Microtubule-dependent ribosome localization in C. elegans neurons

  1. Kentaro Noma
  2. Alexandr Goncharov
  3. Mark H Ellisman
  4. Yishi Jin  Is a corresponding author
  1. University of California, San Diego, United States

Abstract

Subcellular localization of ribosomes defines the capacity for local translation. Methods to visualize ribosomes in live multicellular organisms are desirable for mechanistic investigations of the cell biology of ribosomes. Here, we developed an approach using split GFP for tissue-specific visualization of ribosomes in live Caenorhabditis elegans. Ribosomes are detected as puncta in the axons and synaptic terminals of specific neuron types, correlating with ribosome distribution at the ultrastructural level. We found that axonal ribosomes change localization during neuronal development and after axonal injury. Using genetic screens, we showed that the microtubule cytoskeleton and the JIP3 protein UNC-16 exert distinct effects on localization of axonal and somatic ribosomes. Our data demonstrate the utility of tissue-specific visualization of ribosomes in vivo, and provide insight into the mechanisms of active regulation of ribosome localization in neurons.

Article and author information

Author details

  1. Kentaro Noma

    Division of Biological Sciences, Neurobiology Section, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Alexandr Goncharov

    Division of Biological Sciences, Neurobiology Section, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Mark H Ellisman

    National Center for Research in Biological Systems, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Yishi Jin

    Division of Biological Sciences, Neurobiology Section, University of California, San Diego, San Diego, United States
    For correspondence
    yijin@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9371-9860

Funding

Howard Hughes Medical Institute

  • Yishi Jin

National Institutes of Health (R01 035546)

  • Yishi Jin

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

Reviewing Editor

  1. Anna Akhmanova, Utrecht University, Netherlands

Version history

  1. Received: February 28, 2017
  2. Accepted: August 1, 2017
  3. Accepted Manuscript published: August 2, 2017 (version 1)
  4. Version of Record published: August 16, 2017 (version 2)

Copyright

© 2017, Noma 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.

Metrics

  • 6,031
    Page views
  • 879
    Downloads
  • 30
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Kentaro Noma
  2. Alexandr Goncharov
  3. Mark H Ellisman
  4. Yishi Jin
(2017)
Microtubule-dependent ribosome localization in C. elegans neurons
eLife 6:e26376.
https://doi.org/10.7554/eLife.26376

Share this article

https://doi.org/10.7554/eLife.26376

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.