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

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.
The following previously published data sets were used

Article and author information

Author details

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5330-1689
  2. 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.
  3. Lucio Schiapparelli

    The Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Wanhua Shen

    The Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. John R Yates

    Department of Neuroscience, The Scripps Research Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. 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.
    ORCID icon "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

© 2018, Liu et al.

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.

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  1. Han-Hsuan Liu
  2. Daniel B Mcclatchy
  3. Lucio Schiapparelli
  4. Wanhua Shen
  5. John R Yates
  6. Hollis T Cline
(2018)
Role of the visual experience-dependent nascent proteome in neuronal plasticity
eLife 7:e33420.
https://doi.org/10.7554/eLife.33420

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https://doi.org/10.7554/eLife.33420

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