A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses.

Endogenous retroviruses (ERVs) are remnants of ancient retroviral infections of the host germline transmitted vertically from generation to generation. It is hypothesized that some ERVs are used by the host as restriction factors to block the infection of pathogenic retroviruses. Indeed, some ERVs e...

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Autores principales:	Frederick Arnaud, Marco Caporale, Mariana Varela, Roman Biek, Bernardo Chessa, Alberto Alberti, Matthew Golder, Manuela Mura, Ya-Ping Zhang, Li Yu, Filipe Pereira, James C Demartini, Kreg Leymaster, Thomas E Spencer, Massimo Palmarini
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2007
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/1f5ec5efef904ddbb9e383f439f7aa89
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spelling	oai:doaj.org-article:1f5ec5efef904ddbb9e383f439f7aa892021-12-02T19:59:51ZA paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses.1553-73661553-737410.1371/journal.ppat.0030170https://doaj.org/article/1f5ec5efef904ddbb9e383f439f7aa892007-11-01T00:00:00Zhttps://doi.org/10.1371/journal.ppat.0030170https://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Endogenous retroviruses (ERVs) are remnants of ancient retroviral infections of the host germline transmitted vertically from generation to generation. It is hypothesized that some ERVs are used by the host as restriction factors to block the infection of pathogenic retroviruses. Indeed, some ERVs efficiently interfere with the replication of related exogenous retroviruses. However, data suggesting that these mechanisms have influenced the coevolution of endogenous and/or exogenous retroviruses and their hosts have been more difficult to obtain. Sheep are an interesting model system to study retrovirus-host coevolution because of the coexistence in this animal species of two exogenous (i.e., horizontally transmitted) oncogenic retroviruses, Jaagsiekte sheep retrovirus and Enzootic nasal tumor virus, with highly related and biologically active endogenous retroviruses (enJSRVs). Here, we isolated and characterized the evolutionary history and molecular virology of 27 enJSRV proviruses. enJSRVs have been integrating in the host genome for the last 5-7 million y. Two enJSRV proviruses (enJS56A1 and enJSRV-20), which entered the host genome within the last 3 million y (before and during speciation within the genus Ovis), acquired in two temporally distinct events a defective Gag polyprotein resulting in a transdominant phenotype able to block late replication steps of related exogenous retroviruses. Both transdominant proviruses became fixed in the host genome before or around sheep domestication (approximately 9,000 y ago). Interestingly, a provirus escaping the transdominant enJSRVs has emerged very recently, most likely within the last 200 y. Thus, we determined sequentially distinct events during evolution that are indicative of an evolutionary antagonism between endogenous and exogenous retroviruses. This study strongly suggests that endogenization and selection of ERVs acting as restriction factors is a mechanism used by the host to fight retroviral infections.Frederick ArnaudMarco CaporaleMariana VarelaRoman BiekBernardo ChessaAlberto AlbertiMatthew GolderManuela MuraYa-Ping ZhangLi YuFilipe PereiraJames C DemartiniKreg LeymasterThomas E SpencerMassimo PalmariniPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 3, Iss 11, p e170 (2007)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Frederick Arnaud Marco Caporale Mariana Varela Roman Biek Bernardo Chessa Alberto Alberti Matthew Golder Manuela Mura Ya-Ping Zhang Li Yu Filipe Pereira James C Demartini Kreg Leymaster Thomas E Spencer Massimo Palmarini A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses.
description	Endogenous retroviruses (ERVs) are remnants of ancient retroviral infections of the host germline transmitted vertically from generation to generation. It is hypothesized that some ERVs are used by the host as restriction factors to block the infection of pathogenic retroviruses. Indeed, some ERVs efficiently interfere with the replication of related exogenous retroviruses. However, data suggesting that these mechanisms have influenced the coevolution of endogenous and/or exogenous retroviruses and their hosts have been more difficult to obtain. Sheep are an interesting model system to study retrovirus-host coevolution because of the coexistence in this animal species of two exogenous (i.e., horizontally transmitted) oncogenic retroviruses, Jaagsiekte sheep retrovirus and Enzootic nasal tumor virus, with highly related and biologically active endogenous retroviruses (enJSRVs). Here, we isolated and characterized the evolutionary history and molecular virology of 27 enJSRV proviruses. enJSRVs have been integrating in the host genome for the last 5-7 million y. Two enJSRV proviruses (enJS56A1 and enJSRV-20), which entered the host genome within the last 3 million y (before and during speciation within the genus Ovis), acquired in two temporally distinct events a defective Gag polyprotein resulting in a transdominant phenotype able to block late replication steps of related exogenous retroviruses. Both transdominant proviruses became fixed in the host genome before or around sheep domestication (approximately 9,000 y ago). Interestingly, a provirus escaping the transdominant enJSRVs has emerged very recently, most likely within the last 200 y. Thus, we determined sequentially distinct events during evolution that are indicative of an evolutionary antagonism between endogenous and exogenous retroviruses. This study strongly suggests that endogenization and selection of ERVs acting as restriction factors is a mechanism used by the host to fight retroviral infections.
format	article
author	Frederick Arnaud Marco Caporale Mariana Varela Roman Biek Bernardo Chessa Alberto Alberti Matthew Golder Manuela Mura Ya-Ping Zhang Li Yu Filipe Pereira James C Demartini Kreg Leymaster Thomas E Spencer Massimo Palmarini
author_facet	Frederick Arnaud Marco Caporale Mariana Varela Roman Biek Bernardo Chessa Alberto Alberti Matthew Golder Manuela Mura Ya-Ping Zhang Li Yu Filipe Pereira James C Demartini Kreg Leymaster Thomas E Spencer Massimo Palmarini
author_sort	Frederick Arnaud
title	A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses.
title_short	A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses.
title_full	A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses.
title_fullStr	A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses.
title_full_unstemmed	A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses.
title_sort	paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses.
publisher	Public Library of Science (PLoS)
publishDate	2007
url	https://doaj.org/article/1f5ec5efef904ddbb9e383f439f7aa89
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A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses.

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