Influenza induces endoplasmic reticulum stress, caspase-12-dependent apoptosis, and c-Jun N-terminal kinase-mediated transforming growth factor-β release in lung epithelial cells.
Identifieur interne : 000617 ( PubMed/Corpus ); précédent : 000616; suivant : 000618Influenza induces endoplasmic reticulum stress, caspase-12-dependent apoptosis, and c-Jun N-terminal kinase-mediated transforming growth factor-β release in lung epithelial cells.
Auteurs : Elle C. Roberson ; Jane E. Tully ; Amy S. Guala ; Jessica N. Reiss ; Karolyn E. Godburn ; Derek A. Pociask ; John F. Alcorn ; David W H. Riches ; Oliver Dienz ; Yvonne M W. Janssen-Heininger ; Vikas AnathySource :
- American journal of respiratory cell and molecular biology [ 1535-4989 ] ; 2012.
English descriptors
- KwdEn :
- Animals, Apoptosis, Caspase 12 (metabolism), Cells, Cultured, Endoplasmic Reticulum (drug effects), Endoplasmic Reticulum (metabolism), Endoplasmic Reticulum (virology), Endoplasmic Reticulum Stress, Enzyme Activation, Enzyme-Linked Immunosorbent Assay, Influenza A Virus, H1N1 Subtype (physiology), JNK Mitogen-Activated Protein Kinases (metabolism), Lung (metabolism), Lung (pathology), Lung (virology), Mice, Mice, Inbred C57BL, Orthomyxoviridae Infections (metabolism), Orthomyxoviridae Infections (pathology), Respiratory Mucosa (metabolism), Respiratory Mucosa (pathology), Respiratory Mucosa (virology), Staurosporine (pharmacology), Thapsigargin (pharmacology), Transcription Factors (genetics), Transcription Factors (metabolism), Transforming Growth Factor beta (metabolism), Viral Load.
- MESH :
- chemical , genetics : Transcription Factors.
- chemical , metabolism : Caspase 12, JNK Mitogen-Activated Protein Kinases, Transcription Factors, Transforming Growth Factor beta.
- drug effects : Endoplasmic Reticulum.
- metabolism : Endoplasmic Reticulum, Lung, Orthomyxoviridae Infections, Respiratory Mucosa.
- pathology : Lung, Orthomyxoviridae Infections, Respiratory Mucosa.
- chemical , pharmacology : Staurosporine, Thapsigargin.
- physiology : Influenza A Virus, H1N1 Subtype.
- virology : Endoplasmic Reticulum, Lung, Respiratory Mucosa.
- Animals, Apoptosis, Cells, Cultured, Endoplasmic Reticulum Stress, Enzyme Activation, Enzyme-Linked Immunosorbent Assay, Mice, Mice, Inbred C57BL, Viral Load.
Abstract
Influenza A virus (IAV) infection is known to induce endoplasmic reticulum (ER) stress, Fas-dependent apoptosis, and TGF-β production in a variety of cells. However, the relationship between these events in murine primary tracheal epithelial cells (MTECS), which are considered one of the primary sites of IAV infection and replication, is unclear. We show that IAV infection induced ER stress marker activating transcription factor-6 and endoplasmic reticulum protein 57-kD (ERp57), but not C/EBP homologous protein (CHOP). In contrast, the ER stress inducer thapsigargin (THP) increased CHOP. IAV infection activated caspases and apoptosis, independently of Fas and caspase-8, in MTECs. Instead, apoptosis was mediated by caspase-12. A decrease in ERp57 attenuated the IAV burden and decreased caspase-12 activation and apoptosis in epithelial cells. TGF-β production was enhanced in IAV-infected MTECs, compared with THP or staurosporine. IAV infection caused the activation of c-Jun N-terminal kinase (JNK). Furthermore, IAV-induced TGF-β production required the presence of JNK1, a finding that suggests a role for JNK1 in IAV-induced epithelial injury and subsequent TGF-β production. These novel findings suggest a potential mechanistic role for a distinct ER stress response induced by IAV, and a profibrogenic/repair response in contrast to other pharmacological inducers of ER stress. These responses may also have a potential role in acute lung injury, fibroproliferative acute respiratory distress syndrome, and the recently identified H1N1 influenza-induced exacerbations of chronic obstructive pulmonary disease (Wedzicha JA. Proc Am Thorac Soc 2004;1:115-120) and idiopathic pulmonary fibrosis (Umeda Y, et al. Int Med 2010;49:2333-2336).
DOI: 10.1165/rcmb.2010-0460OC
PubMed: 21799120
Links to Exploration step
pubmed:21799120Le document en format XML
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Roberson</name><affiliation><nlm:affiliation>Department of Pathology, University of Vermont, Burlington, VT 05405, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Tully, Jane E" sort="Tully, Jane E" uniqKey="Tully J" first="Jane E" last="Tully">Jane E. Tully</name></author><author><name sortKey="Guala, Amy S" sort="Guala, Amy S" uniqKey="Guala A" first="Amy S" last="Guala">Amy S. Guala</name></author><author><name sortKey="Reiss, Jessica N" sort="Reiss, Jessica N" uniqKey="Reiss J" first="Jessica N" last="Reiss">Jessica N. Reiss</name></author><author><name sortKey="Godburn, Karolyn E" sort="Godburn, Karolyn E" uniqKey="Godburn K" first="Karolyn E" last="Godburn">Karolyn E. Godburn</name></author><author><name sortKey="Pociask, Derek A" sort="Pociask, Derek A" uniqKey="Pociask D" first="Derek A" last="Pociask">Derek A. Pociask</name></author><author><name sortKey="Alcorn, John F" sort="Alcorn, John F" uniqKey="Alcorn J" first="John F" last="Alcorn">John F. Alcorn</name></author><author><name sortKey="Riches, David W H" sort="Riches, David W H" uniqKey="Riches D" first="David W H" last="Riches">David W H. Riches</name></author><author><name sortKey="Dienz, Oliver" sort="Dienz, Oliver" uniqKey="Dienz O" first="Oliver" last="Dienz">Oliver Dienz</name></author><author><name sortKey="Janssen Heininger, Yvonne M W" sort="Janssen Heininger, Yvonne M W" uniqKey="Janssen Heininger Y" first="Yvonne M W" last="Janssen-Heininger">Yvonne M W. Janssen-Heininger</name></author><author><name sortKey="Anathy, Vikas" sort="Anathy, Vikas" uniqKey="Anathy V" first="Vikas" last="Anathy">Vikas Anathy</name></author></analytic><series><title level="j">American journal of respiratory cell and molecular biology</title><idno type="eISSN">1535-4989</idno><imprint><date when="2012" type="published">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Apoptosis</term><term>Caspase 12 (metabolism)</term><term>Cells, Cultured</term><term>Endoplasmic Reticulum (drug effects)</term><term>Endoplasmic Reticulum (metabolism)</term><term>Endoplasmic Reticulum (virology)</term><term>Endoplasmic Reticulum Stress</term><term>Enzyme Activation</term><term>Enzyme-Linked Immunosorbent Assay</term><term>Influenza A Virus, H1N1 Subtype (physiology)</term><term>JNK Mitogen-Activated Protein Kinases (metabolism)</term><term>Lung (metabolism)</term><term>Lung (pathology)</term><term>Lung (virology)</term><term>Mice</term><term>Mice, Inbred C57BL</term><term>Orthomyxoviridae Infections (metabolism)</term><term>Orthomyxoviridae Infections (pathology)</term><term>Respiratory Mucosa (metabolism)</term><term>Respiratory Mucosa (pathology)</term><term>Respiratory Mucosa (virology)</term><term>Staurosporine (pharmacology)</term><term>Thapsigargin (pharmacology)</term><term>Transcription Factors (genetics)</term><term>Transcription Factors (metabolism)</term><term>Transforming Growth Factor beta (metabolism)</term><term>Viral Load</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Transcription Factors</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Caspase 12</term><term>JNK Mitogen-Activated Protein Kinases</term><term>Transcription Factors</term><term>Transforming Growth Factor beta</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Endoplasmic Reticulum</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Endoplasmic Reticulum</term><term>Lung</term><term>Orthomyxoviridae Infections</term><term>Respiratory Mucosa</term></keywords><keywords scheme="MESH" qualifier="pathology" xml:lang="en"><term>Lung</term><term>Orthomyxoviridae Infections</term><term>Respiratory Mucosa</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Staurosporine</term><term>Thapsigargin</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Influenza A Virus, H1N1 Subtype</term></keywords><keywords scheme="MESH" qualifier="virology" xml:lang="en"><term>Endoplasmic Reticulum</term><term>Lung</term><term>Respiratory Mucosa</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Apoptosis</term><term>Cells, Cultured</term><term>Endoplasmic Reticulum Stress</term><term>Enzyme Activation</term><term>Enzyme-Linked Immunosorbent Assay</term><term>Mice</term><term>Mice, Inbred C57BL</term><term>Viral Load</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Influenza A virus (IAV) infection is known to induce endoplasmic reticulum (ER) stress, Fas-dependent apoptosis, and TGF-β production in a variety of cells. However, the relationship between these events in murine primary tracheal epithelial cells (MTECS), which are considered one of the primary sites of IAV infection and replication, is unclear. We show that IAV infection induced ER stress marker activating transcription factor-6 and endoplasmic reticulum protein 57-kD (ERp57), but not C/EBP homologous protein (CHOP). In contrast, the ER stress inducer thapsigargin (THP) increased CHOP. IAV infection activated caspases and apoptosis, independently of Fas and caspase-8, in MTECs. Instead, apoptosis was mediated by caspase-12. A decrease in ERp57 attenuated the IAV burden and decreased caspase-12 activation and apoptosis in epithelial cells. TGF-β production was enhanced in IAV-infected MTECs, compared with THP or staurosporine. IAV infection caused the activation of c-Jun N-terminal kinase (JNK). Furthermore, IAV-induced TGF-β production required the presence of JNK1, a finding that suggests a role for JNK1 in IAV-induced epithelial injury and subsequent TGF-β production. These novel findings suggest a potential mechanistic role for a distinct ER stress response induced by IAV, and a profibrogenic/repair response in contrast to other pharmacological inducers of ER stress. These responses may also have a potential role in acute lung injury, fibroproliferative acute respiratory distress syndrome, and the recently identified H1N1 influenza-induced exacerbations of chronic obstructive pulmonary disease (Wedzicha JA. Proc Am Thorac Soc 2004;1:115-120) and idiopathic pulmonary fibrosis (Umeda Y, et al. Int Med 2010;49:2333-2336).</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">21799120</PMID><DateCompleted><Year>2012</Year><Month>06</Month><Day>25</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1535-4989</ISSN><JournalIssue CitedMedium="Internet"><Volume>46</Volume><Issue>5</Issue><PubDate><Year>2012</Year><Month>May</Month></PubDate></JournalIssue><Title>American journal of respiratory cell and molecular biology</Title><ISOAbbreviation>Am. J. Respir. Cell Mol. Biol.</ISOAbbreviation></Journal><ArticleTitle>Influenza induces endoplasmic reticulum stress, caspase-12-dependent apoptosis, and c-Jun N-terminal kinase-mediated transforming growth factor-β release in lung epithelial cells.</ArticleTitle><Pagination><MedlinePgn>573-81</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1165/rcmb.2010-0460OC</ELocationID><Abstract><AbstractText>Influenza A virus (IAV) infection is known to induce endoplasmic reticulum (ER) stress, Fas-dependent apoptosis, and TGF-β production in a variety of cells. However, the relationship between these events in murine primary tracheal epithelial cells (MTECS), which are considered one of the primary sites of IAV infection and replication, is unclear. We show that IAV infection induced ER stress marker activating transcription factor-6 and endoplasmic reticulum protein 57-kD (ERp57), but not C/EBP homologous protein (CHOP). In contrast, the ER stress inducer thapsigargin (THP) increased CHOP. IAV infection activated caspases and apoptosis, independently of Fas and caspase-8, in MTECs. Instead, apoptosis was mediated by caspase-12. A decrease in ERp57 attenuated the IAV burden and decreased caspase-12 activation and apoptosis in epithelial cells. TGF-β production was enhanced in IAV-infected MTECs, compared with THP or staurosporine. IAV infection caused the activation of c-Jun N-terminal kinase (JNK). Furthermore, IAV-induced TGF-β production required the presence of JNK1, a finding that suggests a role for JNK1 in IAV-induced epithelial injury and subsequent TGF-β production. These novel findings suggest a potential mechanistic role for a distinct ER stress response induced by IAV, and a profibrogenic/repair response in contrast to other pharmacological inducers of ER stress. These responses may also have a potential role in acute lung injury, fibroproliferative acute respiratory distress syndrome, and the recently identified H1N1 influenza-induced exacerbations of chronic obstructive pulmonary disease (Wedzicha JA. Proc Am Thorac Soc 2004;1:115-120) and idiopathic pulmonary fibrosis (Umeda Y, et al. Int Med 2010;49:2333-2336).</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Roberson</LastName><ForeName>Elle C</ForeName><Initials>EC</Initials><AffiliationInfo><Affiliation>Department of Pathology, University of Vermont, Burlington, VT 05405, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tully</LastName><ForeName>Jane E</ForeName><Initials>JE</Initials></Author><Author ValidYN="Y"><LastName>Guala</LastName><ForeName>Amy S</ForeName><Initials>AS</Initials></Author><Author ValidYN="Y"><LastName>Reiss</LastName><ForeName>Jessica N</ForeName><Initials>JN</Initials></Author><Author ValidYN="Y"><LastName>Godburn</LastName><ForeName>Karolyn E</ForeName><Initials>KE</Initials></Author><Author ValidYN="Y"><LastName>Pociask</LastName><ForeName>Derek A</ForeName><Initials>DA</Initials></Author><Author ValidYN="Y"><LastName>Alcorn</LastName><ForeName>John F</ForeName><Initials>JF</Initials></Author><Author ValidYN="Y"><LastName>Riches</LastName><ForeName>David W H</ForeName><Initials>DW</Initials></Author><Author ValidYN="Y"><LastName>Dienz</LastName><ForeName>Oliver</ForeName><Initials>O</Initials></Author><Author ValidYN="Y"><LastName>Janssen-Heininger</LastName><ForeName>Yvonne M W</ForeName><Initials>YM</Initials></Author><Author ValidYN="Y"><LastName>Anathy</LastName><ForeName>Vikas</ForeName><Initials>V</Initials></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>P20 RR021905</GrantID><Acronym>RR</Acronym><Agency>NCRR NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>P20 RR021905-05</GrantID><Acronym>RR</Acronym><Agency>NCRR NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 HL079331</GrantID><Acronym>HL</Acronym><Agency>NHLBI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>HL079331</GrantID><Acronym>HL</Acronym><Agency>NHLBI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>P20 GM103496</GrantID><Acronym>GM</Acronym><Agency>NIGMS 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><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2011</Year><Month>07</Month><Day>28</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Am J Respir Cell Mol Biol</MedlineTA><NlmUniqueID>8917225</NlmUniqueID><ISSNLinking>1044-1549</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D014157">Transcription Factors</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D016212">Transforming Growth Factor beta</NameOfSubstance></Chemical><Chemical><RegistryNumber>67526-95-8</RegistryNumber><NameOfSubstance UI="D019284">Thapsigargin</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.7.11.24</RegistryNumber><NameOfSubstance UI="D048031">JNK Mitogen-Activated Protein Kinases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.4.22.-</RegistryNumber><NameOfSubstance UI="D053454">Caspase 12</NameOfSubstance></Chemical><Chemical><RegistryNumber>H88EPA0A3N</RegistryNumber><NameOfSubstance UI="D019311">Staurosporine</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D017209" MajorTopicYN="Y">Apoptosis</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D053454" MajorTopicYN="N">Caspase 12</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002478" MajorTopicYN="N">Cells, Cultured</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D004721" MajorTopicYN="N">Endoplasmic Reticulum</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D059865" MajorTopicYN="Y">Endoplasmic Reticulum Stress</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D004789" MajorTopicYN="N">Enzyme Activation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D004797" MajorTopicYN="N">Enzyme-Linked Immunosorbent Assay</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D053118" MajorTopicYN="N">Influenza A Virus, H1N1 Subtype</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D048031" MajorTopicYN="N">JNK Mitogen-Activated Protein Kinases</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008168" MajorTopicYN="N">Lung</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName><QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">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="D009976" MajorTopicYN="N">Orthomyxoviridae Infections</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName><QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020545" MajorTopicYN="N">Respiratory Mucosa</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName><QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName><QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D019311" MajorTopicYN="N">Staurosporine</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D019284" MajorTopicYN="N">Thapsigargin</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014157" MajorTopicYN="N">Transcription Factors</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D016212" MajorTopicYN="N">Transforming Growth Factor beta</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D019562" MajorTopicYN="N">Viral Load</DescriptorName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2011</Year><Month>7</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2011</Year><Month>7</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2012</Year><Month>6</Month><Day>26</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">21799120</ArticleId><ArticleId IdType="pii">2010-0460OC</ArticleId><ArticleId 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