Defective mitochondrial ISCs biogenesis switches on IRP1 to fine tune selective mitophagy.
Identifieur interne : 000148 ( Main/Exploration ); précédent : 000147; suivant : 000149Defective mitochondrial ISCs biogenesis switches on IRP1 to fine tune selective mitophagy.
Auteurs : Hao Wu [République populaire de Chine] ; Huifang Wei [République populaire de Chine] ; Di Zhang [République populaire de Chine] ; Sheikh Arslan Sehgal [Pakistan] ; Dejiu Zhang [République populaire de Chine] ; Xiaohui Wang [République populaire de Chine] ; Yan Qin [République populaire de Chine] ; Lei Liu [République populaire de Chine] ; Quan Chen [République populaire de Chine]Source :
- Redox biology [ 2213-2317 ] ; 2020.
Abstract
Both iron metabolism and mitophagy, a selective mitochondrial degradation process via autolysosomal pathway, are fundamental for the cellular well-being. Mitochondria are the major site for iron metabolism, especially the biogenesis of iron-sulfur clusters (ISCs) via the mitochondria-localized ISCs assembly machinery. Here we report that mitochondrial ISCs biogenesis is coupled with receptor-mediated mitophagy in mammalian cells. Perturbation of mitochondrial ISCs biogenesis, either by depleting iron with the iron chelator or by knocking down the core components of the mitochondrial ISCs assembly machinery, triggers FUNDC1-dependent mitophagy. IRP1, one of the cellular iron sensors to maintain iron homeostasis, is crucial for iron stresses induced mitophagy. Knockdown of IRP1 disturbed iron stresses induced mitophagy. Furthermore, IRP1 could bind to a newly characterized IRE in the 5' untranslated region of the Bcl-xL mRNA and suppress its translation. Bcl-xL is an intrinsic inhibitory protein of the mitochondrial phosphatase PGAM5, which catalyzes the dephosphorylation of FUNDC1 for mitophagy activation. Alterations of the IRP1/Bcl-xL axis navigate iron stresses induced mitophagy. We conclude that ISCs serve as physiological signals for mitophagy activation, thus coupling mitophagy with iron metabolism.
DOI: 10.1016/j.redox.2020.101661
PubMed: 32795936
PubMed Central: PMC7426581
Affiliations:
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Electronic address: whao.1988@mail.hzau.edu.cn.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, 430070, China; State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101</wicri:regionArea><wicri:noRegion>100101</wicri:noRegion></affiliation></author><author><name sortKey="Wei, Huifang" sort="Wei, Huifang" uniqKey="Wei H" first="Huifang" last="Wei">Huifang Wei</name><affiliation wicri:level="1"><nlm:affiliation>China-US (Henan) Hormel Cancer Institute, Zhengzhou, 450003, China; Department of Pathophysiology, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, 450001, Henan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>China-US (Henan) Hormel Cancer Institute, Zhengzhou, 450003, China; Department of Pathophysiology, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, 450001, Henan</wicri:regionArea><wicri:noRegion>Henan</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Di" sort="Zhang, Di" uniqKey="Zhang D" first="Di" last="Zhang">Di Zhang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China; University of Chinese Academy of Sciences, Beijing, 100101, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China; University of Chinese Academy of Sciences, Beijing, 100101</wicri:regionArea><wicri:noRegion>100101</wicri:noRegion></affiliation></author><author><name sortKey="Sehgal, Sheikh Arslan" sort="Sehgal, Sheikh Arslan" uniqKey="Sehgal S" first="Sheikh Arslan" last="Sehgal">Sheikh Arslan Sehgal</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China; University of Chinese Academy of Sciences, Beijing, 100101, China; COMSATS University, Islamabad, Sahiwal Campus, Pakistan.</nlm:affiliation><country xml:lang="fr">Pakistan</country><wicri:regionArea>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China; University of Chinese Academy of Sciences, Beijing, 100101, China; COMSATS University, Islamabad, Sahiwal Campus</wicri:regionArea><wicri:noRegion>Sahiwal Campus</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Dejiu" sort="Zhang, Dejiu" uniqKey="Zhang D" first="Dejiu" last="Zhang">Dejiu Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101</wicri:regionArea><wicri:noRegion>100101</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Xiaohui" sort="Wang, Xiaohui" uniqKey="Wang X" first="Xiaohui" last="Wang">Xiaohui Wang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101</wicri:regionArea><wicri:noRegion>100101</wicri:noRegion></affiliation></author><author><name sortKey="Qin, Yan" sort="Qin, Yan" uniqKey="Qin Y" first="Yan" last="Qin">Yan Qin</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101</wicri:regionArea><wicri:noRegion>100101</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Lei" sort="Liu, Lei" uniqKey="Liu L" first="Lei" last="Liu">Lei Liu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China. Electronic address: liulei@ioz.ac.cn.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101</wicri:regionArea><wicri:noRegion>100101</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Quan" sort="Chen, Quan" uniqKey="Chen Q" first="Quan" last="Chen">Quan Chen</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China; University of Chinese Academy of Sciences, Beijing, 100101, China; Tianjin Key Laboratory of Protein Science, College of Life Sciences, Nankai University, Tianjin, 300071, China. Electronic address: chenq@ioz.ac.cn.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China; University of Chinese Academy of Sciences, Beijing, 100101, China; Tianjin Key Laboratory of Protein Science, College of Life Sciences, Nankai University, Tianjin, 300071</wicri:regionArea><wicri:noRegion>300071</wicri:noRegion></affiliation></author></analytic><series><title level="j">Redox biology</title><idno type="eISSN">2213-2317</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Both iron metabolism and mitophagy, a selective mitochondrial degradation process via autolysosomal pathway, are fundamental for the cellular well-being. Mitochondria are the major site for iron metabolism, especially the biogenesis of iron-sulfur clusters (ISCs) via the mitochondria-localized ISCs assembly machinery. Here we report that mitochondrial ISCs biogenesis is coupled with receptor-mediated mitophagy in mammalian cells. Perturbation of mitochondrial ISCs biogenesis, either by depleting iron with the iron chelator or by knocking down the core components of the mitochondrial ISCs assembly machinery, triggers FUNDC1-dependent mitophagy. IRP1, one of the cellular iron sensors to maintain iron homeostasis, is crucial for iron stresses induced mitophagy. Knockdown of IRP1 disturbed iron stresses induced mitophagy. Furthermore, IRP1 could bind to a newly characterized IRE in the 5' untranslated region of the Bcl-xL mRNA and suppress its translation. Bcl-xL is an intrinsic inhibitory protein of the mitochondrial phosphatase PGAM5, which catalyzes the dephosphorylation of FUNDC1 for mitophagy activation. Alterations of the IRP1/Bcl-xL axis navigate iron stresses induced mitophagy. We conclude that ISCs serve as physiological signals for mitophagy activation, thus coupling mitophagy with iron metabolism.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">32795936</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>14</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">2213-2317</ISSN><JournalIssue CitedMedium="Internet"><Volume>36</Volume><PubDate><Year>2020</Year><Month>Sep</Month></PubDate></JournalIssue><Title>Redox biology</Title><ISOAbbreviation>Redox Biol</ISOAbbreviation></Journal><ArticleTitle>Defective mitochondrial ISCs biogenesis switches on IRP1 to fine tune selective mitophagy.</ArticleTitle><Pagination><MedlinePgn>101661</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S2213-2317(20)30866-1</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.redox.2020.101661</ELocationID><Abstract><AbstractText>Both iron metabolism and mitophagy, a selective mitochondrial degradation process via autolysosomal pathway, are fundamental for the cellular well-being. Mitochondria are the major site for iron metabolism, especially the biogenesis of iron-sulfur clusters (ISCs) via the mitochondria-localized ISCs assembly machinery. Here we report that mitochondrial ISCs biogenesis is coupled with receptor-mediated mitophagy in mammalian cells. Perturbation of mitochondrial ISCs biogenesis, either by depleting iron with the iron chelator or by knocking down the core components of the mitochondrial ISCs assembly machinery, triggers FUNDC1-dependent mitophagy. IRP1, one of the cellular iron sensors to maintain iron homeostasis, is crucial for iron stresses induced mitophagy. Knockdown of IRP1 disturbed iron stresses induced mitophagy. Furthermore, IRP1 could bind to a newly characterized IRE in the 5' untranslated region of the Bcl-xL mRNA and suppress its translation. Bcl-xL is an intrinsic inhibitory protein of the mitochondrial phosphatase PGAM5, which catalyzes the dephosphorylation of FUNDC1 for mitophagy activation. Alterations of the IRP1/Bcl-xL axis navigate iron stresses induced mitophagy. We conclude that ISCs serve as physiological signals for mitophagy activation, thus coupling mitophagy with iron metabolism.</AbstractText><CopyrightInformation>Copyright © 2020 The Authors. Published by Elsevier B.V. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wu</LastName><ForeName>Hao</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, 430070, China; State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China. Electronic address: whao.1988@mail.hzau.edu.cn.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wei</LastName><ForeName>Huifang</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>China-US (Henan) Hormel Cancer Institute, Zhengzhou, 450003, China; Department of Pathophysiology, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, 450001, Henan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Di</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China; University of Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sehgal</LastName><ForeName>Sheikh Arslan</ForeName><Initials>SA</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China; University of Chinese Academy of Sciences, Beijing, 100101, China; COMSATS University, Islamabad, Sahiwal Campus, Pakistan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Dejiu</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Xiaohui</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Qin</LastName><ForeName>Yan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Key Laboratory of RNA Biology, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Lei</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China. Electronic address: liulei@ioz.ac.cn.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Quan</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China; University of Chinese Academy of Sciences, Beijing, 100101, China; Tianjin Key Laboratory of Protein Science, College of Life Sciences, Nankai University, Tianjin, 300071, China. Electronic address: chenq@ioz.ac.cn.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>07</Month><Day>27</Day></ArticleDate></Article><MedlineJournalInfo><Country>Netherlands</Country><MedlineTA>Redox Biol</MedlineTA><NlmUniqueID>101605639</NlmUniqueID><ISSNLinking>2213-2317</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Bcl-xL</Keyword><Keyword MajorTopicYN="N">FUNDC1</Keyword><Keyword MajorTopicYN="N">ISCs</Keyword><Keyword MajorTopicYN="N">Mitophagy</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>05</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>07</Month><Day>21</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>07</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>8</Month><Day>17</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>8</Month><Day>17</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>8</Month><Day>16</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32795936</ArticleId><ArticleId IdType="pii">S2213-2317(20)30866-1</ArticleId><ArticleId IdType="doi">10.1016/j.redox.2020.101661</ArticleId><ArticleId IdType="pmc">PMC7426581</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Pakistan</li><li>République populaire de Chine</li></country></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Wu, Hao" sort="Wu, Hao" uniqKey="Wu H" first="Hao" last="Wu">Hao Wu</name></noRegion><name sortKey="Chen, Quan" sort="Chen, Quan" uniqKey="Chen Q" first="Quan" last="Chen">Quan Chen</name><name sortKey="Liu, Lei" sort="Liu, Lei" uniqKey="Liu L" first="Lei" last="Liu">Lei Liu</name><name sortKey="Qin, Yan" sort="Qin, Yan" uniqKey="Qin Y" first="Yan" last="Qin">Yan Qin</name><name sortKey="Wang, Xiaohui" sort="Wang, Xiaohui" uniqKey="Wang X" first="Xiaohui" last="Wang">Xiaohui Wang</name><name sortKey="Wei, Huifang" sort="Wei, Huifang" uniqKey="Wei H" first="Huifang" last="Wei">Huifang Wei</name><name sortKey="Zhang, Dejiu" sort="Zhang, Dejiu" uniqKey="Zhang D" first="Dejiu" last="Zhang">Dejiu Zhang</name><name sortKey="Zhang, Di" sort="Zhang, Di" uniqKey="Zhang D" first="Di" last="Zhang">Di Zhang</name></country><country name="Pakistan"><noRegion><name sortKey="Sehgal, Sheikh Arslan" sort="Sehgal, Sheikh Arslan" uniqKey="Sehgal S" first="Sheikh Arslan" last="Sehgal">Sheikh Arslan Sehgal</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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