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Panorama of ancient metazoan macromolecular complexes.

Identifieur interne : 000415 ( PubMed/Corpus ); précédent : 000414; suivant : 000416

Panorama of ancient metazoan macromolecular complexes.

Auteurs : Cuihong Wan ; Blake Borgeson ; Sadhna Phanse ; Fan Tu ; Kevin Drew ; Greg Clark ; Xuejian Xiong ; Olga Kagan ; Julian Kwan ; Alexandr Bezginov ; Kyle Chessman ; Swati Pal ; Graham Cromar ; Ophelia Papoulas ; Zuyao Ni ; Daniel R. Boutz ; Snejana Stoilova ; Pierre C. Havugimana ; Xinghua Guo ; Ramy H. Malty ; Mihail Sarov ; Jack Greenblatt ; Mohan Babu ; W Brent Derry ; Elisabeth R. Tillier ; John B. Wallingford ; John Parkinson ; Edward M. Marcotte ; Andrew Emili

Source :

RBID : pubmed:26344197

English descriptors

Abstract

Macromolecular complexes are essential to conserved biological processes, but their prevalence across animals is unclear. By combining extensive biochemical fractionation with quantitative mass spectrometry, here we directly examined the composition of soluble multiprotein complexes among diverse metazoan models. Using an integrative approach, we generated a draft conservation map consisting of more than one million putative high-confidence co-complex interactions for species with fully sequenced genomes that encompasses functional modules present broadly across all extant animals. Clustering reveals a spectrum of conservation, ranging from ancient eukaryotic assemblies that have probably served cellular housekeeping roles for at least one billion years, ancestral complexes that have accrued contemporary components, and rarer metazoan innovations linked to multicellularity. We validated these projections by independent co-fractionation experiments in evolutionarily distant species, affinity purification and functional analyses. The comprehensiveness, centrality and modularity of these reconstructed interactomes reflect their fundamental mechanistic importance and adaptive value to animal cell systems.

DOI: 10.1038/nature14877
PubMed: 26344197

Links to Exploration step

pubmed:26344197

Le document en format XML

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<name sortKey="Papoulas, Ophelia" sort="Papoulas, Ophelia" uniqKey="Papoulas O" first="Ophelia" last="Papoulas">Ophelia Papoulas</name>
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<name sortKey="Pal, Swati" sort="Pal, Swati" uniqKey="Pal S" first="Swati" last="Pal">Swati Pal</name>
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<name sortKey="Papoulas, Ophelia" sort="Papoulas, Ophelia" uniqKey="Papoulas O" first="Ophelia" last="Papoulas">Ophelia Papoulas</name>
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<name sortKey="Ni, Zuyao" sort="Ni, Zuyao" uniqKey="Ni Z" first="Zuyao" last="Ni">Zuyao Ni</name>
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<name sortKey="Guo, Xinghua" sort="Guo, Xinghua" uniqKey="Guo X" first="Xinghua" last="Guo">Xinghua Guo</name>
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<name sortKey="Malty, Ramy H" sort="Malty, Ramy H" uniqKey="Malty R" first="Ramy H" last="Malty">Ramy H. Malty</name>
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<nlm:affiliation>Department of Biochemistry, University of Regina, Regina, Saskatchewan S4S 0A2, Canada.</nlm:affiliation>
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<name sortKey="Sarov, Mihail" sort="Sarov, Mihail" uniqKey="Sarov M" first="Mihail" last="Sarov">Mihail Sarov</name>
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<name sortKey="Tillier, Elisabeth R" sort="Tillier, Elisabeth R" uniqKey="Tillier E" first="Elisabeth R" last="Tillier">Elisabeth R. Tillier</name>
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<term>Multiprotein Complexes (metabolism)</term>
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<div type="abstract" xml:lang="en">Macromolecular complexes are essential to conserved biological processes, but their prevalence across animals is unclear. By combining extensive biochemical fractionation with quantitative mass spectrometry, here we directly examined the composition of soluble multiprotein complexes among diverse metazoan models. Using an integrative approach, we generated a draft conservation map consisting of more than one million putative high-confidence co-complex interactions for species with fully sequenced genomes that encompasses functional modules present broadly across all extant animals. Clustering reveals a spectrum of conservation, ranging from ancient eukaryotic assemblies that have probably served cellular housekeeping roles for at least one billion years, ancestral complexes that have accrued contemporary components, and rarer metazoan innovations linked to multicellularity. We validated these projections by independent co-fractionation experiments in evolutionarily distant species, affinity purification and functional analyses. The comprehensiveness, centrality and modularity of these reconstructed interactomes reflect their fundamental mechanistic importance and adaptive value to animal cell systems.</div>
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</PubDate>
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<Title>Nature</Title>
<ISOAbbreviation>Nature</ISOAbbreviation>
</Journal>
<ArticleTitle>Panorama of ancient metazoan macromolecular complexes.</ArticleTitle>
<Pagination>
<MedlinePgn>339-44</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1038/nature14877</ELocationID>
<Abstract>
<AbstractText>Macromolecular complexes are essential to conserved biological processes, but their prevalence across animals is unclear. By combining extensive biochemical fractionation with quantitative mass spectrometry, here we directly examined the composition of soluble multiprotein complexes among diverse metazoan models. Using an integrative approach, we generated a draft conservation map consisting of more than one million putative high-confidence co-complex interactions for species with fully sequenced genomes that encompasses functional modules present broadly across all extant animals. Clustering reveals a spectrum of conservation, ranging from ancient eukaryotic assemblies that have probably served cellular housekeeping roles for at least one billion years, ancestral complexes that have accrued contemporary components, and rarer metazoan innovations linked to multicellularity. We validated these projections by independent co-fractionation experiments in evolutionarily distant species, affinity purification and functional analyses. The comprehensiveness, centrality and modularity of these reconstructed interactomes reflect their fundamental mechanistic importance and adaptive value to animal cell systems.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Wan</LastName>
<ForeName>Cuihong</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S 3E1, Canada.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Center for Systems and Synthetic Biology, Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, Texas 78712, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Borgeson</LastName>
<ForeName>Blake</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>Center for Systems and Synthetic Biology, Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, Texas 78712, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Phanse</LastName>
<ForeName>Sadhna</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S 3E1, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tu</LastName>
<ForeName>Fan</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Center for Systems and Synthetic Biology, Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, Texas 78712, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Drew</LastName>
<ForeName>Kevin</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>Center for Systems and Synthetic Biology, Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, Texas 78712, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Clark</LastName>
<ForeName>Greg</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>Department of Medical Biophysics, Toronto, Ontario M5G 1L7, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Xiong</LastName>
<ForeName>Xuejian</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kagan</LastName>
<ForeName>Olga</ForeName>
<Initials>O</Initials>
<AffiliationInfo>
<Affiliation>Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S 3E1, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kwan</LastName>
<ForeName>Julian</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S 3E1, Canada.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bezginov</LastName>
<ForeName>Alexandr</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Department of Medical Biophysics, Toronto, Ontario M5G 1L7, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chessman</LastName>
<ForeName>Kyle</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Pal</LastName>
<ForeName>Swati</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Cromar</LastName>
<ForeName>Graham</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Papoulas</LastName>
<ForeName>Ophelia</ForeName>
<Initials>O</Initials>
<AffiliationInfo>
<Affiliation>Center for Systems and Synthetic Biology, Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, Texas 78712, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ni</LastName>
<ForeName>Zuyao</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S 3E1, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Boutz</LastName>
<ForeName>Daniel R</ForeName>
<Initials>DR</Initials>
<AffiliationInfo>
<Affiliation>Center for Systems and Synthetic Biology, Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, Texas 78712, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Stoilova</LastName>
<ForeName>Snejana</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S 3E1, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Havugimana</LastName>
<ForeName>Pierre C</ForeName>
<Initials>PC</Initials>
<AffiliationInfo>
<Affiliation>Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S 3E1, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Guo</LastName>
<ForeName>Xinghua</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S 3E1, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Malty</LastName>
<ForeName>Ramy H</ForeName>
<Initials>RH</Initials>
<AffiliationInfo>
<Affiliation>Department of Biochemistry, University of Regina, Regina, Saskatchewan S4S 0A2, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sarov</LastName>
<ForeName>Mihail</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Greenblatt</LastName>
<ForeName>Jack</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S 3E1, Canada.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Babu</LastName>
<ForeName>Mohan</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Department of Biochemistry, University of Regina, Regina, Saskatchewan S4S 0A2, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Derry</LastName>
<ForeName>W Brent</ForeName>
<Initials>WB</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tillier</LastName>
<ForeName>Elisabeth R</ForeName>
<Initials>ER</Initials>
<AffiliationInfo>
<Affiliation>Department of Medical Biophysics, Toronto, Ontario M5G 1L7, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wallingford</LastName>
<ForeName>John B</ForeName>
<Initials>JB</Initials>
<AffiliationInfo>
<Affiliation>Center for Systems and Synthetic Biology, Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, Texas 78712, USA.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Molecular Biosciences, University of Texas at Austin, Austin, Texas 78712, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Parkinson</LastName>
<ForeName>John</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Marcotte</LastName>
<ForeName>Edward M</ForeName>
<Initials>EM</Initials>
<AffiliationInfo>
<Affiliation>Center for Systems and Synthetic Biology, Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, Texas 78712, USA.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Molecular Biosciences, University of Texas at Austin, Austin, Texas 78712, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Emili</LastName>
<ForeName>Andrew</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, Ontario M5S 3E1, Canada.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>F32GM112495</GrantID>
<Acronym>GM</Acronym>
<Agency>NIGMS NIH HHS</Agency>
<Country>United States</Country>
</Grant>
<Grant>
<GrantID>R01 GM076536</GrantID>
<Acronym>GM</Acronym>
<Agency>NIGMS NIH HHS</Agency>
<Country>United States</Country>
</Grant>
<Grant>
<GrantID>DP1 GM106408</GrantID>
<Acronym>GM</Acronym>
<Agency>NIGMS NIH HHS</Agency>
<Country>United States</Country>
</Grant>
<Grant>
<GrantID>R01 GM067779</GrantID>
<Acronym>GM</Acronym>
<Agency>NIGMS NIH HHS</Agency>
<Country>United States</Country>
</Grant>
<Grant>
<Agency>Canadian Institutes of Health Research</Agency>
<Country>Canada</Country>
</Grant>
<Grant>
<GrantID>F32 GM112495</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>
<PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2015</Year>
<Month>09</Month>
<Day>07</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>Nature</MedlineTA>
<NlmUniqueID>0410462</NlmUniqueID>
<ISSNLinking>0028-0836</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D046912">Multiprotein Complexes</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
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<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D066264" MajorTopicYN="N">Datasets as Topic</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D019143" MajorTopicYN="Y">Evolution, Molecular</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D046912" MajorTopicYN="N">Multiprotein Complexes</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D025941" MajorTopicYN="N">Protein Interaction Mapping</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060066" MajorTopicYN="Y">Protein Interaction Maps</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015203" MajorTopicYN="N">Reproducibility of Results</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D049490" MajorTopicYN="N">Systems Biology</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D053719" MajorTopicYN="N">Tandem Mass Spectrometry</DescriptorName>
</MeshHeading>
</MeshHeadingList>
<OtherID Source="NLM">NIHMS704400</OtherID>
<OtherID Source="NLM">PMC5036527</OtherID>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2014</Year>
<Month>12</Month>
<Day>15</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2015</Year>
<Month>06</Month>
<Day>30</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2015</Year>
<Month>9</Month>
<Day>8</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="pubmed">
<Year>2015</Year>
<Month>9</Month>
<Day>8</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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