Involvement of Striatal Cholinergic Interneurons and M1 and M4 Muscarinic Receptors in Motor Symptoms of Parkinson's Disease.
Identifieur interne : 000100 ( PubMed/Curation ); précédent : 000099; suivant : 000101Involvement of Striatal Cholinergic Interneurons and M1 and M4 Muscarinic Receptors in Motor Symptoms of Parkinson's Disease.
Auteurs : Samira Ztaou [France] ; Nicolas Maurice ; Jeremy Camon [France] ; Gaëlle Guiraudie-Capraz [France] ; Lydia Kerkerian-Le Goff ; Corinne Beurrier ; Martine Liberge [France] ; Marianne Amalric [France]Source :
- The Journal of neuroscience : the official journal of the Society for Neuroscience [ 1529-2401 ] ; 2016.
Abstract
Over the last decade, striatal cholinergic interneurons (ChIs) have reemerged as key actors in the pathophysiology of basal-ganglia-related movement disorders. However, the mechanisms involved are still unclear. In this study, we address the role of ChI activity in the expression of parkinsonian-like motor deficits in a unilateral nigrostriatal 6-hydroxydopamine (6-OHDA) lesion model using optogenetic and pharmacological approaches. Dorsal striatal photoinhibition of ChIs in lesioned ChAT(cre/cre) mice expressing halorhodopsin in ChIs reduces akinesia, bradykinesia, and sensorimotor neglect. Muscarinic acetylcholine receptor (mAChR) blockade by scopolamine produces similar anti-parkinsonian effects. To decipher which of the mAChR subtypes provides these beneficial effects, systemic and intrastriatal administration of the selective M1 and M4 mAChR antagonists telenzepine and tropicamide, respectively, were tested in the same model of Parkinson's disease. The two compounds alleviate 6-OHDA lesion-induced motor deficits. Telenzepine produces its beneficial effects by blocking postsynaptic M1 mAChRs expressed on medium spiny neurons (MSNs) at the origin of the indirect striatopallidal and direct striatonigral pathways. The anti-parkinsonian effects of tropicamide were almost completely abolished in mutant lesioned mice that lack M4 mAChRs specifically in dopamine D1-receptor-expressing neurons, suggesting that postsynaptic M4 mAChRs expressed on direct MSNs mediate the antiakinetic action of tropicamide. The present results show that altered cholinergic transmission via M1 and M4 mAChRs of the dorsal striatum plays a pivotal role in the occurrence of motor symptoms in Parkinson's disease.
DOI: 10.1523/JNEUROSCI.0873-16.2016
PubMed: 27581457
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Nicolas Maurice<affiliation><nlm:affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, IBDM, 13288 Marseille cdx 09, France, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation><affiliation><nlm:affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, IBDM, 13288 Marseille cdx 09, France, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation><affiliation><nlm:affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, IBDM, 13288 Marseille cdx 09, France, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation>Le document en format XML
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Goff</name><affiliation><nlm:affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, IBDM, 13288 Marseille cdx 09, France, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation></author><author><name sortKey="Beurrier, Corinne" sort="Beurrier, Corinne" uniqKey="Beurrier C" first="Corinne" last="Beurrier">Corinne Beurrier</name><affiliation><nlm:affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, IBDM, 13288 Marseille cdx 09, France, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation></author><author><name sortKey="Liberge, Martine" sort="Liberge, Martine" uniqKey="Liberge M" first="Martine" last="Liberge">Martine Liberge</name><affiliation wicri:level="1"><nlm:affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, LNC, FR3C, 13331 Marseille cdx 03, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Aix Marseille University, Centre National de la Recherche Scientifique, LNC, FR3C, 13331 Marseille cdx 03</wicri:regionArea></affiliation></author><author><name sortKey="Amalric, Marianne" sort="Amalric, Marianne" uniqKey="Amalric M" first="Marianne" last="Amalric">Marianne Amalric</name><affiliation wicri:level="1"><nlm:affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, LNC, FR3C, 13331 Marseille cdx 03, France, marianne.amalric@univ-amu.fr.</nlm:affiliation><country wicri:rule="url">France</country><wicri:regionArea>Aix Marseille University, Centre National de la Recherche Scientifique, LNC, FR3C, 13331 Marseille cdx 03, France</wicri:regionArea></affiliation></author></analytic><series><title level="j">The Journal of neuroscience : the official journal of the Society for Neuroscience</title><idno type="eISSN">1529-2401</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">Over the last decade, striatal cholinergic interneurons (ChIs) have reemerged as key actors in the pathophysiology of basal-ganglia-related movement disorders. However, the mechanisms involved are still unclear. In this study, we address the role of ChI activity in the expression of parkinsonian-like motor deficits in a unilateral nigrostriatal 6-hydroxydopamine (6-OHDA) lesion model using optogenetic and pharmacological approaches. Dorsal striatal photoinhibition of ChIs in lesioned ChAT(cre/cre) mice expressing halorhodopsin in ChIs reduces akinesia, bradykinesia, and sensorimotor neglect. Muscarinic acetylcholine receptor (mAChR) blockade by scopolamine produces similar anti-parkinsonian effects. To decipher which of the mAChR subtypes provides these beneficial effects, systemic and intrastriatal administration of the selective M1 and M4 mAChR antagonists telenzepine and tropicamide, respectively, were tested in the same model of Parkinson's disease. The two compounds alleviate 6-OHDA lesion-induced motor deficits. Telenzepine produces its beneficial effects by blocking postsynaptic M1 mAChRs expressed on medium spiny neurons (MSNs) at the origin of the indirect striatopallidal and direct striatonigral pathways. The anti-parkinsonian effects of tropicamide were almost completely abolished in mutant lesioned mice that lack M4 mAChRs specifically in dopamine D1-receptor-expressing neurons, suggesting that postsynaptic M4 mAChRs expressed on direct MSNs mediate the antiakinetic action of tropicamide. The present results show that altered cholinergic transmission via M1 and M4 mAChRs of the dorsal striatum plays a pivotal role in the occurrence of motor symptoms in Parkinson's disease.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">27581457</PMID><DateCreated><Year>2016</Year><Month>09</Month><Day>01</Day></DateCreated><DateRevised><Year>2016</Year><Month>09</Month><Day>01</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1529-2401</ISSN><JournalIssue CitedMedium="Internet"><Volume>36</Volume><Issue>35</Issue><PubDate><Year>2016</Year><Month>Aug</Month><Day>31</Day></PubDate></JournalIssue><Title>The Journal of neuroscience : the official journal of the Society for Neuroscience</Title><ISOAbbreviation>J. Neurosci.</ISOAbbreviation></Journal><ArticleTitle>Involvement of Striatal Cholinergic Interneurons and M1 and M4 Muscarinic Receptors in Motor Symptoms of Parkinson's Disease.</ArticleTitle><Pagination><MedlinePgn>9161-72</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1523/JNEUROSCI.0873-16.2016</ELocationID><Abstract><AbstractText Label="UNLABELLED">Over the last decade, striatal cholinergic interneurons (ChIs) have reemerged as key actors in the pathophysiology of basal-ganglia-related movement disorders. However, the mechanisms involved are still unclear. In this study, we address the role of ChI activity in the expression of parkinsonian-like motor deficits in a unilateral nigrostriatal 6-hydroxydopamine (6-OHDA) lesion model using optogenetic and pharmacological approaches. Dorsal striatal photoinhibition of ChIs in lesioned ChAT(cre/cre) mice expressing halorhodopsin in ChIs reduces akinesia, bradykinesia, and sensorimotor neglect. Muscarinic acetylcholine receptor (mAChR) blockade by scopolamine produces similar anti-parkinsonian effects. To decipher which of the mAChR subtypes provides these beneficial effects, systemic and intrastriatal administration of the selective M1 and M4 mAChR antagonists telenzepine and tropicamide, respectively, were tested in the same model of Parkinson's disease. The two compounds alleviate 6-OHDA lesion-induced motor deficits. Telenzepine produces its beneficial effects by blocking postsynaptic M1 mAChRs expressed on medium spiny neurons (MSNs) at the origin of the indirect striatopallidal and direct striatonigral pathways. The anti-parkinsonian effects of tropicamide were almost completely abolished in mutant lesioned mice that lack M4 mAChRs specifically in dopamine D1-receptor-expressing neurons, suggesting that postsynaptic M4 mAChRs expressed on direct MSNs mediate the antiakinetic action of tropicamide. The present results show that altered cholinergic transmission via M1 and M4 mAChRs of the dorsal striatum plays a pivotal role in the occurrence of motor symptoms in Parkinson's disease.</AbstractText><AbstractText Label="SIGNIFICANCE STATEMENT" NlmCategory="UNASSIGNED">The striatum, where dopaminergic and cholinergic systems interact, is the pivotal structure of basal ganglia involved in pathophysiological changes underlying Parkinson's disease. Here, using optogenetic and pharmacological approaches, we investigated the involvement of striatal cholinergic interneurons (ChIs) and muscarinic receptor subtypes (mAChRs) in the occurrence of a wide range of motor deficits such as akinesia, bradykinesia, motor coordination, and sensorimotor neglect after unilateral nigrostriatal 6-hydroxydopamine lesion in mice. Our results show that photoinhibition of ChIs in the dorsal striatum and pharmacological blockade of muscarinic receptors, specifically postsynaptic M1 and M4 mAChRs, alleviate lesion-induced motor deficits. The present study points to these receptor subtypes as potential targets for the symptomatic treatment of parkinsonian-like motor symptoms.</AbstractText><CopyrightInformation>Copyright © 2016 the authors 0270-6474/16/369162-12$15.00/0.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Ztaou</LastName><ForeName>Samira</ForeName><Initials>S</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-2058-4915</Identifier><AffiliationInfo><Affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, LNC, FR3C, 13331 Marseille cdx 03, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maurice</LastName><ForeName>Nicolas</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, IBDM, 13288 Marseille cdx 09, France, and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Camon</LastName><ForeName>Jeremy</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, LNC, FR3C, 13331 Marseille cdx 03, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Guiraudie-Capraz</LastName><ForeName>Gaëlle</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, NICN, 13344 Marseille cdx 15, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kerkerian-Le Goff</LastName><ForeName>Lydia</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, IBDM, 13288 Marseille cdx 09, France, and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Beurrier</LastName><ForeName>Corinne</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, IBDM, 13288 Marseille cdx 09, France, and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liberge</LastName><ForeName>Martine</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, LNC, FR3C, 13331 Marseille cdx 03, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Amalric</LastName><ForeName>Marianne</ForeName><Initials>M</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-9915-6763</Identifier><AffiliationInfo><Affiliation>Aix Marseille University, Centre National de la Recherche Scientifique, LNC, FR3C, 13331 Marseille cdx 03, France, marianne.amalric@univ-amu.fr.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Neurosci</MedlineTA><NlmUniqueID>8102140</NlmUniqueID><ISSNLinking>0270-6474</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Parkinson's disease</Keyword><Keyword MajorTopicYN="N">basal ganglia</Keyword><Keyword MajorTopicYN="N">cholinergic interneurons</Keyword><Keyword MajorTopicYN="N">motor symptoms</Keyword><Keyword MajorTopicYN="N">muscarinic receptors</Keyword><Keyword MajorTopicYN="N">striatum</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2016</Year><Month>03</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2016</Year><Month>07</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2016</Year><Month>9</Month><Day>2</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2016</Year><Month>9</Month><Day>2</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2016</Year><Month>9</Month><Day>2</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">27581457</ArticleId><ArticleId IdType="pii">36/35/9161</ArticleId><ArticleId IdType="doi">10.1523/JNEUROSCI.0873-16.2016</ArticleId></ArticleIdList></PubmedData></pubmed></record>Pour manipuler ce document sous Unix (Dilib)
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