Treadmill exercise reverses dendritic spine loss in direct and indirect striatal medium spiny neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) mouse model of Parkinson's disease
Exercise has been shown to be beneficial for Parkinson's disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia function and modifies disease progression. Dopamine (DA) depletion leads to loss of dendritic spines within the caudate nucleus and put...
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| Published in | Neurobiology of disease Vol. 63; pp. 201 - 209 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.03.2014
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0969-9961 1095-953X 1095-953X |
| DOI | 10.1016/j.nbd.2013.11.017 |
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| Abstract | Exercise has been shown to be beneficial for Parkinson's disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia function and modifies disease progression. Dopamine (DA) depletion leads to loss of dendritic spines within the caudate nucleus and putamen (striatum) in PD and its animal models and contributes to motor impairments. Striatal medium spiny neurons (MSNs) can be delineated into two populations, the dopamine D1 receptor (DA-D1R)-containing MSNs of the direct pathway and dopamine D2 receptor (DA-D2R)-containing MSNs of the indirect pathway. There is evidence to suggest that the DA-D2R-indirect pathway MSNs may be preferentially affected after DA-depletion with a predominate loss of dendritic spine density when compared to MSNs of the DA-D1R-direct pathway in rodents; however, others have reported that both pathways may be affected in primates. The purpose of this study was to investigate the effects of intensive exercise on dendritic spine density and arborization in MSNs of these two pathways in the MPTP mouse model of PD. We found that MPTP led to a decrease in dendritic spine density in both DA-D1R- and DA-D2R-containing MSNs and 30days of intensive treadmill exercise led to increased dendritic spine density and arborization in MSNs of both pathways. In addition, exercise increased the expression of synaptic proteins PSD-95 and synaptophysin. Taken together these findings support the potential effect of exercise in modifying synaptic connectivity within the DA-depleted striatum and in modifying disease progression in individuals with PD.
•MPTP leads to reduced spine density in MSNs in both pathways of the basal ganglia.•Treadmill exercise increases spine density in MSNs of both pathways in MPTP mice.•Exercise increases dendritic arborization of striatal MSNs in MPTP mice.•MPTP induced DA depletion leads to selective pruning of DA-D2R-containing MSNs.•Exercise increases expression of proteins PSD-95 and synaptophysin in MPTP mice. |
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| AbstractList | Exercise has been shown to be beneficial for Parkinson's disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia function and modifies disease progression. Dopamine (DA) depletion leads to loss of dendritic spines within the caudate nucleus and putamen (striatum) in PD and its animal models and contributes to motor impairments. Striatal medium spiny neurons (MSNs) can be delineated into two populations, the dopamine D1 receptor (DA-D1R)-containing MSNs of the direct pathway and dopamine D2 receptor (DA-D2R)-containing MSNs of the indirect pathway. There is evidence to suggest that the DA-D2R-indirect pathway MSNs may be preferentially affected after DA-depletion with a predominate loss of dendritic spine density when compared to MSNs of the DA-D1R-direct pathway in rodents; however, others have reported that both pathways may be affected in primates. The purpose of this study was to investigate the effects of intensive exercise on dendritic spine density and arborization in MSNs of these two pathways in the MPTP mouse model of PD. We found that MPTP led to a decrease in dendritic spine density in both DA-D1R- and DA-D2R-containing MSNs and 30days of intensive treadmill exercise led to increased dendritic spine density and arborization in MSNs of both pathways. In addition, exercise increased the expression of synaptic proteins PSD-95 and synaptophysin. Taken together these findings support the potential effect of exercise in modifying synaptic connectivity within the DA-depleted striatum and in modifying disease progression in individuals with PD.
•MPTP leads to reduced spine density in MSNs in both pathways of the basal ganglia.•Treadmill exercise increases spine density in MSNs of both pathways in MPTP mice.•Exercise increases dendritic arborization of striatal MSNs in MPTP mice.•MPTP induced DA depletion leads to selective pruning of DA-D2R-containing MSNs.•Exercise increases expression of proteins PSD-95 and synaptophysin in MPTP mice. Exercise has been shown to be beneficial for Parkinson’s disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia function and modifies disease progression. Dopamine (DA) depletion leads to loss of dendritic spines within the caudate nucleus and putamen (striatum) in PD and its animal models and contributes to motor impairments. Striatal medium spiny neurons (MSNs) can be delineated into two populations, the dopamine D 1 receptor (DA-D 1 R)-containing MSNs of the direct pathway and dopamine D 2 receptor (DA-D 2 R)-containing MSNs of the indirect pathway. There is evidence to suggest that the DA-D 2 R-indirect pathway MSNs may be preferentially affected after DA-depletion with a predominate loss of dendritic spine density when compared to MSNs of the DA-D 1 R-direct pathway in rodents; however, others have reported that both pathways may be affected in primates. The purpose of this study was to investigate the effects of intensive exercise on dendritic spine density and arborization in MSNs of these two pathways in the MPTP mouse model of PD. We found that MPTP led to a decrease in dendritic spine density in both DA-D 1 R-and DA-D 2 R-containing MSNs and 30 days of intensive treadmill exercise led to increased dendritic spine density and arborization in MSNs of both pathways. In addition, exercise increased the expression of synaptic proteins PSD-95 and synaptophysin. Taken together these findings support the potential effect of exercise in modifying synaptic connectivity within the DA-depleted striatum and in modifying disease progression in individuals with PD. Exercise has been shown to be beneficial for Parkinson's disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia function and modifies disease progression. Dopamine (DA) depletion leads to loss of dendritic spines within the caudate nucleus and putamen (striatum) in PD and its animal models and contributes to motor impairments. Striatal medium spiny neurons (MSNs) can be delineated into two populations, the dopamine D1 receptor (DA-D1R)-containing MSNs of the direct pathway and dopamine D2 receptor (DA-D2R)-containing MSNs of the indirect pathway. There is evidence to suggest that the DA-D2R-indirect pathway MSNs may be preferentially affected after DA-depletion with a predominate loss of dendritic spine density when compared to MSNs of the DA-D1R-direct pathway in rodents; however, others have reported that both pathways may be affected in primates. The purpose of this study was to investigate the effects of intensive exercise on dendritic spine density and arborization in MSNs of these two pathways in the MPTP mouse model of PD. We found that MPTP led to a decrease in dendritic spine density in both DA-D1R- and DA-D2R-containing MSNs and 30 days of intensive treadmill exercise led to increased dendritic spine density and arborization in MSNs of both pathways. In addition, exercise increased the expression of synaptic proteins PSD-95 and synaptophysin. Taken together these findings support the potential effect of exercise in modifying synaptic connectivity within the DA-depleted striatum and in modifying disease progression in individuals with PD. Exercise has been shown to be beneficial for Parkinson's disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia function and modifies disease progression. Dopamine (DA) depletion leads to loss of dendritic spines within the caudate nucleus and putamen (striatum) in PD and its animal models and contributes to motor impairments. Striatal medium spiny neurons (MSNs) can be delineated into two populations, the dopamine D1 receptor (DA-D1R)-containing MSNs of the direct pathway and dopamine D2 receptor (DA-D2R)-containing MSNs of the indirect pathway. There is evidence to suggest that the DA-D2R-indirect pathway MSNs may be preferentially affected after DA-depletion with a predominate loss of dendritic spine density when compared to MSNs of the DA-D1R-direct pathway in rodents; however, others have reported that both pathways may be affected in primates. The purpose of this study was to investigate the effects of intensive exercise on dendritic spine density and arborization in MSNs of these two pathways in the MPTP mouse model of PD. We found that MPTP led to a decrease in dendritic spine density in both DA-D1R- and DA-D2R-containing MSNs and 30 days of intensive treadmill exercise led to increased dendritic spine density and arborization in MSNs of both pathways. In addition, exercise increased the expression of synaptic proteins PSD-95 and synaptophysin. Taken together these findings support the potential effect of exercise in modifying synaptic connectivity within the DA-depleted striatum and in modifying disease progression in individuals with PD.Exercise has been shown to be beneficial for Parkinson's disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia function and modifies disease progression. Dopamine (DA) depletion leads to loss of dendritic spines within the caudate nucleus and putamen (striatum) in PD and its animal models and contributes to motor impairments. Striatal medium spiny neurons (MSNs) can be delineated into two populations, the dopamine D1 receptor (DA-D1R)-containing MSNs of the direct pathway and dopamine D2 receptor (DA-D2R)-containing MSNs of the indirect pathway. There is evidence to suggest that the DA-D2R-indirect pathway MSNs may be preferentially affected after DA-depletion with a predominate loss of dendritic spine density when compared to MSNs of the DA-D1R-direct pathway in rodents; however, others have reported that both pathways may be affected in primates. The purpose of this study was to investigate the effects of intensive exercise on dendritic spine density and arborization in MSNs of these two pathways in the MPTP mouse model of PD. We found that MPTP led to a decrease in dendritic spine density in both DA-D1R- and DA-D2R-containing MSNs and 30 days of intensive treadmill exercise led to increased dendritic spine density and arborization in MSNs of both pathways. In addition, exercise increased the expression of synaptic proteins PSD-95 and synaptophysin. Taken together these findings support the potential effect of exercise in modifying synaptic connectivity within the DA-depleted striatum and in modifying disease progression in individuals with PD. Abstract Exercise has been shown to be beneficial for Parkinson's disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia function and modifies disease progression. Dopamine (DA) depletion leads to loss of dendritic spines within the caudate nucleus and putamen (striatum) in PD and its animal models and contributes to motor impairments. Striatal medium spiny neurons (MSNs) can be delineated into two populations, the dopamine D1 receptor (DA-D1 R)-containing MSNs of the direct pathway and dopamine D2 receptor (DA-D2 R)-containing MSNs of the indirect pathway. There is evidence to suggest that the DA-D2 R-indirect pathway MSNs may be preferentially affected after DA-depletion with a predominate loss of dendritic spine density when compared to MSNs of the DA-D1 R-direct pathway in rodents; however, others have reported that both pathways may be affected in primates. The purpose of this study was to investigate the effects of intensive exercise on dendritic spine density and arborization in MSNs of these two pathways in the MPTP mouse model of PD. We found that MPTP led to a decrease in dendritic spine density in both DA-D1 R- and DA-D2 R-containing MSNs and 30 days of intensive treadmill exercise led to increased dendritic spine density and arborization in MSNs of both pathways. In addition, exercise increased the expression of synaptic proteins PSD-95 and synaptophysin. Taken together these findings support the potential effect of exercise in modifying synaptic connectivity within the DA-depleted striatum and in modifying disease progression in individuals with PD. Exercise has been shown to be beneficial for Parkinson's disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia function and modifies disease progression. Dopamine (DA) depletion leads to loss of dendritic spines within the caudate nucleus and putamen (striatum) in PD and its animal models and contributes to motor impairments. Striatal medium spiny neurons (MSNs) can be delineated into two populations, the dopamine D1 receptor (DA-D1R)-containing MSNs of the direct pathway and dopamine D2 receptor (DA-D2R)-containing MSNs of the indirect pathway. There is evidence to suggest that the DA-D2R-indirect pathway MSNs may be preferentially affected after DA-depletion with a predominate loss of dendritic spine density when compared to MSNs of the DA-D1R-direct pathway in rodents; however, others have reported that both pathways may be affected in primates. The purpose of this study was to investigate the effects of intensive exercise on dendritic spine density and arborization in MSNs of these two pathways in the MPTP mouse model of PD. We found that MPTP led to a decrease in dendritic spine density in both DA-D1R- and DA-D2R-containing MSNs and 30 days of intensive treadmill exercise led to increased dendritic spine density and arborization in MSNs of both pathways. In addition, exercise increased the expression of synaptic proteins PSD-95 and synaptophysin. Taken together these findings support the potential effect of exercise in modifying synaptic connectivity within the DA-depleted striatum and in modifying disease progression in individuals with PD. |
| Author | Akopian, Garnik K. Jakowec, Michael W. Leyshon, Brian J. Petzinger, Giselle M. Vučković, Marta G. Hoffman, Matilde V. Walsh, John P. Toy, William A. |
| AuthorAffiliation | 2 The George and MaryLou Boone Center for Parkinson’s Disease Research, Andrus Center for Gerontology, University of Southern California, Los Angeles, CA, 90033 3 Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA, 90033 1 The George and MaryLou Boone Center for Parkinson’s Disease Research, Department of Neurology, University of Southern California, Los Angeles, CA, 90033 |
| AuthorAffiliation_xml | – name: 2 The George and MaryLou Boone Center for Parkinson’s Disease Research, Andrus Center for Gerontology, University of Southern California, Los Angeles, CA, 90033 – name: 3 Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA, 90033 – name: 1 The George and MaryLou Boone Center for Parkinson’s Disease Research, Department of Neurology, University of Southern California, Los Angeles, CA, 90033 |
| Author_xml | – sequence: 1 givenname: William A. surname: Toy fullname: Toy, William A. email: wtoy@usc.edu organization: The George and MaryLou Boone Center for Parkinson's Disease Research, Department of Neurology, University of Southern California, Los Angeles, CA 90033, USA – sequence: 2 givenname: Giselle M. surname: Petzinger fullname: Petzinger, Giselle M. organization: The George and MaryLou Boone Center for Parkinson's Disease Research, Department of Neurology, University of Southern California, Los Angeles, CA 90033, USA – sequence: 3 givenname: Brian J. surname: Leyshon fullname: Leyshon, Brian J. organization: The George and MaryLou Boone Center for Parkinson's Disease Research, Department of Neurology, University of Southern California, Los Angeles, CA 90033, USA – sequence: 4 givenname: Garnik K. surname: Akopian fullname: Akopian, Garnik K. organization: The George and MaryLou Boone Center for Parkinson's Disease Research, Andrus Center for Gerontology, University of Southern California, Los Angeles, CA 90033, USA – sequence: 5 givenname: John P. surname: Walsh fullname: Walsh, John P. organization: The George and MaryLou Boone Center for Parkinson's Disease Research, Andrus Center for Gerontology, University of Southern California, Los Angeles, CA 90033, USA – sequence: 6 givenname: Matilde V. surname: Hoffman fullname: Hoffman, Matilde V. organization: The George and MaryLou Boone Center for Parkinson's Disease Research, Department of Neurology, University of Southern California, Los Angeles, CA 90033, USA – sequence: 7 givenname: Marta G. surname: Vučković fullname: Vučković, Marta G. organization: The George and MaryLou Boone Center for Parkinson's Disease Research, Department of Neurology, University of Southern California, Los Angeles, CA 90033, USA – sequence: 8 givenname: Michael W. surname: Jakowec fullname: Jakowec, Michael W. organization: The George and MaryLou Boone Center for Parkinson's Disease Research, Department of Neurology, University of Southern California, Los Angeles, CA 90033, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24316165$$D View this record in MEDLINE/PubMed |
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| Keywords | Neuroplasticity GFP Striatum Parkinson's Basal ganglia Dopamine Synaptogenesis |
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| Snippet | Exercise has been shown to be beneficial for Parkinson's disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia... Abstract Exercise has been shown to be beneficial for Parkinson's disease (PD). A major interest in our lab has been to investigate how exercise modulates... Exercise has been shown to be beneficial for Parkinson’s disease (PD). A major interest in our lab has been to investigate how exercise modulates basal ganglia... |
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| SubjectTerms | Analysis of Variance Animals Basal ganglia Corpus Striatum - pathology Dendritic Spines - pathology Dendritic Spines - ultrastructure Disease Models, Animal Dopamine Exercise Test GFP Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Lysine - analogs & derivatives Male Mice Mice, Inbred C57BL Mice, Transgenic MPTP Poisoning - pathology MPTP Poisoning - rehabilitation Neurology Neurons - pathology Neurons - ultrastructure Neuroplasticity Parkinson's Physical Conditioning, Animal - methods Primates Receptors, Dopamine D2 - genetics Receptors, Dopamine D2 - metabolism Silver Staining Striatum Synaptogenesis Time Factors |
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| Title | Treadmill exercise reverses dendritic spine loss in direct and indirect striatal medium spiny neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) mouse model of Parkinson's disease |
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