A Ubl/ubiquitin switch in the activation of Parkin.
Identifieur interne : 000604 ( PubMed/Checkpoint ); précédent : 000603; suivant : 000605A Ubl/ubiquitin switch in the activation of Parkin.
Auteurs : Véronique Sauvé [Canada] ; Asparouh Lilov [Canada] ; Marjan Seirafi [Canada] ; Marta Vranas [Canada] ; Shafqat Rasool [Canada] ; Guennadi Kozlov [Canada] ; Tara Sprules [Canada] ; Jimin Wang [États-Unis] ; Jean-François Trempe [Canada] ; Kalle Gehring [Canada]Source :
- The EMBO journal [ 1460-2075 ] ; 2015.
English descriptors
- KwdEn :
- Cloning, Molecular, Crystallization, Enzyme Activation (genetics), Humans, Mitochondria (metabolism), Models, Molecular, Mutagenesis, Nuclear Magnetic Resonance, Biomolecular, Phosphorylation, Protein Binding, Protein Conformation, Protein Kinases (chemistry), Protein Kinases (metabolism), Protein Structure, Tertiary, Scattering, Small Angle, Ubiquitin (metabolism), Ubiquitin-Conjugating Enzymes (metabolism), Ubiquitin-Protein Ligases (chemistry), Ubiquitin-Protein Ligases (metabolism).
- MESH :
- chemical , chemistry : Protein Kinases, Ubiquitin-Protein Ligases.
- genetics : Enzyme Activation.
- metabolism : Mitochondria, Protein Kinases, Ubiquitin, Ubiquitin-Conjugating Enzymes, Ubiquitin-Protein Ligases.
- Cloning, Molecular, Crystallization, Humans, Models, Molecular, Mutagenesis, Nuclear Magnetic Resonance, Biomolecular, Phosphorylation, Protein Binding, Protein Conformation, Protein Structure, Tertiary, Scattering, Small Angle.
Abstract
Mutations in Parkin and PINK1 cause an inherited early-onset form of Parkinson's disease. The two proteins function together in a mitochondrial quality control pathway whereby PINK1 accumulates on damaged mitochondria and activates Parkin to induce mitophagy. How PINK1 kinase activity releases the auto-inhibited ubiquitin ligase activity of Parkin remains unclear. Here, we identify a binding switch between phospho-ubiquitin (pUb) and the ubiquitin-like domain (Ubl) of Parkin as a key element. By mutagenesis and SAXS, we show that pUb binds to RING1 of Parkin at a site formed by His302 and Arg305. pUb binding promotes disengagement of the Ubl from RING1 and subsequent Parkin phosphorylation. A crystal structure of Parkin Δ86-130 at 2.54 Å resolution allowed the design of mutations that specifically release the Ubl domain from RING1. These mutations mimic pUb binding and promote Parkin phosphorylation. Measurements of the E2 ubiquitin-conjugating enzyme UbcH7 binding to Parkin and Parkin E3 ligase activity suggest that Parkin phosphorylation regulates E3 ligase activity downstream of pUb binding.
DOI: 10.15252/embj.201592237
PubMed: 26254305
Affiliations:
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Department of Biochemistry, McGill University, Montréal, QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC</wicri:regionArea><orgName type="university">Université McGill</orgName><placeName><settlement type="city">Montréal</settlement><region type="state">Québec</region></placeName></affiliation></author><author><name sortKey="Sprules, Tara" sort="Sprules, Tara" uniqKey="Sprules T" first="Tara" last="Sprules">Tara Sprules</name><affiliation wicri:level="1"><nlm:affiliation>Quebec/Eastern Canada High Field NMR Facility (QANUC), Montréal, QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Quebec/Eastern Canada High Field NMR Facility (QANUC), Montréal, QC</wicri:regionArea><wicri:noRegion>QC</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Jimin" sort="Wang, Jimin" uniqKey="Wang J" 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Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC</wicri:regionArea><orgName type="university">Université McGill</orgName><placeName><settlement type="city">Montréal</settlement><region type="state">Québec</region></placeName></affiliation></author><author><name sortKey="Lilov, Asparouh" sort="Lilov, Asparouh" uniqKey="Lilov A" first="Asparouh" last="Lilov">Asparouh Lilov</name><affiliation wicri:level="4"><nlm:affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC</wicri:regionArea><orgName type="university">Université McGill</orgName><placeName><settlement type="city">Montréal</settlement><region type="state">Québec</region></placeName></affiliation></author><author><name sortKey="Seirafi, Marjan" sort="Seirafi, Marjan" uniqKey="Seirafi M" first="Marjan" last="Seirafi">Marjan Seirafi</name><affiliation wicri:level="4"><nlm:affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC</wicri:regionArea><orgName type="university">Université McGill</orgName><placeName><settlement type="city">Montréal</settlement><region type="state">Québec</region></placeName></affiliation></author><author><name sortKey="Vranas, Marta" sort="Vranas, Marta" uniqKey="Vranas M" first="Marta" last="Vranas">Marta Vranas</name><affiliation wicri:level="4"><nlm:affiliation>Department of Pharmacology and Therapeutics, McGill University, Montréal, QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Pharmacology and Therapeutics, McGill University, Montréal, QC</wicri:regionArea><orgName type="university">Université McGill</orgName><placeName><settlement type="city">Montréal</settlement><region type="state">Québec</region></placeName></affiliation></author><author><name sortKey="Rasool, Shafqat" sort="Rasool, Shafqat" uniqKey="Rasool S" first="Shafqat" last="Rasool">Shafqat Rasool</name><affiliation wicri:level="4"><nlm:affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada Department of Pharmacology and Therapeutics, McGill University, Montréal, QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada Department of Pharmacology and Therapeutics, McGill University, Montréal, QC</wicri:regionArea><orgName type="university">Université McGill</orgName><placeName><settlement type="city">Montréal</settlement><region type="state">Québec</region></placeName></affiliation></author><author><name sortKey="Kozlov, Guennadi" sort="Kozlov, Guennadi" uniqKey="Kozlov G" first="Guennadi" last="Kozlov">Guennadi Kozlov</name><affiliation wicri:level="4"><nlm:affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC</wicri:regionArea><orgName type="university">Université McGill</orgName><placeName><settlement type="city">Montréal</settlement><region type="state">Québec</region></placeName></affiliation></author><author><name sortKey="Sprules, Tara" sort="Sprules, Tara" uniqKey="Sprules T" first="Tara" last="Sprules">Tara Sprules</name><affiliation wicri:level="1"><nlm:affiliation>Quebec/Eastern Canada High Field NMR Facility (QANUC), Montréal, QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Quebec/Eastern Canada High Field NMR Facility (QANUC), Montréal, QC</wicri:regionArea><wicri:noRegion>QC</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Jimin" sort="Wang, Jimin" uniqKey="Wang J" first="Jimin" last="Wang">Jimin Wang</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT</wicri:regionArea><placeName><region type="state">Connecticut</region></placeName></affiliation></author><author><name sortKey="Trempe, Jean Francois" sort="Trempe, Jean Francois" uniqKey="Trempe J" first="Jean-François" last="Trempe">Jean-François Trempe</name><affiliation wicri:level="4"><nlm:affiliation>Department of Pharmacology and Therapeutics, McGill University, Montréal, QC, Canada jeanfrancois.trempe@mcgill.ca kalle.gehring@mcgill.ca.</nlm:affiliation><country wicri:rule="url">Canada</country><wicri:regionArea>Department of Pharmacology and Therapeutics, McGill University, Montréal, QC</wicri:regionArea><orgName type="university">Université McGill</orgName><placeName><settlement type="city">Montréal</settlement><region type="state">Québec</region></placeName></affiliation></author><author><name sortKey="Gehring, Kalle" sort="Gehring, Kalle" uniqKey="Gehring K" first="Kalle" last="Gehring">Kalle Gehring</name><affiliation wicri:level="4"><nlm:affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada jeanfrancois.trempe@mcgill.ca kalle.gehring@mcgill.ca.</nlm:affiliation><country wicri:rule="url">Canada</country><wicri:regionArea>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC</wicri:regionArea><orgName type="university">Université McGill</orgName><placeName><settlement type="city">Montréal</settlement><region type="state">Québec</region></placeName></affiliation></author></analytic><series><title level="j">The EMBO journal</title><idno type="eISSN">1460-2075</idno><imprint><date when="2015" type="published">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Cloning, Molecular</term><term>Crystallization</term><term>Enzyme Activation (genetics)</term><term>Humans</term><term>Mitochondria (metabolism)</term><term>Models, Molecular</term><term>Mutagenesis</term><term>Nuclear Magnetic Resonance, Biomolecular</term><term>Phosphorylation</term><term>Protein Binding</term><term>Protein Conformation</term><term>Protein Kinases (chemistry)</term><term>Protein Kinases (metabolism)</term><term>Protein Structure, Tertiary</term><term>Scattering, Small Angle</term><term>Ubiquitin (metabolism)</term><term>Ubiquitin-Conjugating Enzymes (metabolism)</term><term>Ubiquitin-Protein Ligases (chemistry)</term><term>Ubiquitin-Protein Ligases (metabolism)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Protein Kinases</term><term>Ubiquitin-Protein Ligases</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Enzyme Activation</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Mitochondria</term><term>Protein Kinases</term><term>Ubiquitin</term><term>Ubiquitin-Conjugating Enzymes</term><term>Ubiquitin-Protein Ligases</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Cloning, Molecular</term><term>Crystallization</term><term>Humans</term><term>Models, Molecular</term><term>Mutagenesis</term><term>Nuclear Magnetic Resonance, Biomolecular</term><term>Phosphorylation</term><term>Protein Binding</term><term>Protein Conformation</term><term>Protein Structure, Tertiary</term><term>Scattering, Small Angle</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Mutations in Parkin and PINK1 cause an inherited early-onset form of Parkinson's disease. The two proteins function together in a mitochondrial quality control pathway whereby PINK1 accumulates on damaged mitochondria and activates Parkin to induce mitophagy. How PINK1 kinase activity releases the auto-inhibited ubiquitin ligase activity of Parkin remains unclear. Here, we identify a binding switch between phospho-ubiquitin (pUb) and the ubiquitin-like domain (Ubl) of Parkin as a key element. By mutagenesis and SAXS, we show that pUb binds to RING1 of Parkin at a site formed by His302 and Arg305. pUb binding promotes disengagement of the Ubl from RING1 and subsequent Parkin phosphorylation. A crystal structure of Parkin Δ86-130 at 2.54 Å resolution allowed the design of mutations that specifically release the Ubl domain from RING1. These mutations mimic pUb binding and promote Parkin phosphorylation. Measurements of the E2 ubiquitin-conjugating enzyme UbcH7 binding to Parkin and Parkin E3 ligase activity suggest that Parkin phosphorylation regulates E3 ligase activity downstream of pUb binding.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">26254305</PMID><DateCreated><Year>2015</Year><Month>10</Month><Day>15</Day></DateCreated><DateCompleted><Year>2016</Year><Month>02</Month><Day>02</Day></DateCompleted><DateRevised><Year>2017</Year><Month>02</Month><Day>20</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1460-2075</ISSN><JournalIssue CitedMedium="Internet"><Volume>34</Volume><Issue>20</Issue><PubDate><Year>2015</Year><Month>Oct</Month><Day>14</Day></PubDate></JournalIssue><Title>The EMBO journal</Title><ISOAbbreviation>EMBO J.</ISOAbbreviation></Journal><ArticleTitle>A Ubl/ubiquitin switch in the activation of Parkin.</ArticleTitle><Pagination><MedlinePgn>2492-505</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.15252/embj.201592237</ELocationID><Abstract><AbstractText>Mutations in Parkin and PINK1 cause an inherited early-onset form of Parkinson's disease. The two proteins function together in a mitochondrial quality control pathway whereby PINK1 accumulates on damaged mitochondria and activates Parkin to induce mitophagy. How PINK1 kinase activity releases the auto-inhibited ubiquitin ligase activity of Parkin remains unclear. Here, we identify a binding switch between phospho-ubiquitin (pUb) and the ubiquitin-like domain (Ubl) of Parkin as a key element. By mutagenesis and SAXS, we show that pUb binds to RING1 of Parkin at a site formed by His302 and Arg305. pUb binding promotes disengagement of the Ubl from RING1 and subsequent Parkin phosphorylation. A crystal structure of Parkin Δ86-130 at 2.54 Å resolution allowed the design of mutations that specifically release the Ubl domain from RING1. These mutations mimic pUb binding and promote Parkin phosphorylation. Measurements of the E2 ubiquitin-conjugating enzyme UbcH7 binding to Parkin and Parkin E3 ligase activity suggest that Parkin phosphorylation regulates E3 ligase activity downstream of pUb binding.</AbstractText><CopyrightInformation>© 2015 The Authors. Published under the terms of the CC BY 4.0 license.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Sauvé</LastName><ForeName>Véronique</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lilov</LastName><ForeName>Asparouh</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Seirafi</LastName><ForeName>Marjan</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vranas</LastName><ForeName>Marta</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Pharmacology and Therapeutics, McGill University, Montréal, QC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rasool</LastName><ForeName>Shafqat</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada Department of Pharmacology and Therapeutics, McGill University, Montréal, QC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kozlov</LastName><ForeName>Guennadi</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sprules</LastName><ForeName>Tara</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Quebec/Eastern Canada High Field NMR Facility (QANUC), Montréal, QC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Jimin</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Trempe</LastName><ForeName>Jean-François</ForeName><Initials>JF</Initials><AffiliationInfo><Affiliation>Department of Pharmacology and Therapeutics, McGill University, Montréal, QC, Canada jeanfrancois.trempe@mcgill.ca kalle.gehring@mcgill.ca.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gehring</LastName><ForeName>Kalle</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Groupe de recherché axé sur la structure des protéines and Department of Biochemistry, McGill University, Montréal, QC, Canada jeanfrancois.trempe@mcgill.ca kalle.gehring@mcgill.ca.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>MOP-125924</GrantID><Agency>Canadian Institutes of Health Research</Agency><Country>Canada</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2015</Year><Month>08</Month><Day>07</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>EMBO J</MedlineTA><NlmUniqueID>8208664</NlmUniqueID><ISSNLinking>0261-4189</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D025801">Ubiquitin</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.3.2.23</RegistryNumber><NameOfSubstance UI="C079437">UBE2L3 protein, human</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.3.2.23</RegistryNumber><NameOfSubstance UI="D044763">Ubiquitin-Conjugating Enzymes</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.3.2.27</RegistryNumber><NameOfSubstance UI="D044767">Ubiquitin-Protein Ligases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.3.2.27</RegistryNumber><NameOfSubstance UI="C111567">parkin protein</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.7.-</RegistryNumber><NameOfSubstance UI="D011494">Protein Kinases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.7.11.1</RegistryNumber><NameOfSubstance UI="C433927">PTEN-induced putative kinase</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>EMBO J. 2015 Oct 14;34(20):2486-8</RefSource><PMID 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MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008958" MajorTopicYN="Y">Models, Molecular</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D016296" MajorTopicYN="N">Mutagenesis</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D019906" MajorTopicYN="N">Nuclear Magnetic Resonance, Biomolecular</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010766" MajorTopicYN="N">Phosphorylation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D011485" MajorTopicYN="N">Protein Binding</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D011487" MajorTopicYN="N">Protein Conformation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D011494" MajorTopicYN="N">Protein Kinases</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D017434" MajorTopicYN="N">Protein Structure, Tertiary</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D053838" MajorTopicYN="N">Scattering, Small Angle</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D025801" MajorTopicYN="N">Ubiquitin</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D044763" MajorTopicYN="N">Ubiquitin-Conjugating Enzymes</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D044767" MajorTopicYN="N">Ubiquitin-Protein Ligases</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading></MeshHeadingList><OtherID Source="NLM">PMC4609182</OtherID><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Parkinson's disease</Keyword><Keyword MajorTopicYN="N">mitochondria</Keyword><Keyword MajorTopicYN="N">mitophagy</Keyword><Keyword MajorTopicYN="N">phosphorylation</Keyword><Keyword MajorTopicYN="N">ubiquitination</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2015</Year><Month>06</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2015</Year><Month>07</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2015</Year><Month>8</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2015</Year><Month>8</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2016</Year><Month>2</Month><Day>3</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">26254305</ArticleId><ArticleId IdType="pii">embj.201592237</ArticleId><ArticleId IdType="doi">10.15252/embj.201592237</ArticleId><ArticleId IdType="pmc">PMC4609182</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Canada</li><li>États-Unis</li></country><region><li>Connecticut</li><li>Québec</li></region><settlement><li>Montréal</li></settlement><orgName><li>Université McGill</li></orgName></list><tree><country name="Canada"><region name="Québec"><name sortKey="Sauve, Veronique" sort="Sauve, Veronique" uniqKey="Sauve V" first="Véronique" last="Sauvé">Véronique Sauvé</name></region><name sortKey="Gehring, Kalle" sort="Gehring, Kalle" uniqKey="Gehring K" first="Kalle" last="Gehring">Kalle Gehring</name><name sortKey="Kozlov, Guennadi" sort="Kozlov, Guennadi" uniqKey="Kozlov G" first="Guennadi" last="Kozlov">Guennadi Kozlov</name><name sortKey="Lilov, Asparouh" sort="Lilov, Asparouh" uniqKey="Lilov A" first="Asparouh" last="Lilov">Asparouh Lilov</name><name sortKey="Rasool, Shafqat" sort="Rasool, Shafqat" uniqKey="Rasool S" first="Shafqat" last="Rasool">Shafqat Rasool</name><name sortKey="Seirafi, Marjan" sort="Seirafi, Marjan" uniqKey="Seirafi M" first="Marjan" last="Seirafi">Marjan Seirafi</name><name sortKey="Sprules, Tara" sort="Sprules, Tara" uniqKey="Sprules T" first="Tara" last="Sprules">Tara Sprules</name><name sortKey="Trempe, Jean Francois" sort="Trempe, Jean Francois" uniqKey="Trempe J" first="Jean-François" last="Trempe">Jean-François Trempe</name><name sortKey="Vranas, Marta" sort="Vranas, Marta" uniqKey="Vranas M" first="Marta" last="Vranas">Marta Vranas</name></country><country name="États-Unis"><region name="Connecticut"><name sortKey="Wang, Jimin" sort="Wang, Jimin" uniqKey="Wang J" first="Jimin" last="Wang">Jimin Wang</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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