Cargando…
New World feline APOBEC3 potently controls inter-genus lentiviral transmission
BACKGROUND: The apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3 (APOBEC3; A3) gene family appears only in mammalian genomes. Some A3 proteins can be incorporated into progeny virions and inhibit lentiviral replication. In turn, the lentiviral viral infectivity factor (Vif) countera...
Autores principales: | , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2018
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5894237/ https://www.ncbi.nlm.nih.gov/pubmed/29636069 http://dx.doi.org/10.1186/s12977-018-0414-5 |
_version_ | 1783313461606875136 |
---|---|
author | Konno, Yoriyuki Nagaoka, Shumpei Kimura, Izumi Yamamoto, Keisuke Kagawa, Yumiko Kumata, Ryuichi Aso, Hirofumi Ueda, Mahoko Takahashi Nakagawa, So Kobayashi, Tomoko Koyanagi, Yoshio Sato, Kei |
author_facet | Konno, Yoriyuki Nagaoka, Shumpei Kimura, Izumi Yamamoto, Keisuke Kagawa, Yumiko Kumata, Ryuichi Aso, Hirofumi Ueda, Mahoko Takahashi Nakagawa, So Kobayashi, Tomoko Koyanagi, Yoshio Sato, Kei |
author_sort | Konno, Yoriyuki |
collection | PubMed |
description | BACKGROUND: The apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3 (APOBEC3; A3) gene family appears only in mammalian genomes. Some A3 proteins can be incorporated into progeny virions and inhibit lentiviral replication. In turn, the lentiviral viral infectivity factor (Vif) counteracts the A3-mediated antiviral effect by degrading A3 proteins. Recent investigations have suggested that lentiviral vif genes evolved to combat mammalian APOBEC3 proteins, and have further proposed that the Vif-A3 interaction may help determine the co-evolutionary history of cross-species lentiviral transmission in mammals. RESULTS: Here we address the co-evolutionary relationship between two New World felids, the puma (Puma concolor) and the bobcat (Lynx rufus), and their lentiviruses, which are designated puma lentiviruses (PLVs). We demonstrate that PLV-A Vif counteracts the antiviral action of APOBEC3Z3 (A3Z3) of both puma and bobcat, whereas PLV-B Vif counteracts only puma A3Z3. The species specificity of PLV-B Vif is irrespective of the phylogenic relationships of feline species in the genera Puma, Lynx and Acinonyx. We reveal that the amino acid at position 178 in the puma and bobcat A3Z3 is exposed on the protein surface and determines the sensitivity to PLV-B Vif-mediated degradation. Moreover, although both the puma and bobcat A3Z3 genes are polymorphic, their sensitivity/resistance to PLV Vif-mediated degradation is conserved. CONCLUSIONS: To the best of our knowledge, this is the first study suggesting that the host A3 protein potently controls inter-genus lentiviral transmission. Our findings provide the first evidence suggesting that the co-evolutionary arms race between lentiviruses and mammals has occurred in the New World. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12977-018-0414-5) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-5894237 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-58942372018-04-12 New World feline APOBEC3 potently controls inter-genus lentiviral transmission Konno, Yoriyuki Nagaoka, Shumpei Kimura, Izumi Yamamoto, Keisuke Kagawa, Yumiko Kumata, Ryuichi Aso, Hirofumi Ueda, Mahoko Takahashi Nakagawa, So Kobayashi, Tomoko Koyanagi, Yoshio Sato, Kei Retrovirology Research BACKGROUND: The apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3 (APOBEC3; A3) gene family appears only in mammalian genomes. Some A3 proteins can be incorporated into progeny virions and inhibit lentiviral replication. In turn, the lentiviral viral infectivity factor (Vif) counteracts the A3-mediated antiviral effect by degrading A3 proteins. Recent investigations have suggested that lentiviral vif genes evolved to combat mammalian APOBEC3 proteins, and have further proposed that the Vif-A3 interaction may help determine the co-evolutionary history of cross-species lentiviral transmission in mammals. RESULTS: Here we address the co-evolutionary relationship between two New World felids, the puma (Puma concolor) and the bobcat (Lynx rufus), and their lentiviruses, which are designated puma lentiviruses (PLVs). We demonstrate that PLV-A Vif counteracts the antiviral action of APOBEC3Z3 (A3Z3) of both puma and bobcat, whereas PLV-B Vif counteracts only puma A3Z3. The species specificity of PLV-B Vif is irrespective of the phylogenic relationships of feline species in the genera Puma, Lynx and Acinonyx. We reveal that the amino acid at position 178 in the puma and bobcat A3Z3 is exposed on the protein surface and determines the sensitivity to PLV-B Vif-mediated degradation. Moreover, although both the puma and bobcat A3Z3 genes are polymorphic, their sensitivity/resistance to PLV Vif-mediated degradation is conserved. CONCLUSIONS: To the best of our knowledge, this is the first study suggesting that the host A3 protein potently controls inter-genus lentiviral transmission. Our findings provide the first evidence suggesting that the co-evolutionary arms race between lentiviruses and mammals has occurred in the New World. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12977-018-0414-5) contains supplementary material, which is available to authorized users. BioMed Central 2018-04-10 /pmc/articles/PMC5894237/ /pubmed/29636069 http://dx.doi.org/10.1186/s12977-018-0414-5 Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Konno, Yoriyuki Nagaoka, Shumpei Kimura, Izumi Yamamoto, Keisuke Kagawa, Yumiko Kumata, Ryuichi Aso, Hirofumi Ueda, Mahoko Takahashi Nakagawa, So Kobayashi, Tomoko Koyanagi, Yoshio Sato, Kei New World feline APOBEC3 potently controls inter-genus lentiviral transmission |
title | New World feline APOBEC3 potently controls inter-genus lentiviral transmission |
title_full | New World feline APOBEC3 potently controls inter-genus lentiviral transmission |
title_fullStr | New World feline APOBEC3 potently controls inter-genus lentiviral transmission |
title_full_unstemmed | New World feline APOBEC3 potently controls inter-genus lentiviral transmission |
title_short | New World feline APOBEC3 potently controls inter-genus lentiviral transmission |
title_sort | new world feline apobec3 potently controls inter-genus lentiviral transmission |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5894237/ https://www.ncbi.nlm.nih.gov/pubmed/29636069 http://dx.doi.org/10.1186/s12977-018-0414-5 |
work_keys_str_mv | AT konnoyoriyuki newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT nagaokashumpei newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT kimuraizumi newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT yamamotokeisuke newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT kagawayumiko newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT kumataryuichi newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT asohirofumi newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT uedamahokotakahashi newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT nakagawaso newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT kobayashitomoko newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT koyanagiyoshio newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission AT satokei newworldfelineapobec3potentlycontrolsintergenuslentiviraltransmission |