Transcriptional and Translational Landscape of Equine Torovirus.
Identifieur interne : 000995 ( PubMed/Corpus ); précédent : 000994; suivant : 000996Transcriptional and Translational Landscape of Equine Torovirus.
Auteurs : Hazel Stewart ; Katherine Brown ; Adam M. Dinan ; Nerea Irigoyen ; Eric J. Snijder ; Andrew E. FirthSource :
- Journal of virology [ 1098-5514 ] ; 2018.
English descriptors
- KwdEn :
- MESH :
- chemical , biosynthesis : Viral Proteins.
- genetics : Torovirus, Viral Proteins.
- growth & development : Torovirus.
- Animals, Cells, Cultured, Gene Expression Profiling, Horses, Host-Pathogen Interactions, Protein Biosynthesis, Sequence Analysis, RNA, Transcription, Genetic, Virus Cultivation.
Abstract
The genus Torovirus (subfamily Torovirinae, family Coronaviridae, order Nidovirales) encompasses a range of species that infect domestic ungulates, including cattle, sheep, goats, pigs, and horses, causing an acute self-limiting gastroenteritis. Using the prototype species equine torovirus (EToV), we performed parallel RNA sequencing (RNA-seq) and ribosome profiling (Ribo-seq) to analyze the relative expression levels of the known torovirus proteins and transcripts, chimeric sequences produced via discontinuous RNA synthesis (a characteristic of the nidovirus replication cycle), and changes in host transcription and translation as a result of EToV infection. RNA sequencing confirmed that EToV utilizes a unique combination of discontinuous and nondiscontinuous RNA synthesis to produce its subgenomic RNAs (sgRNAs); indeed, we identified transcripts arising from both mechanisms that would result in sgRNAs encoding the nucleocapsid. Our ribosome profiling analysis revealed that ribosomes efficiently translate two novel CUG-initiated open reading frames (ORFs), located within the so-called 5' untranslated region. We have termed the resulting proteins U1 and U2. Comparative genomic analysis confirmed that these ORFs are conserved across all available torovirus sequences, and the inferred amino acid sequences are subject to purifying selection, indicating that U1 and U2 are functionally relevant. This study provides the first high-resolution analysis of transcription and translation in this neglected group of livestock pathogens.IMPORTANCE Toroviruses infect cattle, goats, pigs, and horses worldwide and can cause gastrointestinal disease. There is no treatment or vaccine, and their ability to spill over into humans has not been assessed. These viruses are related to important human pathogens, including severe acute respiratory syndrome (SARS) coronavirus, and they share some common features; however, the mechanism that they use to produce sgRNA molecules differs. Here, we performed deep sequencing to determine how equine torovirus produces sgRNAs. In doing so, we also identified two previously unknown open reading frames "hidden" within the genome. Together these results highlight the similarities and differences between this domestic animal virus and related pathogens of humans and livestock.
DOI: 10.1128/JVI.00589-18
PubMed: 29950409
Links to Exploration step
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Transcriptional and Translational Landscape of Equine Torovirus.</title><author><name sortKey="Stewart, Hazel" sort="Stewart, Hazel" uniqKey="Stewart H" first="Hazel" last="Stewart">Hazel Stewart</name><affiliation><nlm:affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Brown, Katherine" sort="Brown, Katherine" uniqKey="Brown K" first="Katherine" last="Brown">Katherine Brown</name><affiliation><nlm:affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Dinan, Adam M" sort="Dinan, Adam M" uniqKey="Dinan A" first="Adam M" last="Dinan">Adam M. Dinan</name><affiliation><nlm:affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Irigoyen, Nerea" sort="Irigoyen, Nerea" uniqKey="Irigoyen N" first="Nerea" last="Irigoyen">Nerea Irigoyen</name><affiliation><nlm:affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Snijder, Eric J" sort="Snijder, Eric J" uniqKey="Snijder E" first="Eric J" last="Snijder">Eric J. Snijder</name><affiliation><nlm:affiliation>Molecular Virology Laboratory, Department of Medical Microbiology, Leiden University Medical Center, Leiden, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Firth, Andrew E" sort="Firth, Andrew E" uniqKey="Firth A" first="Andrew E" last="Firth">Andrew E. Firth</name><affiliation><nlm:affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom aef24@cam.ac.uk.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2018">2018</date><idno type="RBID">pubmed:29950409</idno><idno type="pmid">29950409</idno><idno type="doi">10.1128/JVI.00589-18</idno><idno type="wicri:Area/PubMed/Corpus">000995</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">000995</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Transcriptional and Translational Landscape of Equine Torovirus.</title><author><name sortKey="Stewart, Hazel" sort="Stewart, Hazel" uniqKey="Stewart H" first="Hazel" last="Stewart">Hazel Stewart</name><affiliation><nlm:affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Brown, Katherine" sort="Brown, Katherine" uniqKey="Brown K" first="Katherine" last="Brown">Katherine Brown</name><affiliation><nlm:affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Dinan, Adam M" sort="Dinan, Adam M" uniqKey="Dinan A" first="Adam M" last="Dinan">Adam M. Dinan</name><affiliation><nlm:affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Irigoyen, Nerea" sort="Irigoyen, Nerea" uniqKey="Irigoyen N" first="Nerea" last="Irigoyen">Nerea Irigoyen</name><affiliation><nlm:affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</nlm:affiliation></affiliation></author><author><name sortKey="Snijder, Eric J" sort="Snijder, Eric J" uniqKey="Snijder E" first="Eric J" last="Snijder">Eric J. Snijder</name><affiliation><nlm:affiliation>Molecular Virology Laboratory, Department of Medical Microbiology, Leiden University Medical Center, Leiden, The Netherlands.</nlm:affiliation></affiliation></author><author><name sortKey="Firth, Andrew E" sort="Firth, Andrew E" uniqKey="Firth A" first="Andrew E" last="Firth">Andrew E. Firth</name><affiliation><nlm:affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom aef24@cam.ac.uk.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Journal of virology</title><idno type="eISSN">1098-5514</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Cells, Cultured</term><term>Gene Expression Profiling</term><term>Horses</term><term>Host-Pathogen Interactions</term><term>Protein Biosynthesis</term><term>Sequence Analysis, RNA</term><term>Torovirus (genetics)</term><term>Torovirus (growth & development)</term><term>Transcription, Genetic</term><term>Viral Proteins (biosynthesis)</term><term>Viral Proteins (genetics)</term><term>Virus Cultivation</term></keywords><keywords scheme="MESH" type="chemical" qualifier="biosynthesis" xml:lang="en"><term>Viral Proteins</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Torovirus</term><term>Viral Proteins</term></keywords><keywords scheme="MESH" qualifier="growth & development" xml:lang="en"><term>Torovirus</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Cells, Cultured</term><term>Gene Expression Profiling</term><term>Horses</term><term>Host-Pathogen Interactions</term><term>Protein Biosynthesis</term><term>Sequence Analysis, RNA</term><term>Transcription, Genetic</term><term>Virus Cultivation</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The genus <i>Torovirus</i> (subfamily <i>Torovirinae</i>, family <i>Coronaviridae</i>, order <i>Nidovirales</i>) encompasses a range of species that infect domestic ungulates, including cattle, sheep, goats, pigs, and horses, causing an acute self-limiting gastroenteritis. Using the prototype species equine torovirus (EToV), we performed parallel RNA sequencing (RNA-seq) and ribosome profiling (Ribo-seq) to analyze the relative expression levels of the known torovirus proteins and transcripts, chimeric sequences produced via discontinuous RNA synthesis (a characteristic of the nidovirus replication cycle), and changes in host transcription and translation as a result of EToV infection. RNA sequencing confirmed that EToV utilizes a unique combination of discontinuous and nondiscontinuous RNA synthesis to produce its subgenomic RNAs (sgRNAs); indeed, we identified transcripts arising from both mechanisms that would result in sgRNAs encoding the nucleocapsid. Our ribosome profiling analysis revealed that ribosomes efficiently translate two novel CUG-initiated open reading frames (ORFs), located within the so-called 5' untranslated region. We have termed the resulting proteins U1 and U2. Comparative genomic analysis confirmed that these ORFs are conserved across all available torovirus sequences, and the inferred amino acid sequences are subject to purifying selection, indicating that U1 and U2 are functionally relevant. This study provides the first high-resolution analysis of transcription and translation in this neglected group of livestock pathogens.<b>IMPORTANCE</b> Toroviruses infect cattle, goats, pigs, and horses worldwide and can cause gastrointestinal disease. There is no treatment or vaccine, and their ability to spill over into humans has not been assessed. These viruses are related to important human pathogens, including severe acute respiratory syndrome (SARS) coronavirus, and they share some common features; however, the mechanism that they use to produce sgRNA molecules differs. Here, we performed deep sequencing to determine how equine torovirus produces sgRNAs. In doing so, we also identified two previously unknown open reading frames "hidden" within the genome. Together these results highlight the similarities and differences between this domestic animal virus and related pathogens of humans and livestock.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">29950409</PMID><DateCompleted><Year>2018</Year><Month>08</Month><Day>27</Day></DateCompleted><DateRevised><Year>2019</Year><Month>03</Month><Day>20</Day></DateRevised><Article PubModel="Electronic-Print"><Journal><ISSN IssnType="Electronic">1098-5514</ISSN><JournalIssue CitedMedium="Internet"><Volume>92</Volume><Issue>17</Issue><PubDate><Year>2018</Year><Month>09</Month><Day>01</Day></PubDate></JournalIssue><Title>Journal of virology</Title><ISOAbbreviation>J. Virol.</ISOAbbreviation></Journal><ArticleTitle>Transcriptional and Translational Landscape of Equine Torovirus.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">e00589-18</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1128/JVI.00589-18</ELocationID><Abstract><AbstractText>The genus <i>Torovirus</i> (subfamily <i>Torovirinae</i>, family <i>Coronaviridae</i>, order <i>Nidovirales</i>) encompasses a range of species that infect domestic ungulates, including cattle, sheep, goats, pigs, and horses, causing an acute self-limiting gastroenteritis. Using the prototype species equine torovirus (EToV), we performed parallel RNA sequencing (RNA-seq) and ribosome profiling (Ribo-seq) to analyze the relative expression levels of the known torovirus proteins and transcripts, chimeric sequences produced via discontinuous RNA synthesis (a characteristic of the nidovirus replication cycle), and changes in host transcription and translation as a result of EToV infection. RNA sequencing confirmed that EToV utilizes a unique combination of discontinuous and nondiscontinuous RNA synthesis to produce its subgenomic RNAs (sgRNAs); indeed, we identified transcripts arising from both mechanisms that would result in sgRNAs encoding the nucleocapsid. Our ribosome profiling analysis revealed that ribosomes efficiently translate two novel CUG-initiated open reading frames (ORFs), located within the so-called 5' untranslated region. We have termed the resulting proteins U1 and U2. Comparative genomic analysis confirmed that these ORFs are conserved across all available torovirus sequences, and the inferred amino acid sequences are subject to purifying selection, indicating that U1 and U2 are functionally relevant. This study provides the first high-resolution analysis of transcription and translation in this neglected group of livestock pathogens.<b>IMPORTANCE</b> Toroviruses infect cattle, goats, pigs, and horses worldwide and can cause gastrointestinal disease. There is no treatment or vaccine, and their ability to spill over into humans has not been assessed. These viruses are related to important human pathogens, including severe acute respiratory syndrome (SARS) coronavirus, and they share some common features; however, the mechanism that they use to produce sgRNA molecules differs. Here, we performed deep sequencing to determine how equine torovirus produces sgRNAs. In doing so, we also identified two previously unknown open reading frames "hidden" within the genome. Together these results highlight the similarities and differences between this domestic animal virus and related pathogens of humans and livestock.</AbstractText><CopyrightInformation>Copyright © 2018 Stewart et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y" EqualContrib="Y"><LastName>Stewart</LastName><ForeName>Hazel</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y" EqualContrib="Y"><LastName>Brown</LastName><ForeName>Katherine</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dinan</LastName><ForeName>Adam M</ForeName><Initials>AM</Initials><AffiliationInfo><Affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Irigoyen</LastName><ForeName>Nerea</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Snijder</LastName><ForeName>Eric J</ForeName><Initials>EJ</Initials><AffiliationInfo><Affiliation>Molecular Virology Laboratory, Department of Medical Microbiology, Leiden University Medical Center, Leiden, The Netherlands.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Firth</LastName><ForeName>Andrew E</ForeName><Initials>AE</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-7986-9520</Identifier><AffiliationInfo><Affiliation>Division of Virology, Department of Pathology, University of Cambridge, Cambridge, United Kingdom 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