Mitochondrial Bol1 and Bol3 function as assembly factors for specific iron-sulfur proteins.
Identifieur interne : 000443 ( Main/Exploration ); précédent : 000442; suivant : 000444Mitochondrial Bol1 and Bol3 function as assembly factors for specific iron-sulfur proteins.
Auteurs : Marta A. Uzarska [Allemagne] ; Veronica Nasta [Italie] ; Benjamin D. Weiler [Allemagne] ; Farah Spantgar [Allemagne] ; Simone Ciofi-Baffoni [Italie] ; Maria Rosaria Saviello [Italie] ; Leonardo Gonnelli [Italie] ; Ulrich Mühlenhoff [Allemagne] ; Lucia Banci [Italie] ; Roland Lill [Allemagne]Source :
- eLife [ 2050-084X ] ; 2016.
Descripteurs français
- KwdFr :
- MESH :
English descriptors
- KwdEn :
- MESH :
- chemical , metabolism : Glutaredoxins, Iron-Sulfur Proteins, Mitochondrial Proteins, Saccharomyces cerevisiae Proteins.
- metabolism : Mitochondria, Saccharomyces cerevisiae.
- Protein Multimerization.
Abstract
Assembly of mitochondrial iron-sulfur (Fe/S) proteins is a key process of cells, and defects cause many rare diseases. In the first phase of this pathway, ten Fe/S cluster (ISC) assembly components synthesize and insert [2Fe-2S] clusters. The second phase is dedicated to the assembly of [4Fe-4S] proteins, yet this part is poorly understood. Here, we characterize the BOLA family proteins Bol1 and Bol3 as specific mitochondrial ISC assembly factors that facilitate [4Fe-4S] cluster insertion into a subset of mitochondrial proteins such as lipoate synthase and succinate dehydrogenase. Bol1-Bol3 perform largely overlapping functions, yet cannot replace the ISC protein Nfu1 that also participates in this phase of Fe/S protein biogenesis. Bol1 and Bol3 form dimeric complexes with both monothiol glutaredoxin Grx5 and Nfu1. Complex formation differentially influences the stability of the Grx5-Bol-shared Fe/S clusters. Our findings provide the biochemical basis for explaining the pathological phenotypes of patients with mutations in BOLA3.
DOI: 10.7554/eLife.16673
PubMed: 27532772
PubMed Central: PMC5014550
Affiliations:
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xml:lang="en">Mitochondrial Bol1 and Bol3 function as assembly factors for specific iron-sulfur proteins.</title><author><name sortKey="Uzarska, Marta A" sort="Uzarska, Marta A" uniqKey="Uzarska M" first="Marta A" last="Uzarska">Marta A. Uzarska</name><affiliation wicri:level="3"><nlm:affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg</wicri:regionArea><placeName><region type="land" nuts="1">Hesse (Land)</region><region type="district" nuts="2">District de Giessen</region><settlement type="city">Marbourg</settlement></placeName></affiliation></author><author><name sortKey="Nasta, Veronica" sort="Nasta, Veronica" uniqKey="Nasta V" first="Veronica" last="Nasta">Veronica Nasta</name><affiliation wicri:level="1"><nlm:affiliation>Magnetic Resonance Center CERM, University of Florence, Florence, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Magnetic Resonance Center CERM, University of Florence, Florence</wicri:regionArea><wicri:noRegion>Florence</wicri:noRegion></affiliation></author><author><name sortKey="Weiler, Benjamin D" sort="Weiler, Benjamin D" uniqKey="Weiler B" first="Benjamin D" last="Weiler">Benjamin D. Weiler</name><affiliation wicri:level="3"><nlm:affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg</wicri:regionArea><placeName><region type="land" nuts="1">Hesse (Land)</region><region type="district" nuts="2">District de Giessen</region><settlement type="city">Marbourg</settlement></placeName></affiliation></author><author><name sortKey="Spantgar, Farah" sort="Spantgar, Farah" uniqKey="Spantgar F" first="Farah" last="Spantgar">Farah Spantgar</name><affiliation wicri:level="3"><nlm:affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg</wicri:regionArea><placeName><region type="land" nuts="1">Hesse (Land)</region><region type="district" nuts="2">District de Giessen</region><settlement type="city">Marbourg</settlement></placeName></affiliation></author><author><name sortKey="Ciofi Baffoni, Simone" sort="Ciofi Baffoni, Simone" uniqKey="Ciofi Baffoni S" first="Simone" last="Ciofi-Baffoni">Simone Ciofi-Baffoni</name><affiliation wicri:level="1"><nlm:affiliation>Magnetic Resonance Center CERM, University of Florence, Florence, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Magnetic Resonance Center CERM, University of Florence, Florence</wicri:regionArea><wicri:noRegion>Florence</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, University of Florence, Florence, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, University of Florence, Florence</wicri:regionArea><wicri:noRegion>Florence</wicri:noRegion></affiliation></author><author><name sortKey="Saviello, Maria Rosaria" sort="Saviello, Maria Rosaria" uniqKey="Saviello M" first="Maria Rosaria" last="Saviello">Maria Rosaria Saviello</name><affiliation wicri:level="1"><nlm:affiliation>Magnetic Resonance Center CERM, University of Florence, Florence, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Magnetic Resonance Center CERM, University of Florence, Florence</wicri:regionArea><wicri:noRegion>Florence</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, University of Florence, Florence, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, University of Florence, Florence</wicri:regionArea><wicri:noRegion>Florence</wicri:noRegion></affiliation></author><author><name sortKey="Gonnelli, Leonardo" sort="Gonnelli, Leonardo" uniqKey="Gonnelli L" first="Leonardo" last="Gonnelli">Leonardo Gonnelli</name><affiliation wicri:level="1"><nlm:affiliation>Magnetic Resonance Center CERM, University of Florence, Florence, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Magnetic Resonance Center CERM, University of Florence, Florence</wicri:regionArea><wicri:noRegion>Florence</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, University of Florence, Florence, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, University of Florence, Florence</wicri:regionArea><wicri:noRegion>Florence</wicri:noRegion></affiliation></author><author><name sortKey="Muhlenhoff, Ulrich" sort="Muhlenhoff, Ulrich" uniqKey="Muhlenhoff U" first="Ulrich" last="Mühlenhoff">Ulrich Mühlenhoff</name><affiliation wicri:level="3"><nlm:affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg</wicri:regionArea><placeName><region type="land" nuts="1">Hesse (Land)</region><region type="district" nuts="2">District de Giessen</region><settlement type="city">Marbourg</settlement></placeName></affiliation></author><author><name sortKey="Banci, Lucia" sort="Banci, Lucia" uniqKey="Banci L" first="Lucia" last="Banci">Lucia Banci</name><affiliation wicri:level="1"><nlm:affiliation>Magnetic Resonance Center CERM, University of Florence, Florence, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Magnetic Resonance Center CERM, University of Florence, Florence</wicri:regionArea><wicri:noRegion>Florence</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, University of Florence, Florence, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, University of Florence, Florence</wicri:regionArea><wicri:noRegion>Florence</wicri:noRegion></affiliation></author><author><name sortKey="Lill, Roland" sort="Lill, Roland" uniqKey="Lill R" first="Roland" last="Lill">Roland Lill</name><affiliation wicri:level="3"><nlm:affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg</wicri:regionArea><placeName><region type="land" nuts="1">Hesse (Land)</region><region type="district" nuts="2">District de Giessen</region><settlement type="city">Marbourg</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>LOEWE Zentrum für Synthetische Mikrobiologie SynMikro, Marburg, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>LOEWE Zentrum für Synthetische Mikrobiologie SynMikro, Marburg</wicri:regionArea><placeName><region type="land" nuts="1">Hesse (Land)</region><region type="district" nuts="2">District de Giessen</region><settlement type="city">Marbourg</settlement></placeName></affiliation></author></analytic><series><title level="j">eLife</title><idno type="eISSN">2050-084X</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Glutaredoxins (metabolism)</term><term>Iron-Sulfur Proteins (metabolism)</term><term>Mitochondria (metabolism)</term><term>Mitochondrial Proteins (metabolism)</term><term>Protein Multimerization (MeSH)</term><term>Saccharomyces cerevisiae (metabolism)</term><term>Saccharomyces cerevisiae Proteins (metabolism)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Ferrosulfoprotéines (métabolisme)</term><term>Glutarédoxines (métabolisme)</term><term>Mitochondries (métabolisme)</term><term>Multimérisation de protéines (MeSH)</term><term>Protéines de Saccharomyces cerevisiae (métabolisme)</term><term>Protéines mitochondriales (métabolisme)</term><term>Saccharomyces cerevisiae (métabolisme)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Glutaredoxins</term><term>Iron-Sulfur Proteins</term><term>Mitochondrial Proteins</term><term>Saccharomyces cerevisiae Proteins</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Mitochondria</term><term>Saccharomyces cerevisiae</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Ferrosulfoprotéines</term><term>Glutarédoxines</term><term>Mitochondries</term><term>Protéines de Saccharomyces cerevisiae</term><term>Protéines mitochondriales</term><term>Saccharomyces cerevisiae</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Protein Multimerization</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Multimérisation de protéines</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Assembly of mitochondrial iron-sulfur (Fe/S) proteins is a key process of cells, and defects cause many rare diseases. In the first phase of this pathway, ten Fe/S cluster (ISC) assembly components synthesize and insert [2Fe-2S] clusters. The second phase is dedicated to the assembly of [4Fe-4S] proteins, yet this part is poorly understood. Here, we characterize the BOLA family proteins Bol1 and Bol3 as specific mitochondrial ISC assembly factors that facilitate [4Fe-4S] cluster insertion into a subset of mitochondrial proteins such as lipoate synthase and succinate dehydrogenase. Bol1-Bol3 perform largely overlapping functions, yet cannot replace the ISC protein Nfu1 that also participates in this phase of Fe/S protein biogenesis. Bol1 and Bol3 form dimeric complexes with both monothiol glutaredoxin Grx5 and Nfu1. Complex formation differentially influences the stability of the Grx5-Bol-shared Fe/S clusters. Our findings provide the biochemical basis for explaining the pathological phenotypes of patients with mutations in BOLA3.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">27532772</PMID><DateCompleted><Year>2017</Year><Month>10</Month><Day>30</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2050-084X</ISSN><JournalIssue CitedMedium="Internet"><Volume>5</Volume><PubDate><Year>2016</Year><Month>08</Month><Day>17</Day></PubDate></JournalIssue><Title>eLife</Title><ISOAbbreviation>Elife</ISOAbbreviation></Journal><ArticleTitle>Mitochondrial Bol1 and Bol3 function as assembly factors for specific iron-sulfur proteins.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.7554/eLife.16673</ELocationID><ELocationID EIdType="pii" ValidYN="Y">e16673</ELocationID><Abstract><AbstractText>Assembly of mitochondrial iron-sulfur (Fe/S) proteins is a key process of cells, and defects cause many rare diseases. In the first phase of this pathway, ten Fe/S cluster (ISC) assembly components synthesize and insert [2Fe-2S] clusters. The second phase is dedicated to the assembly of [4Fe-4S] proteins, yet this part is poorly understood. Here, we characterize the BOLA family proteins Bol1 and Bol3 as specific mitochondrial ISC assembly factors that facilitate [4Fe-4S] cluster insertion into a subset of mitochondrial proteins such as lipoate synthase and succinate dehydrogenase. Bol1-Bol3 perform largely overlapping functions, yet cannot replace the ISC protein Nfu1 that also participates in this phase of Fe/S protein biogenesis. Bol1 and Bol3 form dimeric complexes with both monothiol glutaredoxin Grx5 and Nfu1. Complex formation differentially influences the stability of the Grx5-Bol-shared Fe/S clusters. Our findings provide the biochemical basis for explaining the pathological phenotypes of patients with mutations in BOLA3.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Uzarska</LastName><ForeName>Marta A</ForeName><Initials>MA</Initials><AffiliationInfo><Affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nasta</LastName><ForeName>Veronica</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>Magnetic Resonance Center CERM, University of Florence, Florence, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Weiler</LastName><ForeName>Benjamin D</ForeName><Initials>BD</Initials><AffiliationInfo><Affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Spantgar</LastName><ForeName>Farah</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ciofi-Baffoni</LastName><ForeName>Simone</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Magnetic Resonance Center CERM, University of Florence, Florence, Italy.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Chemistry, University of Florence, Florence, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Saviello</LastName><ForeName>Maria Rosaria</ForeName><Initials>MR</Initials><AffiliationInfo><Affiliation>Magnetic Resonance Center CERM, University of Florence, Florence, Italy.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Chemistry, University of Florence, Florence, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gonnelli</LastName><ForeName>Leonardo</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Magnetic Resonance Center CERM, University of Florence, Florence, Italy.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Chemistry, University of Florence, Florence, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mühlenhoff</LastName><ForeName>Ulrich</ForeName><Initials>U</Initials><AffiliationInfo><Affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Banci</LastName><ForeName>Lucia</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Magnetic Resonance Center CERM, University of Florence, Florence, Italy.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Chemistry, University of Florence, Florence, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lill</LastName><ForeName>Roland</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0002-8345-6518</Identifier><AffiliationInfo><Affiliation>Institut für Zytobiologie und Zytopathologie, Philipps-Universität, Marburg, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>LOEWE Zentrum für Synthetische Mikrobiologie SynMikro, Marburg, Germany.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>08</Month><Day>17</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Elife</MedlineTA><NlmUniqueID>101579614</NlmUniqueID><ISSNLinking>2050-084X</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D054477">Glutaredoxins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C528773">Grx5 protein, S cerevisiae</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D007506">Iron-Sulfur Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D024101">Mitochondrial Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C121524">NFU1 protein, S cerevisiae</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D029701">Saccharomyces cerevisiae Proteins</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D054477" MajorTopicYN="N">Glutaredoxins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D007506" MajorTopicYN="N">Iron-Sulfur Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008928" MajorTopicYN="N">Mitochondria</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D024101" MajorTopicYN="N">Mitochondrial Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D055503" MajorTopicYN="N">Protein Multimerization</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D012441" MajorTopicYN="N">Saccharomyces cerevisiae</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D029701" MajorTopicYN="N">Saccharomyces cerevisiae Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">ISC machinery</Keyword><Keyword MajorTopicYN="Y">S. cerevisiae</Keyword><Keyword MajorTopicYN="Y">biochemistry</Keyword><Keyword MajorTopicYN="Y">cancer biology</Keyword><Keyword MajorTopicYN="Y">human</Keyword><Keyword MajorTopicYN="Y">lipoic acid</Keyword><Keyword MajorTopicYN="Y">metal biology</Keyword><Keyword MajorTopicYN="Y">post-translational modification</Keyword><Keyword MajorTopicYN="Y">respiratory chain</Keyword></KeywordList><CoiStatement>The authors declare that no competing interests exist.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2016</Year><Month>04</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2016</Year><Month>08</Month><Day>08</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2016</Year><Month>8</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2016</Year><Month>8</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2017</Year><Month>10</Month><Day>31</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">27532772</ArticleId><ArticleId IdType="doi">10.7554/eLife.16673</ArticleId><ArticleId IdType="pmc">PMC5014550</ArticleId></ArticleIdList><ReferenceList><Reference><Citation>Elife. 2016 Aug 17;5:null</Citation><ArticleIdList><ArticleId IdType="pubmed">27532773</ArticleId></ArticleIdList></Reference><Reference><Citation>J Biol Chem. 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