SARS Coronavirus nsp1 Protein Induces Template-Dependent Endonucleolytic Cleavage of mRNAs: Viral mRNAs Are Resistant to nsp1-Induced RNA Cleavage
Identifieur interne : 002429 ( Ncbi/Merge ); précédent : 002428; suivant : 002430SARS Coronavirus nsp1 Protein Induces Template-Dependent Endonucleolytic Cleavage of mRNAs: Viral mRNAs Are Resistant to nsp1-Induced RNA Cleavage
Auteurs : Cheng Huang [États-Unis] ; Kumari G. Lokugamage [États-Unis] ; Janet M. Rozovics [États-Unis] ; Krishna Narayanan [États-Unis] ; Bert L. Semler [États-Unis] ; Shinji Makino [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2011.
Descripteurs français
- KwdFr :
- ARN messager (génétique), ARN messager (métabolisme), ARN viral (génétique), ARN viral (métabolisme), Matrices (génétique), Protéines virales non structurales (génétique), Protéines virales non structurales (métabolisme), RNA replicase (génétique), RNA replicase (métabolisme), RT-PCR, Régulation de l'expression des gènes viraux (génétique), Stabilité de l'ARN, Virus du SRAS (génétique), Virus du SRAS (métabolisme).
- MESH :
- génétique : ARN messager, ARN viral, Protéines virales non structurales, RNA replicase, Régulation de l'expression des gènes viraux, Virus du SRAS.
- métabolisme : ARN messager, ARN viral, Protéines virales non structurales, RNA replicase, Virus du SRAS.
- Matrices (génétique), RT-PCR, Stabilité de l'ARN.
English descriptors
- KwdEn :
- Gene Expression Regulation, Viral (genetics), RNA Replicase (genetics), RNA Replicase (metabolism), RNA Stability, RNA, Messenger (genetics), RNA, Messenger (metabolism), RNA, Viral (genetics), RNA, Viral (metabolism), Reverse Transcriptase Polymerase Chain Reaction, SARS Virus (genetics), SARS Virus (metabolism), Templates, Genetic, Viral Nonstructural Proteins (genetics), Viral Nonstructural Proteins (metabolism).
- MESH :
- chemical , genetics : RNA Replicase, RNA, Messenger, RNA, Viral, Viral Nonstructural Proteins.
- genetics : Gene Expression Regulation, Viral, SARS Virus.
- chemical , metabolism : RNA Replicase, RNA, Messenger, RNA, Viral, SARS Virus, Viral Nonstructural Proteins.
- RNA Stability, Reverse Transcriptase Polymerase Chain Reaction, Templates, Genetic.
Abstract
SARS coronavirus (SCoV) nonstructural protein (nsp) 1, a potent inhibitor of host gene expression, possesses a unique mode of action: it binds to 40S ribosomes to inactivate their translation functions and induces host mRNA degradation. Our previous study demonstrated that nsp1 induces RNA modification near the 5′-end of a reporter mRNA having a short 5′ untranslated region and RNA cleavage in the encephalomyocarditis virus internal ribosome entry site (IRES) region of a dicistronic RNA template, but not in those IRES elements from hepatitis C or cricket paralysis viruses. By using primarily cell-free,
Url:
DOI: 10.1371/journal.ppat.1002433
PubMed: 22174690
PubMed Central: 3234236
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PMC:3234236Le document en format XML
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<front><div type="abstract" xml:lang="en"><p>SARS coronavirus (SCoV) nonstructural protein (nsp) 1, a potent inhibitor of host gene expression, possesses a unique mode of action: it binds to 40S ribosomes to inactivate their translation functions and induces host mRNA degradation. Our previous study demonstrated that nsp1 induces RNA modification near the 5′-end of a reporter mRNA having a short 5′ untranslated region and RNA cleavage in the encephalomyocarditis virus internal ribosome entry site (IRES) region of a dicistronic RNA template, but not in those IRES elements from hepatitis C or cricket paralysis viruses. By using primarily cell-free, <italic>in vitro</italic>
translation systems, the present study revealed that the nsp1 induced endonucleolytic RNA cleavage mainly near the 5′ untranslated region of capped mRNA templates. Experiments using dicistronic mRNAs carrying different IRESes showed that nsp1 induced endonucleolytic RNA cleavage within the ribosome loading region of type I and type II picornavirus IRES elements, but not that of classical swine fever virus IRES, which is characterized as a hepatitis C virus-like IRES. The nsp1-induced RNA cleavage of template mRNAs exhibited no apparent preference for a specific nucleotide sequence at the RNA cleavage sites. Remarkably, SCoV mRNAs, which have a 5′ cap structure and 3′ poly A tail like those of typical host mRNAs, were not susceptible to nsp1-mediated RNA cleavage and importantly, the presence of the 5′-end leader sequence protected the SCoV mRNAs from nsp1-induced endonucleolytic RNA cleavage. The escape of viral mRNAs from nsp1-induced RNA cleavage may be an important strategy by which the virus circumvents the action of nsp1 leading to the efficient accumulation of viral mRNAs and viral proteins during infection.</p>
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<author><name sortKey="Huang, Cheng" sort="Huang, Cheng" uniqKey="Huang C" first="Cheng" last="Huang">Cheng Huang</name>
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</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea>
<placeName><region type="state">Texas</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Lokugamage, Kumari G" sort="Lokugamage, Kumari G" uniqKey="Lokugamage K" first="Kumari G." last="Lokugamage">Kumari G. Lokugamage</name>
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</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea>
<placeName><region type="state">Texas</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Rozovics, Janet M" sort="Rozovics, Janet M" uniqKey="Rozovics J" first="Janet M." last="Rozovics">Janet M. Rozovics</name>
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</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Molecular Genetics, School of Medicine, University of California, Irvine, California</wicri:regionArea>
<placeName><region type="state">Californie</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Narayanan, Krishna" sort="Narayanan, Krishna" uniqKey="Narayanan K" first="Krishna" last="Narayanan">Krishna Narayanan</name>
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</nlm:aff>
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<wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea>
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<author><name sortKey="Semler, Bert L" sort="Semler, Bert L" uniqKey="Semler B" first="Bert L." last="Semler">Bert L. Semler</name>
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</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Molecular Genetics, School of Medicine, University of California, Irvine, California</wicri:regionArea>
<placeName><region type="state">Californie</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Makino, Shinji" sort="Makino, Shinji" uniqKey="Makino S" first="Shinji" last="Makino">Shinji Makino</name>
<affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">SARS Coronavirus nsp1 Protein Induces Template-Dependent Endonucleolytic Cleavage of mRNAs: Viral mRNAs Are Resistant to nsp1-Induced RNA Cleavage</title>
<author><name sortKey="Huang, Cheng" sort="Huang, Cheng" uniqKey="Huang C" first="Cheng" last="Huang">Cheng Huang</name>
<affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea>
<placeName><region type="state">Texas</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Lokugamage, Kumari G" sort="Lokugamage, Kumari G" uniqKey="Lokugamage K" first="Kumari G." last="Lokugamage">Kumari G. Lokugamage</name>
<affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea>
<placeName><region type="state">Texas</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Rozovics, Janet M" sort="Rozovics, Janet M" uniqKey="Rozovics J" first="Janet M." last="Rozovics">Janet M. Rozovics</name>
<affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Molecular Genetics, School of Medicine, University of California, Irvine, California, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Molecular Genetics, School of Medicine, University of California, Irvine, California</wicri:regionArea>
<placeName><region type="state">Californie</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Narayanan, Krishna" sort="Narayanan, Krishna" uniqKey="Narayanan K" first="Krishna" last="Narayanan">Krishna Narayanan</name>
<affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea>
<placeName><region type="state">Texas</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Semler, Bert L" sort="Semler, Bert L" uniqKey="Semler B" first="Bert L." last="Semler">Bert L. Semler</name>
<affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Molecular Genetics, School of Medicine, University of California, Irvine, California, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Molecular Genetics, School of Medicine, University of California, Irvine, California</wicri:regionArea>
<placeName><region type="state">Californie</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Makino, Shinji" sort="Makino, Shinji" uniqKey="Makino S" first="Shinji" last="Makino">Shinji Makino</name>
<affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea>
<placeName><region type="state">Texas</region>
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</analytic>
<series><title level="j">PLoS Pathogens</title>
<idno type="ISSN">1553-7366</idno>
<idno type="eISSN">1553-7374</idno>
<imprint><date when="2011">2011</date>
</imprint>
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<front><div type="abstract" xml:lang="en"><p>SARS coronavirus (SCoV) nonstructural protein (nsp) 1, a potent inhibitor of host gene expression, possesses a unique mode of action: it binds to 40S ribosomes to inactivate their translation functions and induces host mRNA degradation. Our previous study demonstrated that nsp1 induces RNA modification near the 5′-end of a reporter mRNA having a short 5′ untranslated region and RNA cleavage in the encephalomyocarditis virus internal ribosome entry site (IRES) region of a dicistronic RNA template, but not in those IRES elements from hepatitis C or cricket paralysis viruses. By using primarily cell-free, <italic>in vitro</italic>
translation systems, the present study revealed that the nsp1 induced endonucleolytic RNA cleavage mainly near the 5′ untranslated region of capped mRNA templates. Experiments using dicistronic mRNAs carrying different IRESes showed that nsp1 induced endonucleolytic RNA cleavage within the ribosome loading region of type I and type II picornavirus IRES elements, but not that of classical swine fever virus IRES, which is characterized as a hepatitis C virus-like IRES. The nsp1-induced RNA cleavage of template mRNAs exhibited no apparent preference for a specific nucleotide sequence at the RNA cleavage sites. Remarkably, SCoV mRNAs, which have a 5′ cap structure and 3′ poly A tail like those of typical host mRNAs, were not susceptible to nsp1-mediated RNA cleavage and importantly, the presence of the 5′-end leader sequence protected the SCoV mRNAs from nsp1-induced endonucleolytic RNA cleavage. The escape of viral mRNAs from nsp1-induced RNA cleavage may be an important strategy by which the virus circumvents the action of nsp1 leading to the efficient accumulation of viral mRNAs and viral proteins during infection.</p>
</div>
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<pubmed><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">SARS coronavirus nsp1 protein induces template-dependent endonucleolytic cleavage of mRNAs: viral mRNAs are resistant to nsp1-induced RNA cleavage.</title>
<author><name sortKey="Huang, Cheng" sort="Huang, Cheng" uniqKey="Huang C" first="Cheng" last="Huang">Cheng Huang</name>
<affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea>
<placeName><region type="state">Texas</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Lokugamage, Kumari G" sort="Lokugamage, Kumari G" uniqKey="Lokugamage K" first="Kumari G" last="Lokugamage">Kumari G. Lokugamage</name>
</author>
<author><name sortKey="Rozovics, Janet M" sort="Rozovics, Janet M" uniqKey="Rozovics J" first="Janet M" last="Rozovics">Janet M. Rozovics</name>
</author>
<author><name sortKey="Narayanan, Krishna" sort="Narayanan, Krishna" uniqKey="Narayanan K" first="Krishna" last="Narayanan">Krishna Narayanan</name>
</author>
<author><name sortKey="Semler, Bert L" sort="Semler, Bert L" uniqKey="Semler B" first="Bert L" last="Semler">Bert L. Semler</name>
</author>
<author><name sortKey="Makino, Shinji" sort="Makino, Shinji" uniqKey="Makino S" first="Shinji" last="Makino">Shinji Makino</name>
</author>
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<date when="2011">2011</date>
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<idno type="doi">10.1371/journal.ppat.1002433</idno>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">SARS coronavirus nsp1 protein induces template-dependent endonucleolytic cleavage of mRNAs: viral mRNAs are resistant to nsp1-induced RNA cleavage.</title>
<author><name sortKey="Huang, Cheng" sort="Huang, Cheng" uniqKey="Huang C" first="Cheng" last="Huang">Cheng Huang</name>
<affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas, United States of America.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Immunology, The University of Texas Medical Branch, Galveston, Texas</wicri:regionArea>
<placeName><region type="state">Texas</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Lokugamage, Kumari G" sort="Lokugamage, Kumari G" uniqKey="Lokugamage K" first="Kumari G" last="Lokugamage">Kumari G. Lokugamage</name>
</author>
<author><name sortKey="Rozovics, Janet M" sort="Rozovics, Janet M" uniqKey="Rozovics J" first="Janet M" last="Rozovics">Janet M. Rozovics</name>
</author>
<author><name sortKey="Narayanan, Krishna" sort="Narayanan, Krishna" uniqKey="Narayanan K" first="Krishna" last="Narayanan">Krishna Narayanan</name>
</author>
<author><name sortKey="Semler, Bert L" sort="Semler, Bert L" uniqKey="Semler B" first="Bert L" last="Semler">Bert L. Semler</name>
</author>
<author><name sortKey="Makino, Shinji" sort="Makino, Shinji" uniqKey="Makino S" first="Shinji" last="Makino">Shinji Makino</name>
</author>
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<series><title level="j">PLoS pathogens</title>
<idno type="eISSN">1553-7374</idno>
<imprint><date when="2011" type="published">2011</date>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Gene Expression Regulation, Viral (genetics)</term>
<term>RNA Replicase (genetics)</term>
<term>RNA Replicase (metabolism)</term>
<term>RNA Stability</term>
<term>RNA, Messenger (genetics)</term>
<term>RNA, Messenger (metabolism)</term>
<term>RNA, Viral (genetics)</term>
<term>RNA, Viral (metabolism)</term>
<term>Reverse Transcriptase Polymerase Chain Reaction</term>
<term>SARS Virus (genetics)</term>
<term>SARS Virus (metabolism)</term>
<term>Templates, Genetic</term>
<term>Viral Nonstructural Proteins (genetics)</term>
<term>Viral Nonstructural Proteins (metabolism)</term>
</keywords>
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<term>ARN messager (métabolisme)</term>
<term>ARN viral (génétique)</term>
<term>ARN viral (métabolisme)</term>
<term>Matrices (génétique)</term>
<term>Protéines virales non structurales (génétique)</term>
<term>Protéines virales non structurales (métabolisme)</term>
<term>RNA replicase (génétique)</term>
<term>RNA replicase (métabolisme)</term>
<term>RT-PCR</term>
<term>Régulation de l'expression des gènes viraux (génétique)</term>
<term>Stabilité de l'ARN</term>
<term>Virus du SRAS (génétique)</term>
<term>Virus du SRAS (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>RNA Replicase</term>
<term>RNA, Messenger</term>
<term>RNA, Viral</term>
<term>Viral Nonstructural Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Gene Expression Regulation, Viral</term>
<term>SARS Virus</term>
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<term>Protéines virales non structurales</term>
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<term>Régulation de l'expression des gènes viraux</term>
<term>Virus du SRAS</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>RNA Replicase</term>
<term>RNA, Messenger</term>
<term>RNA, Viral</term>
<term>SARS Virus</term>
<term>Viral Nonstructural Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>ARN messager</term>
<term>ARN viral</term>
<term>Protéines virales non structurales</term>
<term>RNA replicase</term>
<term>Virus du SRAS</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>RNA Stability</term>
<term>Reverse Transcriptase Polymerase Chain Reaction</term>
<term>Templates, Genetic</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Matrices (génétique)</term>
<term>RT-PCR</term>
<term>Stabilité de l'ARN</term>
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<front><div type="abstract" xml:lang="en">SARS coronavirus (SCoV) nonstructural protein (nsp) 1, a potent inhibitor of host gene expression, possesses a unique mode of action: it binds to 40S ribosomes to inactivate their translation functions and induces host mRNA degradation. Our previous study demonstrated that nsp1 induces RNA modification near the 5'-end of a reporter mRNA having a short 5' untranslated region and RNA cleavage in the encephalomyocarditis virus internal ribosome entry site (IRES) region of a dicistronic RNA template, but not in those IRES elements from hepatitis C or cricket paralysis viruses. By using primarily cell-free, in vitro translation systems, the present study revealed that the nsp1 induced endonucleolytic RNA cleavage mainly near the 5' untranslated region of capped mRNA templates. Experiments using dicistronic mRNAs carrying different IRESes showed that nsp1 induced endonucleolytic RNA cleavage within the ribosome loading region of type I and type II picornavirus IRES elements, but not that of classical swine fever virus IRES, which is characterized as a hepatitis C virus-like IRES. The nsp1-induced RNA cleavage of template mRNAs exhibited no apparent preference for a specific nucleotide sequence at the RNA cleavage sites. Remarkably, SCoV mRNAs, which have a 5' cap structure and 3' poly A tail like those of typical host mRNAs, were not susceptible to nsp1-mediated RNA cleavage and importantly, the presence of the 5'-end leader sequence protected the SCoV mRNAs from nsp1-induced endonucleolytic RNA cleavage. The escape of viral mRNAs from nsp1-induced RNA cleavage may be an important strategy by which the virus circumvents the action of nsp1 leading to the efficient accumulation of viral mRNAs and viral proteins during infection.</div>
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