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

Abstract
Data availability
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Abstract

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 3 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.

Data availability

The following data sets were generated

1. Liu et al
(2018) Xenopus Brain Proteome
ftp://MSV000081728@massive.ucsd.edu.

http://www.proteomexchange.org

The following previously published data sets were used

1. Xenbase
(2014) Xenbase_Xenopus_laevis_05-29-2014
RRID:SCR_003280.

http://www.xenbase.org
1. Wuhr et al
(2014) Molecular Atlas of Development
accession no. PXD000926.

http://kirschner.med.harvard.edu/MADX.html
1. Xenbase
(2015) UniProt_Xenopus_laevis_01-23-2015
Proteome ID: UP000186698.

http://www.xenbase.org
1. Shen et al
(2014) Xenopus brain
ProteomeExchange number: PXD008659.

http://proteomecentral.proteomexchange.org/cgi/GetDataset?ID=PXD008659

Article and author information

Author details

Han-Hsuan Liu

The Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5330-1689
Daniel B Mcclatchy

Department of Molecular Medicine, The Scripps Research Institute, La Jolla, United States

Competing interests
The authors declare that no competing interests exist.
Lucio Schiapparelli

The Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, United States

Competing interests
The authors declare that no competing interests exist.
Wanhua Shen

The Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, United States

Competing interests
The authors declare that no competing interests exist.
John R Yates

Department of Neuroscience, The Scripps Research Institute, La Jolla, United States

Competing interests
The authors declare that no competing interests exist.
Hollis T Cline

The Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, United States

For correspondence
cline@scripps.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4887-9603

Funding

National Institutes of Health (EY011261)

Han-Hsuan Liu
Lucio Schiapparelli
Wanhua Shen
Hollis T Cline

National Institutes of Health (EY019005)

Han-Hsuan Liu
Lucio Schiapparelli
Hollis T Cline

National Institutes of Health (MH067880)

Daniel B Mcclatchy
John R Yates

National Institutes of Health (MH100175)

Daniel B Mcclatchy
John R Yates

DartNeuroScience LLC

Han-Hsuan Liu
Hollis T Cline

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All animal protocols (#08-0083-4) were approved by the Institutional Animal Use and Care Committee of The Scripps Research Institute.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.