Rapamycin, by Inhibiting mTORC1 Signaling, Prevents the Loss of Striatal Bidirectional Synaptic Plasticity in a Rat Model of L-DOPA-Induced Dyskinesia

Levodopa (L-DOPA) treatment is the main gold-standard therapy for Parkinson’s disease (PD). Besides good antiparkinsonian effects, prolonged use of this drug is associated to the development of involuntary movements known as L-DOPA-induced dyskinesia (LID). LID is linked to a sensitization of dopami...

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Veröffentlicht in:	Frontiers in aging neuroscience Jg. 12; S. 230
Hauptverfasser:	Calabrese, Valeria, Di Maio, Anna, Marino, Gioia, Cardinale, Antonella, Natale, Giuseppina, De Rosa, Arianna, Campanelli, Federica, Mancini, Maria, Napolitano, Francesco, Avallone, Luigi, Calabresi, Paolo, Usiello, Alessandro, Ghiglieri, Veronica, Picconi, Barbara
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	Lausanne Frontiers Research Foundation 11.08.2020 Frontiers Media S.A
Schlagworte:	Aging Animal models Basal ganglia Behavior Behavioral plasticity Caudate-putamen Central nervous system diseases DARPP-32 protein depotentiation Dihydroxyphenylalanine Dopamine D1 receptors dorsolateral striatum Dyskinesia Experiments Extracellular signal-regulated kinase functional plasticity Glutamate receptors Glutamic acid receptors (ionotropic) Kinases Laboratories Levodopa levodopa-induced dyskinesia Movement disorders N-Methyl-D-aspartic acid receptors Neostriatum Neurodegenerative diseases Neuroscience Neurosciences Older people Parkinson's disease Phosphorylation Protein kinase A Proteins Rapamycin Rodents Signal transduction Surgery Synapses Synaptic plasticity TOR protein α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors
ISSN:	1663-4365, 1663-4365
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Abstract	Levodopa (L-DOPA) treatment is the main gold-standard therapy for Parkinson’s disease (PD). Besides good antiparkinsonian effects, prolonged use of this drug is associated to the development of involuntary movements known as L-DOPA-induced dyskinesia (LID). LID is linked to a sensitization of dopamine (DA) D1 receptors located on spiny projection neurons (SPNs) of the dorsal striatum. Several evidences have shown that the emergence of LID can be related to striatal D1/cAMP/PKA/DARPP-32 and extracellular signal-regulated kinases (ERK1/2) pathway overactivation associated to aberrant N-methyl-D-aspartate (NMDA) receptor function. In addition, within striatum, ERK1/2 is also able to modulate in a D1R-dependent manner the activity of the mammalian target of Rapamycin complex 1 (mTORC1) pathway under DA depletion and L-DOPA therapy. Consistently, increased mTORC1 signaling appears during chronic administration of L-DOPA and shows a high correlation with the severity of dyskinesia. Furthermore, the abnormal activation of the D1/PKA/DARPP-32 cascade is paralleled by increased phosphorylation of the GluA1 subunit of the AMPA receptor at the PKA Ser845 site. The GluA1 promotes excitatory AMPA receptor-mediated transmission and may be implicated in the alterations found at the corticostriatal synapses of dyskinetic animals. In our study, we investigated the role of mTORC1 pathway activation in modulating bidirectional striatal synaptic plasticity in L-DOPA treated parkinsonian rats. Inhibition of mTORC1 by co-administration of Rapamycin to L-DOPA, was able to limit the magnitude of LID expression, accounting for a therapeutic effect of this drug. In particular, behavioral data showed that in L-DOPA-treated rats, Rapamycin administration induced a selective decrease of distinct components of abnormal involuntary movements (i.e. axial and orolingual dyskinesia). Furthermore, ex vivo patch clamp and intracellular recordings of SPNs revealed that pharmacological inhibition of mTORC1 also resulted associated to a physiological bidirectional plasticity, when compared to dyskinetic rats treated with L-DOPA alone. This study uncovers the important role of mTORC1 inhibition to prevent the loss of striatal bidirectional plasticity under chronic L-DOPA treatment in rodent models of PD.
AbstractList	Levodopa (L-DOPA) treatment is the main gold-standard therapy for Parkinson disease (PD). Besides good antiparkinsonian effects, prolonged use of this drug is associated to the development of involuntary movements known as L-DOPA-induced dyskinesia (LID). L-DOPA-induced dyskinesia is linked to a sensitization of dopamine (DA) D1 receptors located on spiny projection neurons (SPNs) of the dorsal striatum. Several evidences have shown that the emergence of LID can be related to striatal D1/cAMP/PKA/DARPP-32 and extracellular signal-regulated kinases (ERK1/2) pathway overactivation associated to aberrant N-methyl-d-aspartate (NMDA) receptor function. In addition, within striatum, ERK1/2 is also able to modulate in a D1 receptor-dependent manner the activity of the mammalian target of rapamycin complex 1 (mTORC1) pathway under DA depletion and L-DOPA therapy. Consistently, increased mTORC1 signaling appears during chronic administration of L-DOPA and shows a high correlation with the severity of dyskinesia. Furthermore, the abnormal activation of the D1/PKA/DARPP-32 cascade is paralleled by increased phosphorylation of the GluA1 subunit of the α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor at the PKA Ser845 site. The GluA1 promotes excitatory AMPA receptor-mediated transmission and may be implicated in the alterations found at the corticostriatal synapses of dyskinetic animals. In our study, we investigated the role of mTORC1 pathway activation in modulating bidirectional striatal synaptic plasticity in L-DOPA-treated parkinsonian rats. Inhibition of mTORC1 by coadministration of rapamycin to L-DOPA was able to limit the magnitude of LID expression, accounting for a therapeutic effect of this drug. In particular, behavioral data showed that, in L-DOPA-treated rats, rapamycin administration induced a selective decrease of distinct components of abnormal involuntary movements (i.e., axial and orolingual dyskinesia). Furthermore, ex vivo patch clamp and intracellular recordings of SPNs revealed that pharmacological inhibition of mTORC1 also resulted associated with a physiological bidirectional plasticity, when compared to dyskinetic rats treated with L-DOPA alone. This study uncovers the important role of mTORC1 inhibition to prevent the loss of striatal bidirectional plasticity under chronic L-DOPA treatment in rodent models of PD. Levodopa (L-DOPA) treatment is the main gold-standard therapy for Parkinson disease (PD). Besides good antiparkinsonian effects, prolonged use of this drug is associated to the development of involuntary movements known as L-DOPA-induced dyskinesia (LID). L-DOPA-induced dyskinesia is linked to a sensitization of dopamine (DA) D1 receptors located on spiny projection neurons (SPNs) of the dorsal striatum. Several evidences have shown that the emergence of LID can be related to striatal D1/cAMP/PKA/DARPP-32 and extracellular signal-regulated kinases (ERK1/2) pathway overactivation associated to aberrant N-methyl-d-aspartate (NMDA) receptor function. In addition, within striatum, ERK1/2 is also able to modulate in a D1 receptor-dependent manner the activity of the mammalian target of rapamycin complex 1 (mTORC1) pathway under DA depletion and L-DOPA therapy. Consistently, increased mTORC1 signaling appears during chronic administration of L-DOPA and shows a high correlation with the severity of dyskinesia. Furthermore, the abnormal activation of the D1/PKA/DARPP-32 cascade is paralleled by increased phosphorylation of the GluA1 subunit of the α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor at the PKA Ser845 site. The GluA1 promotes excitatory AMPA receptor-mediated transmission and may be implicated in the alterations found at the corticostriatal synapses of dyskinetic animals. In our study, we investigated the role of mTORC1 pathway activation in modulating bidirectional striatal synaptic plasticity in L-DOPA-treated parkinsonian rats. Inhibition of mTORC1 by coadministration of rapamycin to L-DOPA was able to limit the magnitude of LID expression, accounting for a therapeutic effect of this drug. In particular, behavioral data showed that, in L-DOPA-treated rats, rapamycin administration induced a selective decrease of distinct components of abnormal involuntary movements (i.e., axial and orolingual dyskinesia). Furthermore, ex vivo patch clamp and intracellular recordings of SPNs revealed that pharmacological inhibition of mTORC1 also resulted associated with a physiological bidirectional plasticity, when compared to dyskinetic rats treated with L-DOPA alone. This study uncovers the important role of mTORC1 inhibition to prevent the loss of striatal bidirectional plasticity under chronic L-DOPA treatment in rodent models of PD.Levodopa (L-DOPA) treatment is the main gold-standard therapy for Parkinson disease (PD). Besides good antiparkinsonian effects, prolonged use of this drug is associated to the development of involuntary movements known as L-DOPA-induced dyskinesia (LID). L-DOPA-induced dyskinesia is linked to a sensitization of dopamine (DA) D1 receptors located on spiny projection neurons (SPNs) of the dorsal striatum. Several evidences have shown that the emergence of LID can be related to striatal D1/cAMP/PKA/DARPP-32 and extracellular signal-regulated kinases (ERK1/2) pathway overactivation associated to aberrant N-methyl-d-aspartate (NMDA) receptor function. In addition, within striatum, ERK1/2 is also able to modulate in a D1 receptor-dependent manner the activity of the mammalian target of rapamycin complex 1 (mTORC1) pathway under DA depletion and L-DOPA therapy. Consistently, increased mTORC1 signaling appears during chronic administration of L-DOPA and shows a high correlation with the severity of dyskinesia. Furthermore, the abnormal activation of the D1/PKA/DARPP-32 cascade is paralleled by increased phosphorylation of the GluA1 subunit of the α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor at the PKA Ser845 site. The GluA1 promotes excitatory AMPA receptor-mediated transmission and may be implicated in the alterations found at the corticostriatal synapses of dyskinetic animals. In our study, we investigated the role of mTORC1 pathway activation in modulating bidirectional striatal synaptic plasticity in L-DOPA-treated parkinsonian rats. Inhibition of mTORC1 by coadministration of rapamycin to L-DOPA was able to limit the magnitude of LID expression, accounting for a therapeutic effect of this drug. In particular, behavioral data showed that, in L-DOPA-treated rats, rapamycin administration induced a selective decrease of distinct components of abnormal involuntary movements (i.e., axial and orolingual dyskinesia). Furthermore, ex vivo patch clamp and intracellular recordings of SPNs revealed that pharmacological inhibition of mTORC1 also resulted associated with a physiological bidirectional plasticity, when compared to dyskinetic rats treated with L-DOPA alone. This study uncovers the important role of mTORC1 inhibition to prevent the loss of striatal bidirectional plasticity under chronic L-DOPA treatment in rodent models of PD. Levodopa (L-DOPA) treatment is the main gold-standard therapy for Parkinson’s disease (PD). Besides good antiparkinsonian effects, prolonged use of this drug is associated to the development of involuntary movements known as L-DOPA-induced dyskinesia (LID). LID is linked to a sensitization of dopamine (DA) D1 receptors located on spiny projection neurons (SPNs) of the dorsal striatum. Several evidences have shown that the emergence of LID can be related to striatal D1/cAMP/PKA/DARPP-32 and extracellular signal-regulated kinases (ERK1/2) pathway overactivation associated to aberrant N-methyl-D-aspartate (NMDA) receptor function. In addition, within striatum, ERK1/2 is also able to modulate in a D1R-dependent manner the activity of the mammalian target of Rapamycin complex 1 (mTORC1) pathway under DA depletion and L-DOPA therapy. Consistently, increased mTORC1 signaling appears during chronic administration of L-DOPA and shows a high correlation with the severity of dyskinesia. Furthermore, the abnormal activation of the D1/PKA/DARPP-32 cascade is paralleled by increased phosphorylation of the GluA1 subunit of the AMPA receptor at the PKA Ser845 site. The GluA1 promotes excitatory AMPA receptor-mediated transmission and may be implicated in the alterations found at the corticostriatal synapses of dyskinetic animals. In our study, we investigated the role of mTORC1 pathway activation in modulating bidirectional striatal synaptic plasticity in L-DOPA treated parkinsonian rats. Inhibition of mTORC1 by co-administration of Rapamycin to L-DOPA, was able to limit the magnitude of LID expression, accounting for a therapeutic effect of this drug. In particular, behavioral data showed that in L-DOPA-treated rats, Rapamycin administration induced a selective decrease of distinct components of abnormal involuntary movements (i.e. axial and orolingual dyskinesia). Furthermore, ex vivo patch clamp and intracellular recordings of SPNs revealed that pharmacological inhibition of mTORC1 also resulted associated to a physiological bidirectional plasticity, when compared to dyskinetic rats treated with L-DOPA alone. This study uncovers the important role of mTORC1 inhibition to prevent the loss of striatal bidirectional plasticity under chronic L-DOPA treatment in rodent models of PD.
Author	Calabresi, Paolo Di Maio, Anna Marino, Gioia De Rosa, Arianna Natale, Giuseppina Usiello, Alessandro Picconi, Barbara Calabrese, Valeria Campanelli, Federica Avallone, Luigi Mancini, Maria Ghiglieri, Veronica Napolitano, Francesco Cardinale, Antonella
AuthorAffiliation	9 Department of Environmental, Biological and Pharmaceutical Sciences and Technologies (DISTABIF), University of Campania Luigi Vanvitelli , Caserta , Italy 4 Laboratory of Neurophysiology, IRCCS Santa Lucia Foundation , Rome , Italy 7 Neurologia, Fondazione Policlinico Universitario Agostino Gemelli IRCCS , Rome , Italy 10 Università Telematica San Raffaele , Rome , Italy 3 CEINGE Biotecnologie Avanzate , Naples , Italy 6 Department of Veterinary Medicine and Animal Productions, University of Naples Federico II , Naples , Italy 8 Dipartimento di Neuroscienze, Università Cattolica del Sacro Cuore , Rome , Italy 5 Department of Experimental Medicine, Sapienza University of Rome , Rome , Italy 1 Laboratory of Experimental Neurophysiology, IRCCS San Raffaele Pisana , Rome , Italy 2 Department of Medicine, University of Perugia , Perugia , Italy
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Copyright	2020. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Copyright © 2020 Calabrese, Di Maio, Marino, Cardinale, Natale, De Rosa, Campanelli, Mancini, Napolitano, Avallone, Calabresi, Usiello, Ghiglieri and Picconi. Copyright © 2020 Calabrese, Di Maio, Marino, Cardinale, Natale, De Rosa, Campanelli, Mancini, Napolitano, Avallone, Calabresi, Usiello, Ghiglieri and Picconi. 2020 Calabrese, Di Maio, Marino, Cardinale, Natale, De Rosa, Campanelli, Mancini, Napolitano, Avallone, Calabresi, Usiello, Ghiglieri and Picconi
Copyright_xml	– notice: 2020. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: Copyright © 2020 Calabrese, Di Maio, Marino, Cardinale, Natale, De Rosa, Campanelli, Mancini, Napolitano, Avallone, Calabresi, Usiello, Ghiglieri and Picconi. – notice: Copyright © 2020 Calabrese, Di Maio, Marino, Cardinale, Natale, De Rosa, Campanelli, Mancini, Napolitano, Avallone, Calabresi, Usiello, Ghiglieri and Picconi. 2020 Calabrese, Di Maio, Marino, Cardinale, Natale, De Rosa, Campanelli, Mancini, Napolitano, Avallone, Calabresi, Usiello, Ghiglieri and Picconi
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors have contributed equally to this work Edited by: Nicola Simola, University of Cagliari, Italy Reviewed by: Denis Hervé, Institut National de la Santé et de la Recherche Médicale (INSERM), France; Karima Chergui, Karolinska Institutet (KI), Sweden; Charles K. Meshul, VA Medical Center/Portland, United States
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PublicationCentury	2000
PublicationDate	2020-08-11
PublicationDateYYYYMMDD	2020-08-11
PublicationDate_xml	– month: 08 year: 2020 text: 2020-08-11 day: 11
PublicationDecade	2020
PublicationPlace	Lausanne
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PublicationTitle	Frontiers in aging neuroscience
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Publisher	Frontiers Research Foundation Frontiers Media S.A
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Snippet	Levodopa (L-DOPA) treatment is the main gold-standard therapy for Parkinson’s disease (PD). Besides good antiparkinsonian effects, prolonged use of this drug... Levodopa (L-DOPA) treatment is the main gold-standard therapy for Parkinson disease (PD). Besides good antiparkinsonian effects, prolonged use of this drug is...
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SubjectTerms	Aging Animal models Basal ganglia Behavior Behavioral plasticity Caudate-putamen Central nervous system diseases DARPP-32 protein depotentiation Dihydroxyphenylalanine Dopamine D1 receptors dorsolateral striatum Dyskinesia Experiments Extracellular signal-regulated kinase functional plasticity Glutamate receptors Glutamic acid receptors (ionotropic) Kinases Laboratories Levodopa levodopa-induced dyskinesia Movement disorders N-Methyl-D-aspartic acid receptors Neostriatum Neurodegenerative diseases Neuroscience Neurosciences Older people Parkinson's disease Phosphorylation Protein kinase A Proteins Rapamycin Rodents Signal transduction Surgery Synapses Synaptic plasticity TOR protein α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors
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Title	Rapamycin, by Inhibiting mTORC1 Signaling, Prevents the Loss of Striatal Bidirectional Synaptic Plasticity in a Rat Model of L-DOPA-Induced Dyskinesia
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