RGS6 Mediates Effects of Voluntary Running on Adult Hippocampal Neurogenesis

Summary: Voluntary running enhances adult hippocampal neurogenesis, with consequences for hippocampal-dependent learning ability and mood regulation. However, the underlying mechanism remains unclear. Here, we show that voluntary running induces unique and dynamic gene expression changes specificall...

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Main Authors: Yu Gao, Minjie Shen, Jose Carlos Gonzalez, Qiping Dong, Sudharsan Kannan, Johnson T. Hoang, Brian E. Eisinger, Jyotsna Pandey, Sahar Javadi, Qiang Chang, Daifeng Wang, Linda Overstreet-Wadiche, Xinyu Zhao
Format: Article
Language:English
Published: Elsevier 2020-08-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124720309827
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author Yu Gao
Minjie Shen
Jose Carlos Gonzalez
Qiping Dong
Sudharsan Kannan
Johnson T. Hoang
Brian E. Eisinger
Jyotsna Pandey
Sahar Javadi
Qiang Chang
Daifeng Wang
Linda Overstreet-Wadiche
Xinyu Zhao
author_facet Yu Gao
Minjie Shen
Jose Carlos Gonzalez
Qiping Dong
Sudharsan Kannan
Johnson T. Hoang
Brian E. Eisinger
Jyotsna Pandey
Sahar Javadi
Qiang Chang
Daifeng Wang
Linda Overstreet-Wadiche
Xinyu Zhao
author_sort Yu Gao
collection DOAJ
description Summary: Voluntary running enhances adult hippocampal neurogenesis, with consequences for hippocampal-dependent learning ability and mood regulation. However, the underlying mechanism remains unclear. Here, we show that voluntary running induces unique and dynamic gene expression changes specifically within the adult-born hippocampal neurons, with significant impact on genes involved in neuronal maturation and human diseases. We identify the regulator of G protein signaling 6 (RGS6) as a key factor that mediates running impact on adult-born neurons. RGS6 overexpression mimics the positive effects of voluntary running on morphological and physiological maturation of adult new neurons and reduced sensitivity of adult-born neurons to the inhibitory effect of GABAB (γ-Aminobutyric acid B) receptor activation. Knocking down RGS6 abolishes running-enhanced neuronal maturation and hippocampal neurogenesis-dependent learning and anxiolytic effect. Our study provides a data resource showing genome-wide intrinsic molecular changes in adult-born hippocampal neurons that contribute to voluntary running-induced neurogenesis.
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spelling doaj.art-13585a4fa64043f193dcb2306c0231052022-12-21T16:58:45ZengElsevierCell Reports2211-12472020-08-01325107997RGS6 Mediates Effects of Voluntary Running on Adult Hippocampal NeurogenesisYu Gao0Minjie Shen1Jose Carlos Gonzalez2Qiping Dong3Sudharsan Kannan4Johnson T. Hoang5Brian E. Eisinger6Jyotsna Pandey7Sahar Javadi8Qiang Chang9Daifeng Wang10Linda Overstreet-Wadiche11Xinyu Zhao12Waisman Center, University of Wisconsin-Madison, Madison, WI 53705, USA; Department of Neuroscience, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53705, USAWaisman Center, University of Wisconsin-Madison, Madison, WI 53705, USA; Department of Neuroscience, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53705, USADepartment of Neurobiology, University of Alabama at Birmingham, Birmingham, AL 35294, USAWaisman Center, University of Wisconsin-Madison, Madison, WI 53705, USAWaisman Center, University of Wisconsin-Madison, Madison, WI 53705, USA; Department of Neuroscience, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53705, USAWaisman Center, University of Wisconsin-Madison, Madison, WI 53705, USA; Department of Neuroscience, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53705, USAWaisman Center, University of Wisconsin-Madison, Madison, WI 53705, USA; Department of Neuroscience, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53705, USAWaisman Center, University of Wisconsin-Madison, Madison, WI 53705, USAWaisman Center, University of Wisconsin-Madison, Madison, WI 53705, USAWaisman Center, University of Wisconsin-Madison, Madison, WI 53705, USA; Department of Medical Genetics, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53705, USA; Department of Neurology, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53705, USAWaisman Center, University of Wisconsin-Madison, Madison, WI 53705, USA; Department of Biostatistics and Medical Informatics, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53705, USADepartment of Neurobiology, University of Alabama at Birmingham, Birmingham, AL 35294, USAWaisman Center, University of Wisconsin-Madison, Madison, WI 53705, USA; Department of Neuroscience, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53705, USA; Corresponding authorSummary: Voluntary running enhances adult hippocampal neurogenesis, with consequences for hippocampal-dependent learning ability and mood regulation. However, the underlying mechanism remains unclear. Here, we show that voluntary running induces unique and dynamic gene expression changes specifically within the adult-born hippocampal neurons, with significant impact on genes involved in neuronal maturation and human diseases. We identify the regulator of G protein signaling 6 (RGS6) as a key factor that mediates running impact on adult-born neurons. RGS6 overexpression mimics the positive effects of voluntary running on morphological and physiological maturation of adult new neurons and reduced sensitivity of adult-born neurons to the inhibitory effect of GABAB (γ-Aminobutyric acid B) receptor activation. Knocking down RGS6 abolishes running-enhanced neuronal maturation and hippocampal neurogenesis-dependent learning and anxiolytic effect. Our study provides a data resource showing genome-wide intrinsic molecular changes in adult-born hippocampal neurons that contribute to voluntary running-induced neurogenesis.http://www.sciencedirect.com/science/article/pii/S2211124720309827adult neurogenesisRgs6voluntary runningRiboTag-seqhippocampusneuronal maturation
spellingShingle Yu Gao
Minjie Shen
Jose Carlos Gonzalez
Qiping Dong
Sudharsan Kannan
Johnson T. Hoang
Brian E. Eisinger
Jyotsna Pandey
Sahar Javadi
Qiang Chang
Daifeng Wang
Linda Overstreet-Wadiche
Xinyu Zhao
RGS6 Mediates Effects of Voluntary Running on Adult Hippocampal Neurogenesis
Cell Reports
adult neurogenesis
Rgs6
voluntary running
RiboTag-seq
hippocampus
neuronal maturation
title RGS6 Mediates Effects of Voluntary Running on Adult Hippocampal Neurogenesis
title_full RGS6 Mediates Effects of Voluntary Running on Adult Hippocampal Neurogenesis
title_fullStr RGS6 Mediates Effects of Voluntary Running on Adult Hippocampal Neurogenesis
title_full_unstemmed RGS6 Mediates Effects of Voluntary Running on Adult Hippocampal Neurogenesis
title_short RGS6 Mediates Effects of Voluntary Running on Adult Hippocampal Neurogenesis
title_sort rgs6 mediates effects of voluntary running on adult hippocampal neurogenesis
topic adult neurogenesis
Rgs6
voluntary running
RiboTag-seq
hippocampus
neuronal maturation
url http://www.sciencedirect.com/science/article/pii/S2211124720309827
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