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...
Main Authors: | , , , , , , , , |
---|---|
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 |
_version_ | 1818325279948406784 |
---|---|
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. |
first_indexed | 2024-12-13T11:41:58Z |
format | Article |
id | doaj.art-2066d32e79254d5996a2b0f070c94a3e |
institution | Directory Open Access Journal |
issn | 1662-5099 |
language | English |
last_indexed | 2024-12-13T11:41:58Z |
publishDate | 2018-05-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Molecular Neuroscience |
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 |
work_keys_str_mv | AT yanruiyang endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT yanruiyang endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT jiangchen endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT zhenzhenguo endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT zhenzhenguo endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT zhenzhenguo endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT shikundeng endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT shikundeng endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT shikundeng endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT xiangyangdu endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT xiangyangdu endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT shaoxiazhu endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT shaoxiazhu endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT changye endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT yunsshi endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT jiajialiu endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT jiajialiu endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation AT jiajialiu endophilina1promotesactinpolymerizationindendriticspinesrequiredforsynapticpotentiation |