Endophilin A1 Promotes Actin Polymerization in Dendritic Spines Required for Synaptic Potentiation

Endophilin A1 is a member of the N-BAR domain-containing endophilin A protein family that is involved in membrane dynamics and trafficking. At the presynaptic terminal, endophilin As participate in synaptic vesicle recycling and autophagosome formation. By gene knockout studies, here we report that...

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Main Authors: Yanrui Yang, Jiang Chen, Zhenzhen Guo, Shikun Deng, Xiangyang Du, Shaoxia Zhu, Chang Ye, Yun S. Shi, Jia-Jia Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-05-01
Series:Frontiers in Molecular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnmol.2018.00177/full
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author Yanrui Yang
Yanrui Yang
Jiang Chen
Zhenzhen Guo
Zhenzhen Guo
Zhenzhen Guo
Shikun Deng
Shikun Deng
Shikun Deng
Xiangyang Du
Xiangyang Du
Shaoxia Zhu
Shaoxia Zhu
Chang Ye
Yun S. Shi
Jia-Jia Liu
Jia-Jia Liu
Jia-Jia Liu
author_facet Yanrui Yang
Yanrui Yang
Jiang Chen
Zhenzhen Guo
Zhenzhen Guo
Zhenzhen Guo
Shikun Deng
Shikun Deng
Shikun Deng
Xiangyang Du
Xiangyang Du
Shaoxia Zhu
Shaoxia Zhu
Chang Ye
Yun S. Shi
Jia-Jia Liu
Jia-Jia Liu
Jia-Jia Liu
author_sort Yanrui Yang
collection DOAJ
description Endophilin A1 is a member of the N-BAR domain-containing endophilin A protein family that is involved in membrane dynamics and trafficking. At the presynaptic terminal, endophilin As participate in synaptic vesicle recycling and autophagosome formation. By gene knockout studies, here we report that postsynaptic endophilin A1 functions in synaptic plasticity. Ablation of endophilin A1 in the hippocampal CA1 region of mature mouse brain impairs long-term spatial and contextual fear memory. Its loss in CA1 neurons postsynaptic of the Schaffer collateral pathway causes impairment in their AMPA-type glutamate receptor-mediated synaptic transmission and long-term potentiation. In KO neurons, defects in the structural and functional plasticity of dendritic spines can be rescued by overexpression of endophilin A1 but not A2 or A3. Further, endophilin A1 promotes actin polymerization in dendritic spines during synaptic potentiation. These findings reveal a physiological role of endophilin A1 distinct from that of other endophilin As at the postsynaptic site.
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spelling doaj.art-2066d32e79254d5996a2b0f070c94a3e2022-12-21T23:47:36ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992018-05-011110.3389/fnmol.2018.00177381623Endophilin A1 Promotes Actin Polymerization in Dendritic Spines Required for Synaptic PotentiationYanrui Yang0Yanrui Yang1Jiang Chen2Zhenzhen Guo3Zhenzhen Guo4Zhenzhen Guo5Shikun Deng6Shikun Deng7Shikun Deng8Xiangyang Du9Xiangyang Du10Shaoxia Zhu11Shaoxia Zhu12Chang Ye13Yun S. Shi14Jia-Jia Liu15Jia-Jia Liu16Jia-Jia Liu17State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaCAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, ChinaState Key Laboratory of Pharmaceutical Biotechnology and MOE Key Laboratory of Model Animal for Disease Study, Model Animal Research Center, Nanjing University, Nanjing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaCAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, ChinaGraduate School, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaCAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, ChinaGraduate School, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaGraduate School, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaCAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, ChinaState Key Laboratory of Pharmaceutical Biotechnology and MOE Key Laboratory of Model Animal for Disease Study, Model Animal Research Center, Nanjing University, Nanjing, ChinaState Key Laboratory of Pharmaceutical Biotechnology and MOE Key Laboratory of Model Animal for Disease Study, Model Animal Research Center, Nanjing University, Nanjing, ChinaState Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaCAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaEndophilin A1 is a member of the N-BAR domain-containing endophilin A protein family that is involved in membrane dynamics and trafficking. At the presynaptic terminal, endophilin As participate in synaptic vesicle recycling and autophagosome formation. By gene knockout studies, here we report that postsynaptic endophilin A1 functions in synaptic plasticity. Ablation of endophilin A1 in the hippocampal CA1 region of mature mouse brain impairs long-term spatial and contextual fear memory. Its loss in CA1 neurons postsynaptic of the Schaffer collateral pathway causes impairment in their AMPA-type glutamate receptor-mediated synaptic transmission and long-term potentiation. In KO neurons, defects in the structural and functional plasticity of dendritic spines can be rescued by overexpression of endophilin A1 but not A2 or A3. Further, endophilin A1 promotes actin polymerization in dendritic spines during synaptic potentiation. These findings reveal a physiological role of endophilin A1 distinct from that of other endophilin As at the postsynaptic site.https://www.frontiersin.org/article/10.3389/fnmol.2018.00177/fullendophilin A1learning and memorysynaptic transmissionsynaptic potentiationactin polymerizationstructural plasticity
spellingShingle Yanrui Yang
Yanrui Yang
Jiang Chen
Zhenzhen Guo
Zhenzhen Guo
Zhenzhen Guo
Shikun Deng
Shikun Deng
Shikun Deng
Xiangyang Du
Xiangyang Du
Shaoxia Zhu
Shaoxia Zhu
Chang Ye
Yun S. Shi
Jia-Jia Liu
Jia-Jia Liu
Jia-Jia Liu
Endophilin A1 Promotes Actin Polymerization in Dendritic Spines Required for Synaptic Potentiation
Frontiers in Molecular Neuroscience
endophilin A1
learning and memory
synaptic transmission
synaptic potentiation
actin polymerization
structural plasticity
title Endophilin A1 Promotes Actin Polymerization in Dendritic Spines Required for Synaptic Potentiation
title_full Endophilin A1 Promotes Actin Polymerization in Dendritic Spines Required for Synaptic Potentiation
title_fullStr Endophilin A1 Promotes Actin Polymerization in Dendritic Spines Required for Synaptic Potentiation
title_full_unstemmed Endophilin A1 Promotes Actin Polymerization in Dendritic Spines Required for Synaptic Potentiation
title_short Endophilin A1 Promotes Actin Polymerization in Dendritic Spines Required for Synaptic Potentiation
title_sort endophilin a1 promotes actin polymerization in dendritic spines required for synaptic potentiation
topic endophilin A1
learning and memory
synaptic transmission
synaptic potentiation
actin polymerization
structural plasticity
url https://www.frontiersin.org/article/10.3389/fnmol.2018.00177/full
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