Dengue virus preferentially uses human and mosquito non-optimal codons

Autores
Castellano, Luciana A.; McNamara, Ryan J.; Pallarés, Horacio Martín; Gamarnik, Andrea Vanesa; Alvarez, Diego Ezequiel; Bazzini, Ariel Alejandro
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Codon optimality refers to the effect that codon composition has on messenger RNA (mRNA) stability and translation level and implies that synonymous codons are not silent from a regulatory point of view. Here, we investigated the adaptation of virus genomes to the host optimality code using mosquito-borne dengue virus (DENV) as a model. We demonstrated that codon optimality exists in mosquito cells and showed that DENV preferentially uses nonoptimal (destabilizing) codons and avoids codons that are defined as optimal (stabilizing) in either human or mosquito cells. Human genes enriched in the codons preferentially and frequently used by DENV are upregulated during infection, and so is the tRNA decoding the nonoptimal and DENV preferentially used codon for arginine. We found that adaptation during single-host passaging in human or mosquito cells results in the selection of synonymous mutations towards DENV's preferred nonoptimal codons that increase virus fitness. Finally, our analyses revealed that hundreds of viruses preferentially use nonoptimal codons, with those infecting a single host displaying an even stronger bias, suggesting that host-pathogen interaction shapes virus-synonymous codon choice.
Fil: Castellano, Luciana A.. No especifíca;
Fil: McNamara, Ryan J.. No especifíca;
Fil: Pallarés, Horacio Martín. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Gamarnik, Andrea Vanesa. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Alvarez, Diego Ezequiel. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Bazzini, Ariel Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Materia
CODON OPTIMALITY
MOSQUITO
VIRUSES
tRNA
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/265124
Acceder
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network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Dengue virus preferentially uses human and mosquito non-optimal codonsCastellano, Luciana A.McNamara, Ryan J.Pallarés, Horacio MartínGamarnik, Andrea VanesaAlvarez, Diego EzequielBazzini, Ariel AlejandroCODON OPTIMALITYMOSQUITOVIRUSEStRNAhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Codon optimality refers to the effect that codon composition has on messenger RNA (mRNA) stability and translation level and implies that synonymous codons are not silent from a regulatory point of view. Here, we investigated the adaptation of virus genomes to the host optimality code using mosquito-borne dengue virus (DENV) as a model. We demonstrated that codon optimality exists in mosquito cells and showed that DENV preferentially uses nonoptimal (destabilizing) codons and avoids codons that are defined as optimal (stabilizing) in either human or mosquito cells. Human genes enriched in the codons preferentially and frequently used by DENV are upregulated during infection, and so is the tRNA decoding the nonoptimal and DENV preferentially used codon for arginine. We found that adaptation during single-host passaging in human or mosquito cells results in the selection of synonymous mutations towards DENV's preferred nonoptimal codons that increase virus fitness. Finally, our analyses revealed that hundreds of viruses preferentially use nonoptimal codons, with those infecting a single host displaying an even stronger bias, suggesting that host-pathogen interaction shapes virus-synonymous codon choice.Fil: Castellano, Luciana A.. No especifíca;Fil: McNamara, Ryan J.. No especifíca;Fil: Pallarés, Horacio Martín. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; ArgentinaFil: Gamarnik, Andrea Vanesa. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; ArgentinaFil: Alvarez, Diego Ezequiel. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; ArgentinaFil: Bazzini, Ariel Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaNature Publishing Group2024-07info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/265124Castellano, Luciana A.; McNamara, Ryan J.; Pallarés, Horacio Martín; Gamarnik, Andrea Vanesa; Alvarez, Diego Ezequiel; et al.; Dengue virus preferentially uses human and mosquito non-optimal codons; Nature Publishing Group; Molecular Systems Biology; 20; 10; 7-2024; 1085-11081744-4292CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.embopress.org/doi/full/10.1038/s44320-024-00052-7info:eu-repo/semantics/altIdentifier/doi/10.1038/s44320-024-00052-7info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:08:06Zoai:ri.conicet.gov.ar:11336/265124instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 10:08:06.669CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Dengue virus preferentially uses human and mosquito non-optimal codons
title Dengue virus preferentially uses human and mosquito non-optimal codons
spellingShingle Dengue virus preferentially uses human and mosquito non-optimal codons
Castellano, Luciana A.
CODON OPTIMALITY
MOSQUITO
VIRUSES
tRNA
title_short Dengue virus preferentially uses human and mosquito non-optimal codons
title_full Dengue virus preferentially uses human and mosquito non-optimal codons
title_fullStr Dengue virus preferentially uses human and mosquito non-optimal codons
title_full_unstemmed Dengue virus preferentially uses human and mosquito non-optimal codons
title_sort Dengue virus preferentially uses human and mosquito non-optimal codons
dc.creator.none.fl_str_mv Castellano, Luciana A.
McNamara, Ryan J.
Pallarés, Horacio Martín
Gamarnik, Andrea Vanesa
Alvarez, Diego Ezequiel
Bazzini, Ariel Alejandro
author Castellano, Luciana A.
author_facet Castellano, Luciana A.
McNamara, Ryan J.
Pallarés, Horacio Martín
Gamarnik, Andrea Vanesa
Alvarez, Diego Ezequiel
Bazzini, Ariel Alejandro
author_role author
author2 McNamara, Ryan J.
Pallarés, Horacio Martín
Gamarnik, Andrea Vanesa
Alvarez, Diego Ezequiel
Bazzini, Ariel Alejandro
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv CODON OPTIMALITY
MOSQUITO
VIRUSES
tRNA
topic CODON OPTIMALITY
MOSQUITO
VIRUSES
tRNA
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Codon optimality refers to the effect that codon composition has on messenger RNA (mRNA) stability and translation level and implies that synonymous codons are not silent from a regulatory point of view. Here, we investigated the adaptation of virus genomes to the host optimality code using mosquito-borne dengue virus (DENV) as a model. We demonstrated that codon optimality exists in mosquito cells and showed that DENV preferentially uses nonoptimal (destabilizing) codons and avoids codons that are defined as optimal (stabilizing) in either human or mosquito cells. Human genes enriched in the codons preferentially and frequently used by DENV are upregulated during infection, and so is the tRNA decoding the nonoptimal and DENV preferentially used codon for arginine. We found that adaptation during single-host passaging in human or mosquito cells results in the selection of synonymous mutations towards DENV's preferred nonoptimal codons that increase virus fitness. Finally, our analyses revealed that hundreds of viruses preferentially use nonoptimal codons, with those infecting a single host displaying an even stronger bias, suggesting that host-pathogen interaction shapes virus-synonymous codon choice.
Fil: Castellano, Luciana A.. No especifíca;
Fil: McNamara, Ryan J.. No especifíca;
Fil: Pallarés, Horacio Martín. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Gamarnik, Andrea Vanesa. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Alvarez, Diego Ezequiel. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Bazzini, Ariel Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Codon optimality refers to the effect that codon composition has on messenger RNA (mRNA) stability and translation level and implies that synonymous codons are not silent from a regulatory point of view. Here, we investigated the adaptation of virus genomes to the host optimality code using mosquito-borne dengue virus (DENV) as a model. We demonstrated that codon optimality exists in mosquito cells and showed that DENV preferentially uses nonoptimal (destabilizing) codons and avoids codons that are defined as optimal (stabilizing) in either human or mosquito cells. Human genes enriched in the codons preferentially and frequently used by DENV are upregulated during infection, and so is the tRNA decoding the nonoptimal and DENV preferentially used codon for arginine. We found that adaptation during single-host passaging in human or mosquito cells results in the selection of synonymous mutations towards DENV's preferred nonoptimal codons that increase virus fitness. Finally, our analyses revealed that hundreds of viruses preferentially use nonoptimal codons, with those infecting a single host displaying an even stronger bias, suggesting that host-pathogen interaction shapes virus-synonymous codon choice.
publishDate 2024
dc.date.none.fl_str_mv 2024-07
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/265124
Castellano, Luciana A.; McNamara, Ryan J.; Pallarés, Horacio Martín; Gamarnik, Andrea Vanesa; Alvarez, Diego Ezequiel; et al.; Dengue virus preferentially uses human and mosquito non-optimal codons; Nature Publishing Group; Molecular Systems Biology; 20; 10; 7-2024; 1085-1108
1744-4292
CONICET Digital
CONICET
url http://hdl.handle.net/11336/265124
identifier_str_mv Castellano, Luciana A.; McNamara, Ryan J.; Pallarés, Horacio Martín; Gamarnik, Andrea Vanesa; Alvarez, Diego Ezequiel; et al.; Dengue virus preferentially uses human and mosquito non-optimal codons; Nature Publishing Group; Molecular Systems Biology; 20; 10; 7-2024; 1085-1108
1744-4292
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.embopress.org/doi/full/10.1038/s44320-024-00052-7
info:eu-repo/semantics/altIdentifier/doi/10.1038/s44320-024-00052-7
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature Publishing Group
publisher.none.fl_str_mv Nature Publishing Group
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.13397

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