Cancer, Warts, or Asymptomatic Infections: Clinical Presentation Matches Codon Usage Preferences in Human Papillomaviruses
Identifieur interne : 000057 ( Main/Merge ); précédent : 000056; suivant : 000058Cancer, Warts, or Asymptomatic Infections: Clinical Presentation Matches Codon Usage Preferences in Human Papillomaviruses
Auteurs : Marta Félez-Sánchez [Espagne] ; Jan-Hendrik Trösemeier [Allemagne] ; Stéphanie Bedhomme [Espagne, France] ; Maria Isabel González-Bravo [Espagne] ; Christel Kamp [Allemagne] ; Ignacio G. Bravo [Espagne]Source :
- Genome Biology and Evolution [ 1759-6653 ] ; 2015.
Abstract
Viruses rely completely on the hosts’ machinery for translation of viral transcripts. However, for most viruses infecting humans, codon usage preferences (CUPrefs) do not match those of the host. Human papillomaviruses (HPVs) are a showcase to tackle this paradox: they present a large genotypic diversity and a broad range of phenotypic presentations, from asymptomatic infections to productive lesions and cancer. By applying phylogenetic inference and dimensionality reduction methods, we demonstrate first that genes in HPVs are poorly adapted to the average human CUPrefs, the only exception being capsid genes in viruses causing productive lesions. Phylogenetic relationships between HPVs explained only a small proportion of CUPrefs variation. Instead, the most important explanatory factor for viral CUPrefs was infection phenotype, as orthologous genes in viruses with similar clinical presentation displayed similar CUPrefs. Moreover, viral genes with similar spatiotemporal expression patterns also showed similar CUPrefs. Our results suggest that CUPrefs in HPVs reflect either variations in the mutation bias or differential selection pressures depending on the clinical presentation and expression timing. We propose that poor viral CUPrefs may be central to a trade-off between strong viral gene expression and the potential for eliciting protective immune response.
Url:
DOI: 10.1093/gbe/evv129
PubMed: 26139833
PubMed Central: 4558848
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Bellvitge Institute of Biomedical Research (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Virus and Cancer Laboratory. Bellvitge Institute of Biomedical Research (IDIBELL), L'Hospitalet de Llobregat, Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation></author><author><name sortKey="Trosemeier, Jan Hendrik" sort="Trosemeier, Jan Hendrik" uniqKey="Trosemeier J" first="Jan-Hendrik" last="Trösemeier">Jan-Hendrik Trösemeier</name><affiliation wicri:level="3"><nlm:aff id="evv129-AFF3">Molecular Bioinformatics, Institute of Computer Science, Johann Wolfgang Goethe University, Frankfurt am Main, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Molecular Bioinformatics, Institute of Computer Science, Johann Wolfgang Goethe University, Frankfurt am Main</wicri:regionArea><placeName><region type="land" nuts="1">Hesse (Land)</region><region type="district" nuts="2">District de Darmstadt</region><settlement type="city">Francfort-sur-le-Main</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="evv129-AFF4">Paul-Ehrlich-Institut, Federal Institute for Vaccines and Biomedicines, Langen, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Paul-Ehrlich-Institut, Federal Institute for Vaccines and Biomedicines, Langen</wicri:regionArea><wicri:noRegion>Langen</wicri:noRegion><wicri:noRegion>Langen</wicri:noRegion><wicri:noRegion>Langen</wicri:noRegion></affiliation></author><author><name sortKey="Bedhomme, Stephanie" sort="Bedhomme, Stephanie" uniqKey="Bedhomme S" first="Stéphanie" last="Bedhomme">Stéphanie Bedhomme</name><affiliation wicri:level="3"><nlm:aff id="evv129-AFF1">Infections and Cancer Laboratory, Catalan Institute of Oncology, L'Hospitalet de Llobregat, Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Infections and Cancer Laboratory, Catalan Institute of Oncology, L'Hospitalet de Llobregat, Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="evv129-AFF2">Virus and Cancer Laboratory. Bellvitge Institute of Biomedical Research (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Virus and Cancer Laboratory. Bellvitge Institute of Biomedical Research (IDIBELL), L'Hospitalet de Llobregat, Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="evv129-AFF5">Département d'Ecologie Evolutive Centre d’Ecologie Fonctionnelle et Evolutive, CNRS – UMR 5175, Montpellier, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Département d'Ecologie Evolutive Centre d’Ecologie Fonctionnelle et Evolutive, CNRS – UMR 5175, Montpellier</wicri:regionArea><placeName><region type="region">Occitanie (région administrative)</region><region type="old region">Languedoc-Roussillon</region><settlement type="city">Montpellier</settlement></placeName></affiliation></author><author><name sortKey="Gonzalez Bravo, Maria Isabel" sort="Gonzalez Bravo, Maria Isabel" uniqKey="Gonzalez Bravo M" first="Maria Isabel" last="González-Bravo">Maria Isabel González-Bravo</name><affiliation wicri:level="1"><nlm:aff id="evv129-AFF6">Facultad de Economía y Empresa, University Salamanca, Salamanca, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Facultad de Economía y Empresa, University Salamanca, Salamanca</wicri:regionArea><wicri:noRegion>Salamanca</wicri:noRegion></affiliation></author><author><name sortKey="Kamp, Christel" sort="Kamp, Christel" uniqKey="Kamp C" first="Christel" last="Kamp">Christel Kamp</name><affiliation wicri:level="1"><nlm:aff id="evv129-AFF4">Paul-Ehrlich-Institut, Federal Institute for Vaccines and Biomedicines, Langen, Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Paul-Ehrlich-Institut, Federal Institute for Vaccines and Biomedicines, Langen</wicri:regionArea><wicri:noRegion>Langen</wicri:noRegion><wicri:noRegion>Langen</wicri:noRegion><wicri:noRegion>Langen</wicri:noRegion></affiliation></author><author><name sortKey="Bravo, Ignacio G" sort="Bravo, Ignacio G" uniqKey="Bravo I" first="Ignacio G." last="Bravo">Ignacio G. Bravo</name><affiliation wicri:level="3"><nlm:aff id="evv129-AFF1">Infections and Cancer Laboratory, Catalan Institute of Oncology, L'Hospitalet de Llobregat, Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Infections and Cancer Laboratory, Catalan Institute of Oncology, L'Hospitalet de Llobregat, Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="evv129-AFF2">Virus and Cancer Laboratory. Bellvitge Institute of Biomedical Research (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Virus and Cancer Laboratory. Bellvitge Institute of Biomedical Research (IDIBELL), L'Hospitalet de Llobregat, Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation></author></analytic><series><title level="j">Genome Biology and Evolution</title><idno type="eISSN">1759-6653</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Viruses rely completely on the hosts’ machinery for translation of viral transcripts. However, for most viruses infecting humans, codon usage preferences (CUPrefs) do not match those of the host. Human papillomaviruses (HPVs) are a showcase to tackle this paradox: they present a large genotypic diversity and a broad range of phenotypic presentations, from asymptomatic infections to productive lesions and cancer. By applying phylogenetic inference and dimensionality reduction methods, we demonstrate first that genes in HPVs are poorly adapted to the average human CUPrefs, the only exception being capsid genes in viruses causing productive lesions. Phylogenetic relationships between HPVs explained only a small proportion of CUPrefs variation. Instead, the most important explanatory factor for viral CUPrefs was infection phenotype, as orthologous genes in viruses with similar clinical presentation displayed similar CUPrefs. Moreover, viral genes with similar spatiotemporal expression patterns also showed similar CUPrefs. Our results suggest that CUPrefs in HPVs reflect either variations in the mutation bias or differential selection pressures depending on the clinical presentation and expression timing. We propose that poor viral CUPrefs may be central to a trade-off between strong viral gene expression and the potential for eliciting protective immune response.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Akashi, H" uniqKey="Akashi H">H Akashi</name></author><author><name sortKey="Eyre Walker, A" uniqKey="Eyre Walker A">A Eyre-Walker</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Aota, S" uniqKey="Aota S">S Aota</name></author><author><name sortKey="Ikemura, T" uniqKey="Ikemura T">T Ikemura</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Aragones, L" uniqKey="Aragones L">L Aragones</name></author><author><name sortKey="Bosch, A" uniqKey="Bosch A">A Bosch</name></author><author><name sortKey="Pinto, Rm" uniqKey="Pinto R">RM Pinto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Aragones, L" uniqKey="Aragones L">L 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