Decreased Rhes mRNA levels in the brain of patients with Parkinson’s disease and MPTP-treated macaques
In rodent and human brains, the small GTP-binding protein Rhes is highly expressed in virtually all dopaminoceptive striatal GABAergic medium spiny neurons, as well as in large aspiny cholinergic interneurons, where it is thought to modulate dopamine-dependent signaling. Consistent with this knowled...
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| Published in | PloS one Vol. 12; no. 7; p. e0181677 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
25.07.2017
Public Library of Science (PLoS) |
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| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0181677 |
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| Abstract | In rodent and human brains, the small GTP-binding protein Rhes is highly expressed in virtually all dopaminoceptive striatal GABAergic medium spiny neurons, as well as in large aspiny cholinergic interneurons, where it is thought to modulate dopamine-dependent signaling. Consistent with this knowledge, and considering that dopaminergic neurotransmission is altered in neurological and psychiatric disorders, here we sought to investigate whether Rhes mRNA expression is altered in brain regions of patients with Parkinson's disease (PD), Schizophrenia (SCZ), and Bipolar Disorder (BD), when compared to healthy controls (about 200 post-mortem samples). Moreover, we performed the same analysis in the putamen of non-human primate Macaca Mulatta, lesioned with the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Overall, our data indicated comparable Rhes mRNA levels in the brain of patients with SCZ and BD, and their respective healthy controls. In sharp contrast, the putamen of patients suffering from PD showed a significant 35% reduction of this transcript, compared to healthy subjects. Interestingly, in line with observations obtained in humans, we found 27% decrease in Rhes mRNA levels in the putamen of MPTP-treated primates. Based on the established inhibitory influence of Rhes on dopamine-related responses, we hypothesize that its striatal downregulation in PD patients and animal models of PD might represent an adaptive event of the dopaminergic system to functionally counteract the reduced nigrostriatal innervation. |
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| AbstractList | In rodent and human brains, the small GTP-binding protein Rhes is highly expressed in virtually all dopaminoceptive striatal GABAergic medium spiny neurons, as well as in large aspiny cholinergic interneurons, where it is thought to modulate dopamine-dependent signaling. Consistent with this knowledge, and considering that dopaminergic neurotransmission is altered in neurological and psychiatric disorders, here we sought to investigate whether Rhes mRNA expression is altered in brain regions of patients with Parkinson's disease (PD), Schizophrenia (SCZ), and Bipolar Disorder (BD), when compared to healthy controls (about 200 post-mortem samples). Moreover, we performed the same analysis in the putamen of non-human primate Macaca Mulatta, lesioned with the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Overall, our data indicated comparable Rhes mRNA levels in the brain of patients with SCZ and BD, and their respective healthy controls. In sharp contrast, the putamen of patients suffering from PD showed a significant 35% reduction of this transcript, compared to healthy subjects. Interestingly, in line with observations obtained in humans, we found 27% decrease in Rhes mRNA levels in the putamen of MPTP-treated primates. Based on the established inhibitory influence of Rhes on dopamine-related responses, we hypothesize that its striatal downregulation in PD patients and animal models of PD might represent an adaptive event of the dopaminergic system to functionally counteract the reduced nigrostriatal innervation. In rodent and human brains, the small GTP-binding protein Rhes is highly expressed in virtually all dopaminoceptive striatal GABAergic medium spiny neurons, as well as in large aspiny cholinergic interneurons, where it is thought to modulate dopamine-dependent signaling. Consistent with this knowledge, and considering that dopaminergic neurotransmission is altered in neurological and psychiatric disorders, here we sought to investigate whether Rhes mRNA expression is altered in brain regions of patients with Parkinson's disease (PD), Schizophrenia (SCZ), and Bipolar Disorder (BD), when compared to healthy controls (about 200 post-mortem samples). Moreover, we performed the same analysis in the putamen of non-human primate Macaca Mulatta, lesioned with the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Overall, our data indicated comparable Rhes mRNA levels in the brain of patients with SCZ and BD, and their respective healthy controls. In sharp contrast, the putamen of patients suffering from PD showed a significant 35% reduction of this transcript, compared to healthy subjects. Interestingly, in line with observations obtained in humans, we found 27% decrease in Rhes mRNA levels in the putamen of MPTP-treated primates. Based on the established inhibitory influence of Rhes on dopamine-related responses, we hypothesize that its striatal downregulation in PD patients and animal models of PD might represent an adaptive event of the dopaminergic system to functionally counteract the reduced nigrostriatal innervation.In rodent and human brains, the small GTP-binding protein Rhes is highly expressed in virtually all dopaminoceptive striatal GABAergic medium spiny neurons, as well as in large aspiny cholinergic interneurons, where it is thought to modulate dopamine-dependent signaling. Consistent with this knowledge, and considering that dopaminergic neurotransmission is altered in neurological and psychiatric disorders, here we sought to investigate whether Rhes mRNA expression is altered in brain regions of patients with Parkinson's disease (PD), Schizophrenia (SCZ), and Bipolar Disorder (BD), when compared to healthy controls (about 200 post-mortem samples). Moreover, we performed the same analysis in the putamen of non-human primate Macaca Mulatta, lesioned with the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Overall, our data indicated comparable Rhes mRNA levels in the brain of patients with SCZ and BD, and their respective healthy controls. In sharp contrast, the putamen of patients suffering from PD showed a significant 35% reduction of this transcript, compared to healthy subjects. Interestingly, in line with observations obtained in humans, we found 27% decrease in Rhes mRNA levels in the putamen of MPTP-treated primates. Based on the established inhibitory influence of Rhes on dopamine-related responses, we hypothesize that its striatal downregulation in PD patients and animal models of PD might represent an adaptive event of the dopaminergic system to functionally counteract the reduced nigrostriatal innervation. In rodent and human brains, the small GTP-binding protein Rhes is highly expressed in virtually all dopaminoceptive striatal GABAergic medium spiny neurons, as well as in large aspiny cholinergic interneurons, where it is thought to modulate dopamine-dependent signaling. Consistent with this knowledge, and considering that dopaminergic neurotransmission is altered in neurological and psychiatric disorders, here we sought to investigate whether Rhes mRNA expression is altered in brain regions of patients with Parkinson’s disease (PD), Schizophrenia (SCZ), and Bipolar Disorder (BD), when compared to healthy controls (about 200 post-mortem samples). Moreover, we performed the same analysis in the putamen of non-human primate Macaca Mulatta , lesioned with the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Overall, our data indicated comparable Rhes mRNA levels in the brain of patients with SCZ and BD, and their respective healthy controls. In sharp contrast, the putamen of patients suffering from PD showed a significant 35% reduction of this transcript, compared to healthy subjects. Interestingly, in line with observations obtained in humans, we found 27% decrease in Rhes mRNA levels in the putamen of MPTP-treated primates. Based on the established inhibitory influence of Rhes on dopamine-related responses, we hypothesize that its striatal downregulation in PD patients and animal models of PD might represent an adaptive event of the dopaminergic system to functionally counteract the reduced nigrostriatal innervation. |
| Audience | Academic |
| Author | Calabresi, Paolo Pasqualetti, Massimo Punzo, Daniela Morelli, Micaela Thiolat, Marie-Laure Booth Warren, Emily Migliarini, Sara Li, Qin Errico, Francesco Bezard, Erwan Konradi, Christine Usiello, Alessandro Vescovi, Angelo Luigi Napolitano, Francesco |
| AuthorAffiliation | 9 Centre National de la Recherche Scientifique Unité Mixte de Recherche 5293, Institut des Maladies Neurodégénératives, Bordeaux, France 14 Center for Neuroscience and Cognitive Systems, Istituto Italiano di Tecnologia, Rovereto, TN, Italy 11 Department of Medicine, University of Perugia and Clinica Neurologica, Santa Maria della Misericordia Hospital, Perugia, Italy 2 Department of Molecular Medicine and Medical Biotechnology, University of Naples Federico II, Naples, Italy Hudson Institute, AUSTRALIA 4 Department of Biology Unit of Cell and Developmental Biology, University of Pisa, Pisa, Italy 15 Neuroscience Institute, National Research Council (CNR), Pisa, Italy 12 National Research Council of Italy (CNR), Neuroscience Institute, Cagliari, Italy 3 Department of Pharmacology, Vanderbilt University, Nashville, TN, United States of America 13 Department of Biomedical Sciences, section of Neuropsychopharmacology, University of Cagliari, Cagliari, Italy 5 Department of Environmental, Biological |
| AuthorAffiliation_xml | – name: 15 Neuroscience Institute, National Research Council (CNR), Pisa, Italy – name: 10 IRCSS Casa Sollievo della Sofferenza, ISBReMIT-Institute for Stem Cell Biology, Regenerative Medicine and Innovative Therapies, San Giovanni Rotondo, Italy – name: 13 Department of Biomedical Sciences, section of Neuropsychopharmacology, University of Cagliari, Cagliari, Italy – name: 5 Department of Environmental, Biological and Pharmaceutical Sciences and Technologies, University of Campania, Luigi Vanvitelli, Italy – name: Hudson Institute, AUSTRALIA – name: 2 Department of Molecular Medicine and Medical Biotechnology, University of Naples Federico II, Naples, Italy – name: 3 Department of Pharmacology, Vanderbilt University, Nashville, TN, United States of America – name: 11 Department of Medicine, University of Perugia and Clinica Neurologica, Santa Maria della Misericordia Hospital, Perugia, Italy – name: 1 Ceinge Biotecnologie Avanzate, Naples, Italy – name: 14 Center for Neuroscience and Cognitive Systems, Istituto Italiano di Tecnologia, Rovereto, TN, Italy – name: 6 Motac Neuroscience, UK-M15 6WE, Manchester, United Kingdom – name: 7 Institute of Lab Animal Sciences, China Academy of Medical Sciences, Beijing, China – name: 4 Department of Biology Unit of Cell and Developmental Biology, University of Pisa, Pisa, Italy – name: 12 National Research Council of Italy (CNR), Neuroscience Institute, Cagliari, Italy – name: 9 Centre National de la Recherche Scientifique Unité Mixte de Recherche 5293, Institut des Maladies Neurodégénératives, Bordeaux, France – name: 8 Université de Bordeaux, Institut des Maladies Neurodégénératives,Bordeaux, France |
| Author_xml | – sequence: 1 givenname: Francesco surname: Napolitano fullname: Napolitano, Francesco – sequence: 2 givenname: Emily surname: Booth Warren fullname: Booth Warren, Emily – sequence: 3 givenname: Sara surname: Migliarini fullname: Migliarini, Sara – sequence: 4 givenname: Daniela surname: Punzo fullname: Punzo, Daniela – sequence: 5 givenname: Francesco surname: Errico fullname: Errico, Francesco – sequence: 6 givenname: Qin surname: Li fullname: Li, Qin – sequence: 7 givenname: Marie-Laure surname: Thiolat fullname: Thiolat, Marie-Laure – sequence: 8 givenname: Angelo Luigi surname: Vescovi fullname: Vescovi, Angelo Luigi – sequence: 9 givenname: Paolo surname: Calabresi fullname: Calabresi, Paolo – sequence: 10 givenname: Erwan surname: Bezard fullname: Bezard, Erwan – sequence: 11 givenname: Micaela surname: Morelli fullname: Morelli, Micaela – sequence: 12 givenname: Christine surname: Konradi fullname: Konradi, Christine – sequence: 13 givenname: Massimo surname: Pasqualetti fullname: Pasqualetti, Massimo – sequence: 14 givenname: Alessandro surname: Usiello fullname: Usiello, Alessandro |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28742811$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2017 Public Library of Science 2017 Napolitano et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2017 Napolitano et al 2017 Napolitano et al |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Competing Interests: Dr. Erwan Bezard and Qin Li are shareholders of Motac neuroscience Ltd. Motac neuroscience Ltd provided support in the form of dividends for authors, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. This does not alter our adherence to PLOS ONE policies on sharing data and materials. |
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| SubjectTerms | 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine - pharmacology Adaptive systems Aged Aged, 80 and over Animal models Animal sciences Animals Biology and life sciences Bipolar disorder Bipolar Disorder - metabolism Brain Brain Chemistry - drug effects Brain research Case-Control Studies Councils Development and progression Developmental biology Disorders Dopamine Dopamine receptors Dopaminergic mechanisms Female Gene expression Genetic aspects Genomes GTP-binding protein GTP-Binding Proteins - metabolism Health aspects Human performance Humans Innervation Interneurons Laboratory animals Macaca mulatta Male Medicine Medicine and Health Sciences Mental disorders Messenger RNA Middle Aged Monkeys & apes Movement disorders MPTP Neostriatum Neurodegenerative diseases Neurological diseases Neurons Neurosciences Neurotoxins Neurotransmission Parkinson disease Parkinson Disease - metabolism Parkinson's disease Patients Pharmaceutical sciences Primates Proteins Putamen Putamen - chemistry Putamen - metabolism RNA, Messenger - analysis RNA, Messenger - metabolism Rodents Schizophrenia Schizophrenia - metabolism Spiny neurons Transcription γ-Aminobutyric acid |
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| Title | Decreased Rhes mRNA levels in the brain of patients with Parkinson’s disease and MPTP-treated macaques |
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