A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular level

[EN] Superinfection exclusion (SIE), the ability of an established virus infection to interfere with a secondary infection by the same or a closely related virus, has been described for different viruses, including important pathogens of humans, animals, and plants. Citrus tristeza virus (CTV), a po...

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Autores: Bergua, Maria, Zwart, Mark Peter, El-Mohtar, Choaa, Shilts, Turksen, Elena Fito, Santiago Fco, Folimonova, Svetlana Y.
Tipo de recurso: artículo
Fecha de publicación:2014
País:España
Institución:Universitat Politècnica de València (UPV)
Repositorio:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
Idioma:inglés
OAI Identifier:oai:riunet.upv.es:10251/74497
Acceso en línea:https://riunet.upv.es/handle/10251/74497
Access Level:acceso abierto
Palabra clave:Citrus-tristeza-virus
Hepatitis-C virus
Avian Leukosis virus
Borna-disease virus
Rous sarcoma virus
Nicotiana-Benthamiana
Transient expression
Antiviral Immunity
Subgenomic RNAs
Sindbis virus
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oai_identifier_str oai:riunet.upv.es:10251/74497
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular level
title A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular level
spellingShingle A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular level
Bergua, Maria
Citrus-tristeza-virus
Hepatitis-C virus
Avian Leukosis virus
Borna-disease virus
Rous sarcoma virus
Nicotiana-Benthamiana
Transient expression
Antiviral Immunity
Subgenomic RNAs
Sindbis virus
title_short A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular level
title_full A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular level
title_fullStr A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular level
title_full_unstemmed A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular level
title_sort A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular level
dc.creator.none.fl_str_mv Bergua, Maria
Zwart, Mark Peter
El-Mohtar, Choaa
Shilts, Turksen
Elena Fito, Santiago Fco
Folimonova, Svetlana Y.
author Bergua, Maria
author_facet Bergua, Maria
Zwart, Mark Peter
El-Mohtar, Choaa
Shilts, Turksen
Elena Fito, Santiago Fco
Folimonova, Svetlana Y.
author_role author
author2 Zwart, Mark Peter
El-Mohtar, Choaa
Shilts, Turksen
Elena Fito, Santiago Fco
Folimonova, Svetlana Y.
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv National Science Foundation, EEUU
Ministerio de Economía y Competitividad
Ministerio de Ciencia e Innovación
Repositorio Institucional de la Universitat Politècnica de València Riunet
dc.subject.none.fl_str_mv Citrus-tristeza-virus
Hepatitis-C virus
Avian Leukosis virus
Borna-disease virus
Rous sarcoma virus
Nicotiana-Benthamiana
Transient expression
Antiviral Immunity
Subgenomic RNAs
Sindbis virus
topic Citrus-tristeza-virus
Hepatitis-C virus
Avian Leukosis virus
Borna-disease virus
Rous sarcoma virus
Nicotiana-Benthamiana
Transient expression
Antiviral Immunity
Subgenomic RNAs
Sindbis virus
description [EN] Superinfection exclusion (SIE), the ability of an established virus infection to interfere with a secondary infection by the same or a closely related virus, has been described for different viruses, including important pathogens of humans, animals, and plants. Citrus tristeza virus (CTV), a positive-sense RNA virus, represents a valuable model system for studying SIE due to the existence of several phylogenetically distinct strains. Furthermore, CTV allows SIE to be examined at the whole-organism level. Previously, we demonstrated that SIE by CTV is a virus-controlled function that requires the viral protein p33. In this study, we show that p33 mediates SIE at the whole-organism level, while it is not required for exclusion at the cellular level. Primary infection of a host with a fluorescent protein-tagged CTV variant lacking p33 did not interfere with the establishment of a secondary infection by the same virus labeled with a different fluorescent protein. However, cellular coinfection by both viruses was rare. The obtained observations, along with estimates of the cellular multiplicity of infection (MOI) and MOI model selection, suggested that low levels of cellular coinfection appear to be best explained by exclusion at the cellular level. Based on these results, we propose that SIE by CTV is operated at two levels-the cellular and the whole-organism levels-by two distinct mechanisms that could function independently. This novel aspect of viral SIE highlights the intriguing complexity of this phenomenon, further understanding of which may open up new avenues to manage virus diseases. IMPORTANCE Many viruses exhibit superinfection exclusion (SIE), the ability of an established virus infection to interfere with a secondary infection by related viruses. SIE plays an important role in the pathogenesis and evolution of virus populations. The observations described here suggest that SIE could be controlled independently at different levels of the host: the whole-organism level or the level of individual cells. The p33 protein of citrus tristeza virus (CTV), an RNA virus, was shown to mediate SIE at the whole-organism level, while it appeared not to be required for exclusion at the cellular level. SIE by CTV is, therefore, highly complex and appears to use mechanisms different from those proposed for other viruses. A better understanding of this phenomenon may lead to the development of new strategies for controlling viral diseases in human populations and agroecosystems.
publishDate 2014
dc.date.none.fl_str_mv 2014
2014-10-01
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://riunet.upv.es/handle/10251/74497
url https://riunet.upv.es/handle/10251/74497
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv National Science Foundation, China https://doi.org/10.13039/100000001 1050883 Mechanism of Superinfection Exclusion By An RNA Virus
Ministerio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 BFU2012-30805 EVOLUTIONARY SYSTEMS VIROLOGY: EPISTASIS AND THE RUGGEDNESS OF ADAPTIVE LANDSCAPES, MUTATIONS IN REGULATORY SEQUENCES, AND THE HOST DETERMINANTS OF VIRAL FITNESS
Ministerio de Ciencia e Innovación http://dx.doi.org/10.13039/501100004837 JCI-2011-10379 JCI-2011-10379
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Reserva de todos los derechos
http://rightsstatements.org/vocab/InC/1.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Reserva de todos los derechos
http://rightsstatements.org/vocab/InC/1.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
instname:Universitat Politècnica de València (UPV)
instname_str Universitat Politècnica de València (UPV)
reponame_str RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
collection RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling A viral protein mediates superinfection exclusion at the whole organism level while is not required for exclusion at the cellular levelBergua, MariaZwart, Mark PeterEl-Mohtar, ChoaaShilts, TurksenElena Fito, Santiago FcoFolimonova, Svetlana Y.Citrus-tristeza-virusHepatitis-C virusAvian Leukosis virusBorna-disease virusRous sarcoma virusNicotiana-BenthamianaTransient expressionAntiviral ImmunitySubgenomic RNAsSindbis virus[EN] Superinfection exclusion (SIE), the ability of an established virus infection to interfere with a secondary infection by the same or a closely related virus, has been described for different viruses, including important pathogens of humans, animals, and plants. Citrus tristeza virus (CTV), a positive-sense RNA virus, represents a valuable model system for studying SIE due to the existence of several phylogenetically distinct strains. Furthermore, CTV allows SIE to be examined at the whole-organism level. Previously, we demonstrated that SIE by CTV is a virus-controlled function that requires the viral protein p33. In this study, we show that p33 mediates SIE at the whole-organism level, while it is not required for exclusion at the cellular level. Primary infection of a host with a fluorescent protein-tagged CTV variant lacking p33 did not interfere with the establishment of a secondary infection by the same virus labeled with a different fluorescent protein. However, cellular coinfection by both viruses was rare. The obtained observations, along with estimates of the cellular multiplicity of infection (MOI) and MOI model selection, suggested that low levels of cellular coinfection appear to be best explained by exclusion at the cellular level. Based on these results, we propose that SIE by CTV is operated at two levels-the cellular and the whole-organism levels-by two distinct mechanisms that could function independently. This novel aspect of viral SIE highlights the intriguing complexity of this phenomenon, further understanding of which may open up new avenues to manage virus diseases. IMPORTANCE Many viruses exhibit superinfection exclusion (SIE), the ability of an established virus infection to interfere with a secondary infection by related viruses. SIE plays an important role in the pathogenesis and evolution of virus populations. The observations described here suggest that SIE could be controlled independently at different levels of the host: the whole-organism level or the level of individual cells. The p33 protein of citrus tristeza virus (CTV), an RNA virus, was shown to mediate SIE at the whole-organism level, while it appeared not to be required for exclusion at the cellular level. SIE by CTV is, therefore, highly complex and appears to use mechanisms different from those proposed for other viruses. A better understanding of this phenomenon may lead to the development of new strategies for controlling viral diseases in human populations and agroecosystems.This research was supported by the National Science Foundation under grant number 1050883 (to S. Y. Folimonova). Work in Valencia, Spain, was supported by grant BFU2012-30805 (to S. F. Elena) and by a Juan de la Cierva postdoctoral fellowship (JCI-2011-10379, to M. P. Zwart), both from the Spanish Ministerio de Economia y Competitividad.American Society for MicrobiologyNational Science Foundation, EEUUMinisterio de Economía y CompetitividadMinisterio de Ciencia e InnovaciónRepositorio Institucional de la Universitat Politècnica de València Riunet20142014-10-01journal articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://riunet.upv.es/handle/10251/74497reponame:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valénciainstname:Universitat Politècnica de València (UPV)InglésengNational Science Foundation, China https://doi.org/10.13039/100000001 1050883 Mechanism of Superinfection Exclusion By An RNA VirusMinisterio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 BFU2012-30805 EVOLUTIONARY SYSTEMS VIROLOGY: EPISTASIS AND THE RUGGEDNESS OF ADAPTIVE LANDSCAPES, MUTATIONS IN REGULATORY SEQUENCES, AND THE HOST DETERMINANTS OF VIRAL FITNESSMinisterio de Ciencia e Innovación http://dx.doi.org/10.13039/501100004837 JCI-2011-10379 JCI-2011-10379open accesshttp://purl.org/coar/access_right/c_abf2Reserva de todos los derechoshttp://rightsstatements.org/vocab/InC/1.0/info:eu-repo/semantics/openAccessoai:riunet.upv.es:10251/744972026-06-13T07:49:27Z
score 15.301603

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