenesis and disease prevention. Frontiers Media S.A. 2019-09-10 /pmc/articles/PMC6747053/ /pubmed/31552003 http://dx.doi.org/10.3389/fmicb.2019.02093 Text en Copyright © 2019 Chen, Long, Wong, Ho, Burk and Chan. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology Chen, Zigui Long, Teng Wong, Po Yee Ho, Wendy C. S. Burk, Robert D. Chan, Paul K. S. Non-human Primate Papillomaviruses Share Similar Evolutionary Histories and Niche Adaptation as the Human Counterparts |
title | Non-human Primate Papillomaviruses Share Similar Evolutionary Histories and Niche Adaptation as the Human Counterparts |
title_full | Non-human Primate Papillomaviruses Share Similar Evolutionary Histories and Niche Adaptation as the Human Counterparts |
title_fullStr | Non-human Primate Papillomaviruses Share Similar Evolutionary Histories and Niche Adaptation as the Human Counterparts |
title_full_unstemmed | Non-human Primate Papillomaviruses Share Similar Evolutionary Histories and Niche Adaptation as the Human Counterparts |
title_short | Non-human Primate Papillomaviruses Share Similar Evolutionary Histories and Niche Adaptation as the Human Counterparts |
title_sort | non-human primate papillomaviruses share similar evolutionary histories and niche adaptation as the human counterparts |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6747053/ https://www.ncbi.nlm.nih.gov/pubmed/31552003 http://dx.doi.org/10.3389/fmicb.2019.02093 |
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