Physical Activity Dynamically Regulates the Hippocampal Proteome along the Dorso-Ventral Axis

The hippocampus is central for higher cognition and emotions. In patients suffering from neuropsychiatric or neurodegenerative diseases, hippocampal signaling is altered causing cognitive defects. Thus, therapeutic approaches aim at improving cognition by targeting the hippocampus. Enhanced physical...

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Main Authors: Surina Frey, Rico Schieweck, Ignasi Forné, Axel Imhof, Tobias Straub, Bastian Popper, Michael A. Kiebler
Format: Article
Language:English
Published: MDPI AG 2020-05-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/10/3501
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author Surina Frey
Rico Schieweck
Ignasi Forné
Axel Imhof
Tobias Straub
Bastian Popper
Michael A. Kiebler
author_facet Surina Frey
Rico Schieweck
Ignasi Forné
Axel Imhof
Tobias Straub
Bastian Popper
Michael A. Kiebler
author_sort Surina Frey
collection DOAJ
description The hippocampus is central for higher cognition and emotions. In patients suffering from neuropsychiatric or neurodegenerative diseases, hippocampal signaling is altered causing cognitive defects. Thus, therapeutic approaches aim at improving cognition by targeting the hippocampus. Enhanced physical activity (EPA) improves cognition in rodents and humans. A systematic screen, however, for expression changes in the hippocampus along the dorso-ventral axis is missing, which is a prerequisite for understanding molecular mechanisms. Here, we exploited label free mass spectrometry to detect proteomic changes in the hippocampus of male mice upon voluntary wheel running. To identify regional differences, we examined dorsal and ventral CA1, CA3 and dentate gyrus hippocampal subregions. We found metabolic enzymes and actin binding proteins, such as RhoA, being upregulated in the hippocampus upon EPA suggesting a coordination between metabolism and cytoskeleton remodeling; two pathways essential for synaptic plasticity. Strikingly, dorsal and ventral hippocampal subregions respond differentially to EPA. Together, our results provide new insight into proteomic adaptations driven by physical activity in mice. In addition, our results suggest that dorsal and ventral hippocampus, as well as hippocampal subregions themselves, contribute differently to this process. Our study therefore provides an important resource for studying hippocampal subregion diversity in response to EPA.
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spelling doaj.art-185ff0b17ce044b8a686156e0d5c899b2023-11-20T00:34:15ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-05-012110350110.3390/ijms21103501Physical Activity Dynamically Regulates the Hippocampal Proteome along the Dorso-Ventral AxisSurina Frey0Rico Schieweck1Ignasi Forné2Axel Imhof3Tobias Straub4Bastian Popper5Michael A. Kiebler6Department for Cell Biology & Anatomy, Biomedical Center (BMC), Medical Faculty, Ludwig-Maximilians- University, 82152 Planegg-Martinsried, GermanyDepartment for Cell Biology & Anatomy, Biomedical Center (BMC), Medical Faculty, Ludwig-Maximilians- University, 82152 Planegg-Martinsried, GermanyDepartment for Molecular Biology (protein analysis unit), Biomedical Center (BMC), Ludwig-Maximilians-University, 82152 Planegg-Martinsried, GermanyDepartment for Molecular Biology (protein analysis unit), Biomedical Center (BMC), Ludwig-Maximilians-University, 82152 Planegg-Martinsried, GermanyDepartment for Molecular Biology (Core facility bioinformatics), Biomedical Center (BMC), Ludwig-Maximilians-University, 82152 Planegg-Martinsried, GermanyDepartment for Cell Biology & Anatomy, Biomedical Center (BMC), Medical Faculty, Ludwig-Maximilians- University, 82152 Planegg-Martinsried, GermanyDepartment for Cell Biology & Anatomy, Biomedical Center (BMC), Medical Faculty, Ludwig-Maximilians- University, 82152 Planegg-Martinsried, GermanyThe hippocampus is central for higher cognition and emotions. In patients suffering from neuropsychiatric or neurodegenerative diseases, hippocampal signaling is altered causing cognitive defects. Thus, therapeutic approaches aim at improving cognition by targeting the hippocampus. Enhanced physical activity (EPA) improves cognition in rodents and humans. A systematic screen, however, for expression changes in the hippocampus along the dorso-ventral axis is missing, which is a prerequisite for understanding molecular mechanisms. Here, we exploited label free mass spectrometry to detect proteomic changes in the hippocampus of male mice upon voluntary wheel running. To identify regional differences, we examined dorsal and ventral CA1, CA3 and dentate gyrus hippocampal subregions. We found metabolic enzymes and actin binding proteins, such as RhoA, being upregulated in the hippocampus upon EPA suggesting a coordination between metabolism and cytoskeleton remodeling; two pathways essential for synaptic plasticity. Strikingly, dorsal and ventral hippocampal subregions respond differentially to EPA. Together, our results provide new insight into proteomic adaptations driven by physical activity in mice. In addition, our results suggest that dorsal and ventral hippocampus, as well as hippocampal subregions themselves, contribute differently to this process. Our study therefore provides an important resource for studying hippocampal subregion diversity in response to EPA.https://www.mdpi.com/1422-0067/21/10/3501dorsal and ventral hippocampusenhanced physical activitymass spectrometryprotein expressionmetabolism
spellingShingle Surina Frey
Rico Schieweck
Ignasi Forné
Axel Imhof
Tobias Straub
Bastian Popper
Michael A. Kiebler
Physical Activity Dynamically Regulates the Hippocampal Proteome along the Dorso-Ventral Axis
International Journal of Molecular Sciences
dorsal and ventral hippocampus
enhanced physical activity
mass spectrometry
protein expression
metabolism
title Physical Activity Dynamically Regulates the Hippocampal Proteome along the Dorso-Ventral Axis
title_full Physical Activity Dynamically Regulates the Hippocampal Proteome along the Dorso-Ventral Axis
title_fullStr Physical Activity Dynamically Regulates the Hippocampal Proteome along the Dorso-Ventral Axis
title_full_unstemmed Physical Activity Dynamically Regulates the Hippocampal Proteome along the Dorso-Ventral Axis
title_short Physical Activity Dynamically Regulates the Hippocampal Proteome along the Dorso-Ventral Axis
title_sort physical activity dynamically regulates the hippocampal proteome along the dorso ventral axis
topic dorsal and ventral hippocampus
enhanced physical activity
mass spectrometry
protein expression
metabolism
url https://www.mdpi.com/1422-0067/21/10/3501
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