Role of the visual experience-dependent nascent proteome in neuronal plasticity

Experience-dependent synaptic plasticity refines brain circuits during development. To identify novel protein synthesis-dependent mechanisms contributing to experience-dependent plasticity, we conducted a quantitative proteomic screen of the nascent proteome in response to visual experience in Xenop...

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Main Authors: Han-Hsuan Liu, Daniel B McClatchy, Lucio Schiapparelli, Wanhua Shen, John R Yates III, Hollis T Cline
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/33420
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author Han-Hsuan Liu
Daniel B McClatchy
Lucio Schiapparelli
Wanhua Shen
John R Yates III
Hollis T Cline
author_facet Han-Hsuan Liu
Daniel B McClatchy
Lucio Schiapparelli
Wanhua Shen
John R Yates III
Hollis T Cline
author_sort Han-Hsuan Liu
collection DOAJ
description Experience-dependent synaptic plasticity refines brain circuits during development. To identify novel protein synthesis-dependent mechanisms contributing to experience-dependent plasticity, we conducted a quantitative proteomic screen of the nascent proteome in response to visual experience in Xenopus optic tectum using bio-orthogonal metabolic labeling (BONCAT). We identified 83 differentially synthesized candidate plasticity proteins (CPPs). The CPPs form strongly interconnected networks and are annotated to a variety of biological functions, including RNA splicing, protein translation, and chromatin remodeling. Functional analysis of select CPPs revealed the requirement for eukaryotic initiation factor three subunit A (eIF3A), fused in sarcoma (FUS), and ribosomal protein s17 (RPS17) in experience-dependent structural plasticity in tectal neurons and behavioral plasticity in tadpoles. These results demonstrate that the nascent proteome is dynamic in response to visual experience and that de novo synthesis of machinery that regulates RNA splicing and protein translation is required for experience-dependent plasticity.
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spelling doaj.art-0d835f6178594afea8499c342d015dc92022-12-22T02:05:05ZengeLife Sciences Publications LtdeLife2050-084X2018-02-01710.7554/eLife.33420Role of the visual experience-dependent nascent proteome in neuronal plasticityHan-Hsuan Liu0https://orcid.org/0000-0002-5330-1689Daniel B McClatchy1https://orcid.org/0000-0002-0288-5645Lucio Schiapparelli2Wanhua Shen3John R Yates III4Hollis T Cline5https://orcid.org/0000-0002-4887-9603The Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, United States; Department of Neuroscience, The Scripps Research Institute, La Jolla, United States; Kellogg School of Science and Technology, The Scripps Research Institute, La Jolla, United StatesDepartment of Molecular Medicine, The Scripps Research Institute, La Jolla, United StatesThe Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, United States; Department of Neuroscience, The Scripps Research Institute, La Jolla, United StatesThe Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, United States; Department of Neuroscience, The Scripps Research Institute, La Jolla, United States; Zhejiang Key Laboratory of Organ Development and Regeneration, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, ChinaDepartment of Neuroscience, The Scripps Research Institute, La Jolla, United States; Department of Molecular Medicine, The Scripps Research Institute, La Jolla, United StatesThe Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, United States; Department of Neuroscience, The Scripps Research Institute, La Jolla, United States; Kellogg School of Science and Technology, The Scripps Research Institute, La Jolla, United States; Department of Molecular Medicine, The Scripps Research Institute, La Jolla, United StatesExperience-dependent synaptic plasticity refines brain circuits during development. To identify novel protein synthesis-dependent mechanisms contributing to experience-dependent plasticity, we conducted a quantitative proteomic screen of the nascent proteome in response to visual experience in Xenopus optic tectum using bio-orthogonal metabolic labeling (BONCAT). We identified 83 differentially synthesized candidate plasticity proteins (CPPs). The CPPs form strongly interconnected networks and are annotated to a variety of biological functions, including RNA splicing, protein translation, and chromatin remodeling. Functional analysis of select CPPs revealed the requirement for eukaryotic initiation factor three subunit A (eIF3A), fused in sarcoma (FUS), and ribosomal protein s17 (RPS17) in experience-dependent structural plasticity in tectal neurons and behavioral plasticity in tadpoles. These results demonstrate that the nascent proteome is dynamic in response to visual experience and that de novo synthesis of machinery that regulates RNA splicing and protein translation is required for experience-dependent plasticity.https://elifesciences.org/articles/33420nascent proteomeplasticityFUSvisual experienceeIF3AXenopus
spellingShingle Han-Hsuan Liu
Daniel B McClatchy
Lucio Schiapparelli
Wanhua Shen
John R Yates III
Hollis T Cline
Role of the visual experience-dependent nascent proteome in neuronal plasticity
eLife
nascent proteome
plasticity
FUS
visual experience
eIF3A
Xenopus
title Role of the visual experience-dependent nascent proteome in neuronal plasticity
title_full Role of the visual experience-dependent nascent proteome in neuronal plasticity
title_fullStr Role of the visual experience-dependent nascent proteome in neuronal plasticity
title_full_unstemmed Role of the visual experience-dependent nascent proteome in neuronal plasticity
title_short Role of the visual experience-dependent nascent proteome in neuronal plasticity
title_sort role of the visual experience dependent nascent proteome in neuronal plasticity
topic nascent proteome
plasticity
FUS
visual experience
eIF3A
Xenopus
url https://elifesciences.org/articles/33420
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AT danielbmcclatchy roleofthevisualexperiencedependentnascentproteomeinneuronalplasticity
AT lucioschiapparelli roleofthevisualexperiencedependentnascentproteomeinneuronalplasticity
AT wanhuashen roleofthevisualexperiencedependentnascentproteomeinneuronalplasticity
AT johnryatesiii roleofthevisualexperiencedependentnascentproteomeinneuronalplasticity
AT hollistcline roleofthevisualexperiencedependentnascentproteomeinneuronalplasticity