The PARK10 gene USP24 is a negative regulator of autophagy and ULK1 protein stability.
Identifieur interne : 000031 ( Main/Exploration ); précédent : 000030; suivant : 000032The PARK10 gene USP24 is a negative regulator of autophagy and ULK1 protein stability.
Auteurs : Julia A. Thayer [États-Unis] ; Ola Awad ; Nivedita Hegdekar [États-Unis] ; Chinmoy Sarkar [États-Unis] ; Henok Tesfay [États-Unis] ; Cameran Burt [États-Unis] ; Xianmin Zeng [États-Unis] ; Ricardo A. Feldman ; Marta M. Lipinski [États-Unis]Source :
- Autophagy [ 1554-8635 ] ; 2020.
Abstract
Recent studies indicate a causative relationship between defects in autophagy and dopaminergic neuron degeneration in Parkinson disease (PD). However, it is not fully understood how autophagy is regulated in the context of PD. Here we identify USP24 (ubiquitin specific peptidase 24), a gene located in the PARK10 (Parkinson disease 10 [susceptibility]) locus associated with late onset PD, as a novel negative regulator of autophagy. Our data indicate that USP24 regulates autophagy by affecting ubiquitination and stability of the ULK1 protein. Knockdown of USP24 in cell lines and in human induced-pluripotent stem cells (iPSC) differentiated into dopaminergic neurons resulted in elevated ULK1 protein levels and increased autophagy flux in a manner independent of MTORC1 but dependent on the class III phosphatidylinositol 3-kinase (PtdIns3K) activity. Surprisingly, USP24 knockdown also improved neurite extension and/or maintenance in aged iPSC-derived dopaminergic neurons. Furthermore, we observed elevated levels of USP24 in the substantia nigra of a subpopulation of idiopathic PD patients, suggesting that USP24 may negatively regulate autophagy in PD.Abbreviations: Bafilomycin/BafA: bafilomycin A1; DUB: deubiquitinating enzyme; iPSC: induced pluripotent stem cells; MTOR: mechanistic target of rapamycin kinase; MTORC1: MTOR complex 1; nt: non-targeting; PD: Parkinson disease; p-ATG13: phospho-ATG13; PtdIns3P: phosphatidylinositol 3-phosphate; RPS6: ribosomal protein S6; SNPs: single nucleotide polymorphisms; TH: tyrosine hydroxylase; USP24: ubiquitin specific peptidase 24.
DOI: 10.1080/15548627.2019.1598754
PubMed: 30957634
PubMed Central: PMC6984603
Affiliations:
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Thayer</name><affiliation wicri:level="2"><nlm:affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Awad, Ola" sort="Awad, Ola" uniqKey="Awad O" first="Ola" last="Awad">Ola Awad</name><affiliation><nlm:affiliation>Department of Microbiology and Immunology.</nlm:affiliation><wicri:noCountry code="no comma">Department of Microbiology and Immunology.</wicri:noCountry></affiliation></author><author><name sortKey="Hegdekar, Nivedita" sort="Hegdekar, Nivedita" uniqKey="Hegdekar N" first="Nivedita" last="Hegdekar">Nivedita Hegdekar</name><affiliation wicri:level="2"><nlm:affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Sarkar, Chinmoy" sort="Sarkar, Chinmoy" uniqKey="Sarkar C" first="Chinmoy" last="Sarkar">Chinmoy Sarkar</name><affiliation wicri:level="2"><nlm:affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Tesfay, Henok" sort="Tesfay, Henok" uniqKey="Tesfay H" first="Henok" last="Tesfay">Henok Tesfay</name><affiliation wicri:level="2"><nlm:affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Burt, Cameran" sort="Burt, Cameran" uniqKey="Burt C" first="Cameran" last="Burt">Cameran Burt</name><affiliation wicri:level="2"><nlm:affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Zeng, Xianmin" sort="Zeng, Xianmin" uniqKey="Zeng X" first="Xianmin" last="Zeng">Xianmin Zeng</name><affiliation wicri:level="2"><nlm:affiliation>XCell Science Inc, Novato, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>XCell Science Inc, Novato, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Feldman, Ricardo A" sort="Feldman, Ricardo A" uniqKey="Feldman R" first="Ricardo A" last="Feldman">Ricardo A. Feldman</name><affiliation><nlm:affiliation>Department of Microbiology and Immunology.</nlm:affiliation><wicri:noCountry code="no comma">Department of Microbiology and Immunology.</wicri:noCountry></affiliation></author><author><name sortKey="Lipinski, Marta M" sort="Lipinski, Marta M" uniqKey="Lipinski M" first="Marta M" last="Lipinski">Marta M. Lipinski</name><affiliation wicri:level="2"><nlm:affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, MD, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, MD</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author></analytic><series><title level="j">Autophagy</title><idno type="eISSN">1554-8635</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">Recent studies indicate a causative relationship between defects in autophagy and dopaminergic neuron degeneration in Parkinson disease (PD). However, it is not fully understood how autophagy is regulated in the context of PD. Here we identify <i>USP24</i> (ubiquitin specific peptidase 24), a gene located in the <i>PARK10</i> (Parkinson disease 10 [susceptibility]) locus associated with late onset PD, as a novel negative regulator of autophagy. Our data indicate that USP24 regulates autophagy by affecting ubiquitination and stability of the ULK1 protein. Knockdown of <i>USP24</i> in cell lines and in human induced-pluripotent stem cells (iPSC) differentiated into dopaminergic neurons resulted in elevated ULK1 protein levels and increased autophagy flux in a manner independent of MTORC1 but dependent on the class III phosphatidylinositol 3-kinase (PtdIns3K) activity. Surprisingly, <i>USP24</i> knockdown also improved neurite extension and/or maintenance in aged iPSC-derived dopaminergic neurons. Furthermore, we observed elevated levels of USP24 in the <i>substantia nigra</i> of a subpopulation of idiopathic PD patients, suggesting that USP24 may negatively regulate autophagy in PD.<b>Abbreviations</b>: Bafilomycin/BafA: bafilomycin A<sub>1</sub>; DUB: deubiquitinating enzyme; iPSC: induced pluripotent stem cells; MTOR: mechanistic target of rapamycin kinase; MTORC1: MTOR complex 1; nt: non-targeting; PD: Parkinson disease; p-ATG13: phospho-ATG13; PtdIns3P: phosphatidylinositol 3-phosphate; RPS6: ribosomal protein S6; SNPs: single nucleotide polymorphisms; TH: tyrosine hydroxylase; USP24: ubiquitin specific peptidase 24.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">30957634</PMID><DateRevised><Year>2020</Year><Month>04</Month><Day>12</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1554-8635</ISSN><JournalIssue CitedMedium="Internet"><Volume>16</Volume><Issue>1</Issue><PubDate><Year>2020</Year><Month>01</Month></PubDate></JournalIssue><Title>Autophagy</Title><ISOAbbreviation>Autophagy</ISOAbbreviation></Journal><ArticleTitle>The <i>PARK10</i> gene <i>USP24</i> is a negative regulator of autophagy and ULK1 protein stability.</ArticleTitle><Pagination><MedlinePgn>140-153</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1080/15548627.2019.1598754</ELocationID><Abstract><AbstractText>Recent studies indicate a causative relationship between defects in autophagy and dopaminergic neuron degeneration in Parkinson disease (PD). However, it is not fully understood how autophagy is regulated in the context of PD. Here we identify <i>USP24</i> (ubiquitin specific peptidase 24), a gene located in the <i>PARK10</i> (Parkinson disease 10 [susceptibility]) locus associated with late onset PD, as a novel negative regulator of autophagy. Our data indicate that USP24 regulates autophagy by affecting ubiquitination and stability of the ULK1 protein. Knockdown of <i>USP24</i> in cell lines and in human induced-pluripotent stem cells (iPSC) differentiated into dopaminergic neurons resulted in elevated ULK1 protein levels and increased autophagy flux in a manner independent of MTORC1 but dependent on the class III phosphatidylinositol 3-kinase (PtdIns3K) activity. Surprisingly, <i>USP24</i> knockdown also improved neurite extension and/or maintenance in aged iPSC-derived dopaminergic neurons. Furthermore, we observed elevated levels of USP24 in the <i>substantia nigra</i> of a subpopulation of idiopathic PD patients, suggesting that USP24 may negatively regulate autophagy in PD.<b>Abbreviations</b>: Bafilomycin/BafA: bafilomycin A<sub>1</sub>; DUB: deubiquitinating enzyme; iPSC: induced pluripotent stem cells; MTOR: mechanistic target of rapamycin kinase; MTORC1: MTOR complex 1; nt: non-targeting; PD: Parkinson disease; p-ATG13: phospho-ATG13; PtdIns3P: phosphatidylinositol 3-phosphate; RPS6: ribosomal protein S6; SNPs: single nucleotide polymorphisms; TH: tyrosine hydroxylase; USP24: ubiquitin specific peptidase 24.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Thayer</LastName><ForeName>Julia A</ForeName><Initials>JA</Initials><AffiliationInfo><Affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Awad</LastName><ForeName>Ola</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Immunology.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hegdekar</LastName><ForeName>Nivedita</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sarkar</LastName><ForeName>Chinmoy</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tesfay</LastName><ForeName>Henok</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Burt</LastName><ForeName>Cameran</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zeng</LastName><ForeName>Xianmin</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>XCell Science Inc, Novato, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Feldman</LastName><ForeName>Ricardo A</ForeName><Initials>RA</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Immunology.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lipinski</LastName><ForeName>Marta M</ForeName><Initials>MM</Initials><AffiliationInfo><Affiliation>Department of Anesthesiology & Shock, Trauma and Anesthesiology Research Center, University of Maryland School of Medicine, Baltimore, MD, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, MD, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>R01 NS091218</GrantID><Acronym>NS</Acronym><Agency>NINDS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 NS094527</GrantID><Acronym>NS</Acronym><Agency>NINDS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R03 NS087338</GrantID><Acronym>NS</Acronym><Agency>NINDS 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>2019</Year><Month>04</Month><Day>07</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Autophagy</MedlineTA><NlmUniqueID>101265188</NlmUniqueID><ISSNLinking>1554-8627</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Autophagy</Keyword><Keyword MajorTopicYN="Y">Parkinson disease</Keyword><Keyword MajorTopicYN="Y">USP24</Keyword><Keyword MajorTopicYN="Y">dopaminergic neurons</Keyword><Keyword MajorTopicYN="Y">induced-pluripotent stem cells</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate 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