Ca2+ is a key factor in α-synuclein-induced neurotoxicity.
Identifieur interne : 000303 ( PubMed/Checkpoint ); précédent : 000302; suivant : 000304Ca2+ is a key factor in α-synuclein-induced neurotoxicity.
Auteurs : Plamena R. Angelova [Royaume-Uni] ; Marthe H R. Ludtmann [Royaume-Uni] ; Mathew H. Horrocks [Royaume-Uni] ; Alexander Negoda [Canada] ; Nunilo Cremades [Royaume-Uni] ; David Klenerman [Royaume-Uni] ; Christopher M. Dobson [Royaume-Uni] ; Nicholas W. Wood [Royaume-Uni] ; Evgeny V. Pavlov [États-Unis] ; Sonia Gandhi [Royaume-Uni] ; Andrey Y. Abramov [Royaume-Uni]Source :
- Journal of cell science [ 1477-9137 ] ; 2016.
Abstract
Aggregation of α-synuclein leads to the formation of oligomeric intermediates that can interact with membranes to form pores. However, it is unknown how this leads to cell toxicity in Parkinson's disease. We investigated the species-specific effects of α-synuclein on Ca(2+) signalling in primary neurons and astrocytes using live neuronal imaging and electrophysiology on artificial membranes. We demonstrate that α-synuclein induces an increase in basal intracellular Ca(2+) in its unfolded monomeric state as well as in its oligomeric state. Electrophysiology of artificial membranes demonstrated that α-synuclein monomers induce irregular ionic currents, whereas α-synuclein oligomers induce rare discrete channel formation events. Despite the ability of monomeric α-synuclein to affect Ca(2+) signalling, it is only the oligomeric form of α-synuclein that induces cell death. Oligomer-induced cell death was abolished by the exclusion of extracellular Ca(2+), which prevented the α-synuclein-induced Ca(2+) dysregulation. The findings of this study confirm that α-synuclein interacts with membranes to affect Ca(2+) signalling in a structure-specific manner and the oligomeric β-sheet-rich α-synuclein species ultimately leads to Ca(2+) dysregulation and Ca(2+)-dependent cell death.
DOI: 10.1242/jcs.180737
PubMed: 26989132
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Pavlov</name><affiliation wicri:level="1"><nlm:affiliation>Department of Physiology and Biophysics, Dalhousie University, Halifax B3H 4R2, Canada College of Dentistry, New York University, New York 10010, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Physiology and Biophysics, Dalhousie University, Halifax B3H 4R2, Canada College of Dentistry, New York University, New York 10010</wicri:regionArea><wicri:noRegion>New York 10010</wicri:noRegion></affiliation></author><author><name sortKey="Gandhi, Sonia" sort="Gandhi, Sonia" uniqKey="Gandhi S" first="Sonia" last="Gandhi">Sonia Gandhi</name><affiliation wicri:level="1"><nlm:affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK a.abramov@ucl.ac.uk sonia.gandhi@ucl.ac.uk.</nlm:affiliation><country wicri:rule="url">Royaume-Uni</country><wicri:regionArea>UCL Institute of Neurology, Queen Square, London WC1N 3BG</wicri:regionArea><wicri:noRegion>London WC1N 3BG</wicri:noRegion></affiliation></author><author><name sortKey="Abramov, Andrey Y" sort="Abramov, Andrey Y" uniqKey="Abramov A" first="Andrey Y" last="Abramov">Andrey Y. 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Angelova</name><affiliation wicri:level="1"><nlm:affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>UCL Institute of Neurology, Queen Square, London WC1N 3BG</wicri:regionArea><wicri:noRegion>London WC1N 3BG</wicri:noRegion></affiliation></author><author><name sortKey="Ludtmann, Marthe H R" sort="Ludtmann, Marthe H R" uniqKey="Ludtmann M" first="Marthe H R" last="Ludtmann">Marthe H R. Ludtmann</name><affiliation wicri:level="1"><nlm:affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>UCL Institute of Neurology, Queen Square, London WC1N 3BG</wicri:regionArea><wicri:noRegion>London WC1N 3BG</wicri:noRegion></affiliation></author><author><name sortKey="Horrocks, Mathew H" sort="Horrocks, Mathew H" uniqKey="Horrocks M" first="Mathew H" last="Horrocks">Mathew H. Horrocks</name><affiliation wicri:level="4"><nlm:affiliation>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Negoda, Alexander" sort="Negoda, Alexander" uniqKey="Negoda A" first="Alexander" last="Negoda">Alexander Negoda</name><affiliation wicri:level="1"><nlm:affiliation>Department of Physiology and Biophysics, Dalhousie University, Halifax B3H 4R2, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Physiology and Biophysics, Dalhousie University, Halifax B3H 4R2</wicri:regionArea><wicri:noRegion>Halifax B3H 4R2</wicri:noRegion></affiliation></author><author><name sortKey="Cremades, Nunilo" sort="Cremades, Nunilo" uniqKey="Cremades N" first="Nunilo" last="Cremades">Nunilo Cremades</name><affiliation wicri:level="4"><nlm:affiliation>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Klenerman, David" sort="Klenerman, David" uniqKey="Klenerman D" first="David" last="Klenerman">David Klenerman</name><affiliation wicri:level="4"><nlm:affiliation>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Dobson, Christopher M" sort="Dobson, Christopher M" uniqKey="Dobson C" first="Christopher M" last="Dobson">Christopher M. Dobson</name><affiliation wicri:level="4"><nlm:affiliation>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Wood, Nicholas W" sort="Wood, Nicholas W" uniqKey="Wood N" first="Nicholas W" last="Wood">Nicholas W. Wood</name><affiliation wicri:level="1"><nlm:affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>UCL Institute of Neurology, Queen Square, London WC1N 3BG</wicri:regionArea><wicri:noRegion>London WC1N 3BG</wicri:noRegion></affiliation></author><author><name sortKey="Pavlov, Evgeny V" sort="Pavlov, Evgeny V" uniqKey="Pavlov E" first="Evgeny V" last="Pavlov">Evgeny V. Pavlov</name><affiliation wicri:level="1"><nlm:affiliation>Department of Physiology and Biophysics, Dalhousie University, Halifax B3H 4R2, Canada College of Dentistry, New York University, New York 10010, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Physiology and Biophysics, Dalhousie University, Halifax B3H 4R2, Canada College of Dentistry, New York University, New York 10010</wicri:regionArea><wicri:noRegion>New York 10010</wicri:noRegion></affiliation></author><author><name sortKey="Gandhi, Sonia" sort="Gandhi, Sonia" uniqKey="Gandhi S" first="Sonia" last="Gandhi">Sonia Gandhi</name><affiliation wicri:level="1"><nlm:affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK a.abramov@ucl.ac.uk sonia.gandhi@ucl.ac.uk.</nlm:affiliation><country wicri:rule="url">Royaume-Uni</country><wicri:regionArea>UCL Institute of Neurology, Queen Square, London WC1N 3BG</wicri:regionArea><wicri:noRegion>London WC1N 3BG</wicri:noRegion></affiliation></author><author><name sortKey="Abramov, Andrey Y" sort="Abramov, Andrey Y" uniqKey="Abramov A" first="Andrey Y" last="Abramov">Andrey Y. Abramov</name><affiliation wicri:level="1"><nlm:affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK a.abramov@ucl.ac.uk sonia.gandhi@ucl.ac.uk.</nlm:affiliation><country wicri:rule="url">Royaume-Uni</country><wicri:regionArea>UCL Institute of Neurology, Queen Square, London WC1N 3BG</wicri:regionArea><wicri:noRegion>London WC1N 3BG</wicri:noRegion></affiliation></author></analytic><series><title level="j">Journal of cell science</title><idno type="eISSN">1477-9137</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Aggregation of α-synuclein leads to the formation of oligomeric intermediates that can interact with membranes to form pores. However, it is unknown how this leads to cell toxicity in Parkinson's disease. We investigated the species-specific effects of α-synuclein on Ca(2+) signalling in primary neurons and astrocytes using live neuronal imaging and electrophysiology on artificial membranes. We demonstrate that α-synuclein induces an increase in basal intracellular Ca(2+) in its unfolded monomeric state as well as in its oligomeric state. Electrophysiology of artificial membranes demonstrated that α-synuclein monomers induce irregular ionic currents, whereas α-synuclein oligomers induce rare discrete channel formation events. Despite the ability of monomeric α-synuclein to affect Ca(2+) signalling, it is only the oligomeric form of α-synuclein that induces cell death. Oligomer-induced cell death was abolished by the exclusion of extracellular Ca(2+), which prevented the α-synuclein-induced Ca(2+) dysregulation. The findings of this study confirm that α-synuclein interacts with membranes to affect Ca(2+) signalling in a structure-specific manner and the oligomeric β-sheet-rich α-synuclein species ultimately leads to Ca(2+) dysregulation and Ca(2+)-dependent cell death.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">26989132</PMID><DateCreated><Year>2016</Year><Month>05</Month><Day>02</Day></DateCreated><DateRevised><Year>2017</Year><Month>03</Month><Day>24</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1477-9137</ISSN><JournalIssue CitedMedium="Internet"><Volume>129</Volume><Issue>9</Issue><PubDate><Year>2016</Year><Month>May</Month><Day>01</Day></PubDate></JournalIssue><Title>Journal of cell science</Title><ISOAbbreviation>J. Cell. Sci.</ISOAbbreviation></Journal><ArticleTitle>Ca2+ is a key factor in α-synuclein-induced neurotoxicity.</ArticleTitle><Pagination><MedlinePgn>1792-801</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1242/jcs.180737</ELocationID><Abstract><AbstractText>Aggregation of α-synuclein leads to the formation of oligomeric intermediates that can interact with membranes to form pores. However, it is unknown how this leads to cell toxicity in Parkinson's disease. We investigated the species-specific effects of α-synuclein on Ca(2+) signalling in primary neurons and astrocytes using live neuronal imaging and electrophysiology on artificial membranes. We demonstrate that α-synuclein induces an increase in basal intracellular Ca(2+) in its unfolded monomeric state as well as in its oligomeric state. Electrophysiology of artificial membranes demonstrated that α-synuclein monomers induce irregular ionic currents, whereas α-synuclein oligomers induce rare discrete channel formation events. Despite the ability of monomeric α-synuclein to affect Ca(2+) signalling, it is only the oligomeric form of α-synuclein that induces cell death. Oligomer-induced cell death was abolished by the exclusion of extracellular Ca(2+), which prevented the α-synuclein-induced Ca(2+) dysregulation. The findings of this study confirm that α-synuclein interacts with membranes to affect Ca(2+) signalling in a structure-specific manner and the oligomeric β-sheet-rich α-synuclein species ultimately leads to Ca(2+) dysregulation and Ca(2+)-dependent cell death.</AbstractText><CopyrightInformation>© 2016. Published by The Company of Biologists Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Angelova</LastName><ForeName>Plamena R</ForeName><Initials>PR</Initials><AffiliationInfo><Affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ludtmann</LastName><ForeName>Marthe H R</ForeName><Initials>MH</Initials><AffiliationInfo><Affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Horrocks</LastName><ForeName>Mathew H</ForeName><Initials>MH</Initials><AffiliationInfo><Affiliation>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Negoda</LastName><ForeName>Alexander</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Physiology and Biophysics, Dalhousie University, Halifax B3H 4R2, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cremades</LastName><ForeName>Nunilo</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Klenerman</LastName><ForeName>David</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dobson</LastName><ForeName>Christopher M</ForeName><Initials>CM</Initials><AffiliationInfo><Affiliation>Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wood</LastName><ForeName>Nicholas W</ForeName><Initials>NW</Initials><AffiliationInfo><Affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pavlov</LastName><ForeName>Evgeny V</ForeName><Initials>EV</Initials><AffiliationInfo><Affiliation>Department of Physiology and Biophysics, Dalhousie University, Halifax B3H 4R2, Canada College of Dentistry, New York University, New York 10010, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gandhi</LastName><ForeName>Sonia</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK a.abramov@ucl.ac.uk sonia.gandhi@ucl.ac.uk.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Abramov</LastName><ForeName>Andrey Y</ForeName><Initials>AY</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-7646-7235</Identifier><AffiliationInfo><Affiliation>UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK a.abramov@ucl.ac.uk sonia.gandhi@ucl.ac.uk.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>H-1006</GrantID><Agency>Parkinson's UK</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>MC_G1000735</GrantID><Agency>Medical Research Council</Agency><Country>United Kingdom</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>03</Month><Day>17</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>J Cell Sci</MedlineTA><NlmUniqueID>0052457</NlmUniqueID><ISSNLinking>0021-9533</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="Cites"><RefSource>Mol Neurodegener. 2009 Feb 04;4:9</RefSource><PMID Version="1">19193223</PMID></CommentsCorrections><CommentsCorrections 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RefType="Cites"><RefSource>Biochemistry. 2002 Apr 9;41(14):4595-602</RefSource><PMID Version="1">11926821</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Neuron. 2011 Oct 6;72(1):57-71</RefSource><PMID Version="1">21982369</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>J Neurosci. 2003 Jun 15;23(12):5088-95</RefSource><PMID Version="1">12832532</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Antioxid Redox Signal. 2016 Mar 1;24(7):376-91</RefSource><PMID Version="1">26564470</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Aging Cell. 2011 Aug;10(4):595-603</RefSource><PMID Version="1">21332922</PMID></CommentsCorrections></CommentsCorrectionsList><OtherID Source="NLM">PMC4893653</OtherID><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Ca2+ signalling</Keyword><Keyword MajorTopicYN="N">Neuronal death</Keyword><Keyword MajorTopicYN="N">Parkinson's disease</Keyword><Keyword MajorTopicYN="N">α-Synuclein</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2015</Year><Month>09</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2016</Year><Month>02</Month><Day>22</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2016</Year><Month>3</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2016</Year><Month>3</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2016</Year><Month>3</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">26989132</ArticleId><ArticleId IdType="pii">jcs.180737</ArticleId><ArticleId IdType="doi">10.1242/jcs.180737</ArticleId><ArticleId IdType="pmc">PMC4893653</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Canada</li><li>Royaume-Uni</li><li>États-Unis</li></country><region><li>Angleterre</li><li>Angleterre de l'Est</li></region><settlement><li>Cambridge</li></settlement><orgName><li>Université de Cambridge</li></orgName></list><tree><country name="Royaume-Uni"><noRegion><name sortKey="Angelova, Plamena R" sort="Angelova, Plamena R" uniqKey="Angelova P" first="Plamena R" last="Angelova">Plamena R. Angelova</name></noRegion><name sortKey="Abramov, Andrey Y" sort="Abramov, Andrey Y" uniqKey="Abramov A" first="Andrey Y" last="Abramov">Andrey Y. Abramov</name><name sortKey="Cremades, Nunilo" sort="Cremades, Nunilo" uniqKey="Cremades N" first="Nunilo" last="Cremades">Nunilo Cremades</name><name sortKey="Dobson, Christopher M" sort="Dobson, Christopher M" uniqKey="Dobson C" first="Christopher M" last="Dobson">Christopher M. Dobson</name><name sortKey="Gandhi, Sonia" sort="Gandhi, Sonia" uniqKey="Gandhi S" first="Sonia" last="Gandhi">Sonia Gandhi</name><name sortKey="Horrocks, Mathew H" sort="Horrocks, Mathew H" uniqKey="Horrocks M" first="Mathew H" last="Horrocks">Mathew H. Horrocks</name><name sortKey="Klenerman, David" sort="Klenerman, David" uniqKey="Klenerman D" first="David" last="Klenerman">David Klenerman</name><name sortKey="Ludtmann, Marthe H R" sort="Ludtmann, Marthe H R" uniqKey="Ludtmann M" first="Marthe H R" last="Ludtmann">Marthe H R. Ludtmann</name><name sortKey="Wood, Nicholas W" sort="Wood, Nicholas W" uniqKey="Wood N" first="Nicholas W" last="Wood">Nicholas W. Wood</name></country><country name="Canada"><noRegion><name sortKey="Negoda, Alexander" sort="Negoda, Alexander" uniqKey="Negoda A" first="Alexander" last="Negoda">Alexander Negoda</name></noRegion></country><country name="États-Unis"><noRegion><name sortKey="Pavlov, Evgeny V" sort="Pavlov, Evgeny V" uniqKey="Pavlov E" first="Evgeny V" last="Pavlov">Evgeny V. Pavlov</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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