Integrative deep sequencing of the mouse lung transcriptome reveals differential expression of diverse classes of small RNAs in response to respiratory virus infection.
Identifieur interne : 001447 ( PubMed/Curation ); précédent : 001446; suivant : 001448Integrative deep sequencing of the mouse lung transcriptome reveals differential expression of diverse classes of small RNAs in response to respiratory virus infection.
Auteurs : Xinxia Peng [États-Unis] ; Lisa Gralinski ; Martin T. Ferris ; Matthew B. Frieman ; Matthew J. Thomas ; Sean Proll ; Marcus J. Korth ; Jennifer R. Tisoncik ; Mark Heise ; Shujun Luo ; Gary P. Schroth ; Terrence M. Tumpey ; Chengjun Li ; Yoshihiro Kawaoka ; Ralph S. Baric ; Michael G. KatzeSource :
- mBio [ 2150-7511 ] ; 2011.
Descripteurs français
- KwdFr :
- Animaux, Infections à Orthomyxoviridae (immunologie), Infections à coronavirus (immunologie), Petit ARN nucléolaire, Poumon (immunologie), Poumon (virologie), Régulation de l'expression des gènes, Souris, Souris de lignée C57BL, Séquençage nucléotidique à haut débit, Transcriptome, microARN (biosynthèse), microARN (génétique).
- MESH :
- biosynthèse : microARN.
- génétique : microARN.
- immunologie : Infections à Orthomyxoviridae, Infections à coronavirus, Poumon.
- virologie : Poumon.
- Animaux, Petit ARN nucléolaire, Régulation de l'expression des gènes, Souris, Souris de lignée C57BL, Séquençage nucléotidique à haut débit, Transcriptome.
English descriptors
- KwdEn :
- Animals, Coronavirus Infections (immunology), Gene Expression Regulation, High-Throughput Nucleotide Sequencing, Lung (immunology), Lung (virology), Mice, Mice, Inbred C57BL, MicroRNAs (biosynthesis), MicroRNAs (genetics), Orthomyxoviridae Infections (immunology), RNA, Small Nucleolar, Transcriptome.
- MESH :
- chemical , biosynthesis : MicroRNAs.
- chemical , genetics : MicroRNAs.
- immunology : Coronavirus Infections, Lung, Orthomyxoviridae Infections.
- virology : Lung.
- Animals, Gene Expression Regulation, High-Throughput Nucleotide Sequencing, Mice, Mice, Inbred C57BL, RNA, Small Nucleolar, Transcriptome.
Abstract
We previously reported widespread differential expression of long non-protein-coding RNAs (ncRNAs) in response to virus infection. Here, we expanded the study through small RNA transcriptome sequencing analysis of the host response to both severe acute respiratory syndrome coronavirus (SARS-CoV) and influenza virus infections across four founder mouse strains of the Collaborative Cross, a recombinant inbred mouse resource for mapping complex traits. We observed differential expression of over 200 small RNAs of diverse classes during infection. A majority of identified microRNAs (miRNAs) showed divergent changes in expression across mouse strains with respect to SARS-CoV and influenza virus infections and responded differently to a highly pathogenic reconstructed 1918 virus compared to a minimally pathogenic seasonal influenza virus isolate. Novel insights into miRNA expression changes, including the association with pathogenic outcomes and large differences between in vivo and in vitro experimental systems, were further elucidated by a survey of selected miRNAs across diverse virus infections. The small RNAs identified also included many non-miRNA small RNAs, such as small nucleolar RNAs (snoRNAs), in addition to nonannotated small RNAs. An integrative sequencing analysis of both small RNAs and long transcripts from the same samples showed that the results revealing differential expression of miRNAs during infection were largely due to transcriptional regulation and that the predicted miRNA-mRNA network could modulate global host responses to virus infection in a combinatorial fashion. These findings represent the first integrated sequencing analysis of the response of host small RNAs to virus infection and show that small RNAs are an integrated component of complex networks involved in regulating the host response to infection.
DOI: 10.1128/mBio.00198-11
PubMed: 22086488
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Baric</name></author><author><name sortKey="Katze, Michael G" sort="Katze, Michael G" uniqKey="Katze M" first="Michael G" last="Katze">Michael G. Katze</name></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2011" type="published">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Coronavirus Infections (immunology)</term><term>Gene Expression Regulation</term><term>High-Throughput Nucleotide Sequencing</term><term>Lung (immunology)</term><term>Lung (virology)</term><term>Mice</term><term>Mice, Inbred C57BL</term><term>MicroRNAs (biosynthesis)</term><term>MicroRNAs (genetics)</term><term>Orthomyxoviridae Infections (immunology)</term><term>RNA, Small Nucleolar</term><term>Transcriptome</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux</term><term>Infections à Orthomyxoviridae (immunologie)</term><term>Infections à coronavirus (immunologie)</term><term>Petit ARN nucléolaire</term><term>Poumon (immunologie)</term><term>Poumon (virologie)</term><term>Régulation de l'expression des gènes</term><term>Souris</term><term>Souris de lignée C57BL</term><term>Séquençage nucléotidique à haut débit</term><term>Transcriptome</term><term>microARN (biosynthèse)</term><term>microARN (génétique)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="biosynthesis" xml:lang="en"><term>MicroRNAs</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>MicroRNAs</term></keywords><keywords scheme="MESH" qualifier="biosynthèse" xml:lang="fr"><term>microARN</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>microARN</term></keywords><keywords scheme="MESH" qualifier="immunologie" xml:lang="fr"><term>Infections à Orthomyxoviridae</term><term>Infections à coronavirus</term><term>Poumon</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Coronavirus Infections</term><term>Lung</term><term>Orthomyxoviridae Infections</term></keywords><keywords scheme="MESH" qualifier="virologie" xml:lang="fr"><term>Poumon</term></keywords><keywords scheme="MESH" qualifier="virology" xml:lang="en"><term>Lung</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Gene Expression Regulation</term><term>High-Throughput Nucleotide Sequencing</term><term>Mice</term><term>Mice, Inbred C57BL</term><term>RNA, Small Nucleolar</term><term>Transcriptome</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Petit ARN nucléolaire</term><term>Régulation de l'expression des gènes</term><term>Souris</term><term>Souris de lignée C57BL</term><term>Séquençage nucléotidique à haut débit</term><term>Transcriptome</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">We previously reported widespread differential expression of long non-protein-coding RNAs (ncRNAs) in response to virus infection. Here, we expanded the study through small RNA transcriptome sequencing analysis of the host response to both severe acute respiratory syndrome coronavirus (SARS-CoV) and influenza virus infections across four founder mouse strains of the Collaborative Cross, a recombinant inbred mouse resource for mapping complex traits. We observed differential expression of over 200 small RNAs of diverse classes during infection. A majority of identified microRNAs (miRNAs) showed divergent changes in expression across mouse strains with respect to SARS-CoV and influenza virus infections and responded differently to a highly pathogenic reconstructed 1918 virus compared to a minimally pathogenic seasonal influenza virus isolate. Novel insights into miRNA expression changes, including the association with pathogenic outcomes and large differences between in vivo and in vitro experimental systems, were further elucidated by a survey of selected miRNAs across diverse virus infections. The small RNAs identified also included many non-miRNA small RNAs, such as small nucleolar RNAs (snoRNAs), in addition to nonannotated small RNAs. An integrative sequencing analysis of both small RNAs and long transcripts from the same samples showed that the results revealing differential expression of miRNAs during infection were largely due to transcriptional regulation and that the predicted miRNA-mRNA network could modulate global host responses to virus infection in a combinatorial fashion. These findings represent the first integrated sequencing analysis of the response of host small RNAs to virus infection and show that small RNAs are an integrated component of complex networks involved in regulating the host response to infection.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">22086488</PMID><DateCompleted><Year>2012</Year><Month>03</Month><Day>07</Day></DateCompleted><DateRevised><Year>2020</Year><Month>04</Month><Day>04</Day></DateRevised><Article PubModel="Electronic-Print"><Journal><ISSN IssnType="Electronic">2150-7511</ISSN><JournalIssue CitedMedium="Internet"><Volume>2</Volume><Issue>6</Issue><PubDate><Year>2011</Year></PubDate></JournalIssue><Title>mBio</Title><ISOAbbreviation>mBio</ISOAbbreviation></Journal><ArticleTitle>Integrative deep sequencing of the mouse lung transcriptome reveals differential expression of diverse classes of small RNAs in response to respiratory virus infection.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1128/mBio.00198-11</ELocationID><ELocationID EIdType="pii" ValidYN="Y">e00198-11</ELocationID><Abstract><AbstractText Label="UNLABELLED">We previously reported widespread differential expression of long non-protein-coding RNAs (ncRNAs) in response to virus infection. Here, we expanded the study through small RNA transcriptome sequencing analysis of the host response to both severe acute respiratory syndrome coronavirus (SARS-CoV) and influenza virus infections across four founder mouse strains of the Collaborative Cross, a recombinant inbred mouse resource for mapping complex traits. We observed differential expression of over 200 small RNAs of diverse classes during infection. A majority of identified microRNAs (miRNAs) showed divergent changes in expression across mouse strains with respect to SARS-CoV and influenza virus infections and responded differently to a highly pathogenic reconstructed 1918 virus compared to a minimally pathogenic seasonal influenza virus isolate. Novel insights into miRNA expression changes, including the association with pathogenic outcomes and large differences between in vivo and in vitro experimental systems, were further elucidated by a survey of selected miRNAs across diverse virus infections. The small RNAs identified also included many non-miRNA small RNAs, such as small nucleolar RNAs (snoRNAs), in addition to nonannotated small RNAs. An integrative sequencing analysis of both small RNAs and long transcripts from the same samples showed that the results revealing differential expression of miRNAs during infection were largely due to transcriptional regulation and that the predicted miRNA-mRNA network could modulate global host responses to virus infection in a combinatorial fashion. These findings represent the first integrated sequencing analysis of the response of host small RNAs to virus infection and show that small RNAs are an integrated component of complex networks involved in regulating the host response to infection.</AbstractText><AbstractText Label="IMPORTANCE" NlmCategory="OBJECTIVE">Most studies examining the host transcriptional response to infection focus only on protein-coding genes. However, mammalian genomes transcribe many short and long non-protein-coding RNAs (ncRNAs). With the advent of deep-sequencing technologies, systematic transcriptome analysis of the host response, including analysis of ncRNAs of different sizes, is now possible. Using this approach, we recently discovered widespread differential expression of host long (>200 nucleotide [nt]) ncRNAs in response to virus infection. Here, the samples described in the previous report were again used, but we sequenced another fraction of the transcriptome to study very short (about 20 to 30 nt) ncRNAs. We demonstrated that virus infection also altered expression of many short ncRNAs of diverse classes. Putting the results of the two studies together, we show that small RNAs may also play an important role in regulating the host response to virus infection.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Peng</LastName><ForeName>Xinxia</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gralinski</LastName><ForeName>Lisa</ForeName><Initials>L</Initials></Author><Author ValidYN="Y"><LastName>Ferris</LastName><ForeName>Martin T</ForeName><Initials>MT</Initials></Author><Author ValidYN="Y"><LastName>Frieman</LastName><ForeName>Matthew B</ForeName><Initials>MB</Initials></Author><Author ValidYN="Y"><LastName>Thomas</LastName><ForeName>Matthew J</ForeName><Initials>MJ</Initials></Author><Author ValidYN="Y"><LastName>Proll</LastName><ForeName>Sean</ForeName><Initials>S</Initials></Author><Author ValidYN="Y"><LastName>Korth</LastName><ForeName>Marcus J</ForeName><Initials>MJ</Initials></Author><Author ValidYN="Y"><LastName>Tisoncik</LastName><ForeName>Jennifer R</ForeName><Initials>JR</Initials></Author><Author ValidYN="Y"><LastName>Heise</LastName><ForeName>Mark</ForeName><Initials>M</Initials></Author><Author ValidYN="Y"><LastName>Luo</LastName><ForeName>Shujun</ForeName><Initials>S</Initials></Author><Author ValidYN="Y"><LastName>Schroth</LastName><ForeName>Gary P</ForeName><Initials>GP</Initials></Author><Author ValidYN="Y"><LastName>Tumpey</LastName><ForeName>Terrence M</ForeName><Initials>TM</Initials></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Chengjun</ForeName><Initials>C</Initials></Author><Author ValidYN="Y"><LastName>Kawaoka</LastName><ForeName>Yoshihiro</ForeName><Initials>Y</Initials></Author><Author ValidYN="Y"><LastName>Baric</LastName><ForeName>Ralph S</ForeName><Initials>RS</Initials></Author><Author ValidYN="Y"><LastName>Katze</LastName><ForeName>Michael G</ForeName><Initials>MG</Initials></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>HHSN272200800060C</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>P51 OD010425</GrantID><Acronym>OD</Acronym><Agency>NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>U54 AI081680</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2011</Year><Month>11</Month><Day>15</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>mBio</MedlineTA><NlmUniqueID>101519231</NlmUniqueID></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D035683">MicroRNAs</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D020537">RNA, Small Nucleolar</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018352" MajorTopicYN="N">Coronavirus Infections</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005786" MajorTopicYN="Y">Gene Expression Regulation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D059014" MajorTopicYN="N">High-Throughput Nucleotide Sequencing</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008168" MajorTopicYN="N">Lung</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName><QualifierName UI="Q000821" MajorTopicYN="Y">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008810" MajorTopicYN="N">Mice, Inbred C57BL</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D035683" MajorTopicYN="N">MicroRNAs</DescriptorName><QualifierName UI="Q000096" MajorTopicYN="Y">biosynthesis</QualifierName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D009976" MajorTopicYN="N">Orthomyxoviridae Infections</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020537" MajorTopicYN="N">RNA, Small Nucleolar</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D059467" 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