Manganese-Induced Atypical Parkinsonism Is Associated with Altered Basal Ganglia Activity and Changes in Tissue Levels of Monoamines in the Rat
Identifieur interne : 000340 ( Pmc/Checkpoint ); précédent : 000339; suivant : 000341Manganese-Induced Atypical Parkinsonism Is Associated with Altered Basal Ganglia Activity and Changes in Tissue Levels of Monoamines in the Rat
Auteurs : Safa Bouabid [France, Maroc] ; Claire Delaville [France] ; Philippe De Deurwaerdère [France] ; Nouria Lakhdar-Ghazal [Maroc] ; Abdelhamid Benazzouz [France]Source :
- PLoS ONE [ 1932-6203 ] ; 2014.
Abstract
Manganese neurotoxicity is associated with motor and cognitive disturbances known as Manganism. However, the mechanisms underlying these deficits remain unknown. Here we investigated the effects of manganese intoxication on motor and non-motor parkinsonian-like deficits such as locomotor activity, motor coordination, anxiety and “depressive-like” behaviors. Then, we studied the impact of this intoxication on the neuronal activity, the globus pallidus (GP) and subthalamic nucleus (STN). At the end of experiments, post-mortem tissue level of the three monoamines (dopamine, norepinephrine and serotonin) has been determined. The experiments were carried out in adult Sprague-Dawley rats, daily treated with MnCl2 (10 mg/kg/, i.p.) for 5 weeks. We show that manganese progressively reduced locomotor activity as well as motor coordination in parallel with the manifestation of anxiety and “depressive-like” behaviors. Electrophysiological results show that, while majority of GP and STN neurons discharged regularly in controls, manganese increased the number of GP and STN neurons discharging irregularly and/or with bursts. Biochemical results show that manganese significantly decreased tissue levels of norepinephrine and serotonin with increased metabolism of dopamine in the striatum. Our data provide evidence that manganese intoxication is associated with impaired neurotransmission of monoaminergic systems, which is at the origin of changes in basal ganglia neuronal activity and the manifestation of motor and non-motor deficits similar to those observed in atypical Parkinsonism.
Url:
DOI: 10.1371/journal.pone.0098952
PubMed: 24896650
PubMed Central: 4045849
Affiliations:
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<front><div type="abstract" xml:lang="en"><p>Manganese neurotoxicity is associated with motor and cognitive disturbances known as Manganism. However, the mechanisms underlying these deficits remain unknown. Here we investigated the effects of manganese intoxication on motor and non-motor parkinsonian-like deficits such as locomotor activity, motor coordination, anxiety and “depressive-like” behaviors. Then, we studied the impact of this intoxication on the neuronal activity, the globus pallidus (GP) and subthalamic nucleus (STN). At the end of experiments, post-mortem tissue level of the three monoamines (dopamine, norepinephrine and serotonin) has been determined. The experiments were carried out in adult Sprague-Dawley rats, daily treated with MnCl<sub>2</sub>
(10 mg/kg/, i.p.) for 5 weeks. We show that manganese progressively reduced locomotor activity as well as motor coordination in parallel with the manifestation of anxiety and “depressive-like” behaviors. Electrophysiological results show that, while majority of GP and STN neurons discharged regularly in controls, manganese increased the number of GP and STN neurons discharging irregularly and/or with bursts. Biochemical results show that manganese significantly decreased tissue levels of norepinephrine and serotonin with increased metabolism of dopamine in the striatum. Our data provide evidence that manganese intoxication is associated with impaired neurotransmission of monoaminergic systems, which is at the origin of changes in basal ganglia neuronal activity and the manifestation of motor and non-motor deficits similar to those observed in atypical Parkinsonism.</p>
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<biblStruct><analytic><author><name sortKey="Pan, Hs" uniqKey="Pan H">HS Pan</name>
</author>
<author><name sortKey="Walters, Jr" uniqKey="Walters J">JR Walters</name>
</author>
</analytic>
</biblStruct>
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</div1>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24896650</article-id>
<article-id pub-id-type="pmc">4045849</article-id>
<article-id pub-id-type="publisher-id">PONE-D-14-05265</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0098952</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Anatomy</subject>
<subj-group><subject>Nervous System</subject>
<subj-group><subject>Motor System</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Neurochemistry</subject>
<subj-group><subject>Neurotransmitters</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Neuroscience</subject>
<subj-group><subject>Neural Networks</subject>
</subj-group>
</subj-group>
<subj-group><subject>Toxicology</subject>
<subj-group><subject>Neurotoxicology</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Neurology</subject>
<subj-group><subject>Neurobiology of Disease and Regeneration</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Research and Analysis Methods</subject>
<subj-group><subject>Specimen Preparation and Treatment</subject>
<subj-group><subject>Mechanical Treatment of Specimens</subject>
<subj-group><subject>Specimen Disruption</subject>
<subj-group><subject>Electroporation</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Manganese-Induced Atypical Parkinsonism Is Associated with Altered Basal Ganglia Activity and Changes in Tissue Levels of Monoamines in the Rat</article-title>
<alt-title alt-title-type="running-head">Manganese, Basal Ganglia and Monoamines</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Bouabid</surname>
<given-names>Safa</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Delaville</surname>
<given-names>Claire</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>De Deurwaerdère</surname>
<given-names>Philippe</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lakhdar-Ghazal</surname>
<given-names>Nouria</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Benazzouz</surname>
<given-names>Abdelhamid</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Univ. de Bordeaux, Institut des Maladies Neurodégénératives, UMR 5293, Bordeaux, France</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>CNRS, Institut des Maladies Neurodégénératives, UMR 5293, Bordeaux, France</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Université Mohamed V-Agdal, Faculté des Sciences, Equipe Rythmes Biologiques, Neurosciences et Environnement, Rabat, Morocco</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Yung</surname>
<given-names>Wing-ho</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>The Chinese University of Hong Kong, Hong Kong</addr-line>
</aff>
<author-notes><corresp id="cor1">* E-mail: <email>Abdelhamid.Benazzouz@u-bordeaux.fr</email>
</corresp>
<fn fn-type="conflict"><p><bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con"><p>Conceived and designed the experiments: NLG AB. Performed the experiments: SB CD. Analyzed the data: SB CD PDD. Wrote the paper: SB AB.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>4</day>
<month>6</month>
<year>2014</year>
</pub-date>
<volume>9</volume>
<issue>6</issue>
<elocation-id>e98952</elocation-id>
<history><date date-type="received"><day>4</day>
<month>2</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>9</day>
<month>5</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-year>2014</copyright-year>
<copyright-holder>Bouabid et al</copyright-holder>
<license><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<abstract><p>Manganese neurotoxicity is associated with motor and cognitive disturbances known as Manganism. However, the mechanisms underlying these deficits remain unknown. Here we investigated the effects of manganese intoxication on motor and non-motor parkinsonian-like deficits such as locomotor activity, motor coordination, anxiety and “depressive-like” behaviors. Then, we studied the impact of this intoxication on the neuronal activity, the globus pallidus (GP) and subthalamic nucleus (STN). At the end of experiments, post-mortem tissue level of the three monoamines (dopamine, norepinephrine and serotonin) has been determined. The experiments were carried out in adult Sprague-Dawley rats, daily treated with MnCl<sub>2</sub>
(10 mg/kg/, i.p.) for 5 weeks. We show that manganese progressively reduced locomotor activity as well as motor coordination in parallel with the manifestation of anxiety and “depressive-like” behaviors. Electrophysiological results show that, while majority of GP and STN neurons discharged regularly in controls, manganese increased the number of GP and STN neurons discharging irregularly and/or with bursts. Biochemical results show that manganese significantly decreased tissue levels of norepinephrine and serotonin with increased metabolism of dopamine in the striatum. Our data provide evidence that manganese intoxication is associated with impaired neurotransmission of monoaminergic systems, which is at the origin of changes in basal ganglia neuronal activity and the manifestation of motor and non-motor deficits similar to those observed in atypical Parkinsonism.</p>
</abstract>
<funding-group><funding-statement>This study was supported by the “Université Bordeaux Segalen” and exchange grants of the “Groupement de Recherche International” (GDRI N198, CNRS & INSERM France, and CNRST Morocco), Egide-Volubilis N° 20565ZM, CNRS-CNRST Convention Adivmar 22614 and NEUROMED. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><page-count count="11"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>France</li>
<li>Maroc</li>
</country>
<region><li>Aquitaine</li>
<li>Nouvelle-Aquitaine</li>
<li>Rabat-Salé-Kénitra</li>
</region>
<settlement><li>Bordeaux</li>
<li>Rabat</li>
</settlement>
</list>
<tree><country name="France"><region name="Nouvelle-Aquitaine"><name sortKey="Bouabid, Safa" sort="Bouabid, Safa" uniqKey="Bouabid S" first="Safa" last="Bouabid">Safa Bouabid</name>
</region>
<name sortKey="Benazzouz, Abdelhamid" sort="Benazzouz, Abdelhamid" uniqKey="Benazzouz A" first="Abdelhamid" last="Benazzouz">Abdelhamid Benazzouz</name>
<name sortKey="Benazzouz, Abdelhamid" sort="Benazzouz, Abdelhamid" uniqKey="Benazzouz A" first="Abdelhamid" last="Benazzouz">Abdelhamid Benazzouz</name>
<name sortKey="Bouabid, Safa" sort="Bouabid, Safa" uniqKey="Bouabid S" first="Safa" last="Bouabid">Safa Bouabid</name>
<name sortKey="De Deurwaerdere, Philippe" sort="De Deurwaerdere, Philippe" uniqKey="De Deurwaerdere P" first="Philippe" last="De Deurwaerdère">Philippe De Deurwaerdère</name>
<name sortKey="De Deurwaerdere, Philippe" sort="De Deurwaerdere, Philippe" uniqKey="De Deurwaerdere P" first="Philippe" last="De Deurwaerdère">Philippe De Deurwaerdère</name>
<name sortKey="Delaville, Claire" sort="Delaville, Claire" uniqKey="Delaville C" first="Claire" last="Delaville">Claire Delaville</name>
<name sortKey="Delaville, Claire" sort="Delaville, Claire" uniqKey="Delaville C" first="Claire" last="Delaville">Claire Delaville</name>
</country>
<country name="Maroc"><region name="Rabat-Salé-Kénitra"><name sortKey="Bouabid, Safa" sort="Bouabid, Safa" uniqKey="Bouabid S" first="Safa" last="Bouabid">Safa Bouabid</name>
</region>
<name sortKey="Lakhdar Ghazal, Nouria" sort="Lakhdar Ghazal, Nouria" uniqKey="Lakhdar Ghazal N" first="Nouria" last="Lakhdar-Ghazal">Nouria Lakhdar-Ghazal</name>
</country>
</tree>
</affiliations>
</record>
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