Golgi-independent secretory trafficking through recycling endosomes in neuronal dendrites and spines

  1. Aaron B Bowen
  2. Ashley M Bourke
  3. Brian G Hiester
  4. Cyril Hanus
  5. Matthew J Kennedy  Is a corresponding author
  1. University of Colorado School of Medicine, United States
  2. Inserm U894, University Paris-Descartes, France

Abstract

Neurons face the challenge of regulating the abundance, distribution and repertoire of integral membrane proteins within their immense, architecturally complex dendritic arbors. While the endoplasmic reticulum (ER) supports dendritic translation, most dendrites lack the Golgi apparatus (GA), an essential organelle for conventional secretory trafficking. Thus, whether secretory cargo is locally trafficked in dendrites through a non-canonical pathway remains a fundamental question. Here we define the dendritic trafficking itinerary for key synaptic molecules in rat cortical neurons. Following ER exit, the AMPA-type glutamate receptor GluA1 and neuroligin 1 undergo spatially restricted entry into the dendritic secretory pathway and accumulate in recycling endosomes (REs) located in dendrites and spines before reaching the plasma membrane. Surprisingly, GluA1 surface delivery occurred even when GA function was disrupted. Thus, in addition to their canonical role in protein recycling, REs also mediate forward secretory trafficking in neuronal dendrites and spines through a specialized GA-independent trafficking network.

Article and author information

Author details

  1. Aaron B Bowen

    Department of Pharmacology, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Ashley M Bourke

    Department of Pharmacology, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Brian G Hiester

    Department of Pharmacology, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Cyril Hanus

    Center for Psychiatry and Neurosciences, Inserm U894, University Paris-Descartes, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Matthew J Kennedy

    Department of Pharmacology, University of Colorado School of Medicine, Aurora, United States
    For correspondence
    matthew.kennedy@ucdenver.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7029-7802

Funding

National Institute of Neurological Disorders and Stroke (RO1 NS082271)

  • Matthew J Kennedy

McKnight Endowment Fund for Neuroscience

  • Matthew J Kennedy

Pew Charitable Trusts

  • Matthew J Kennedy

National Institute of Neurological Disorders and Stroke (F30 NS092421)

  • Aaron B Bowen

Howard Hughes Medical Institute (Gilliam Fellowship)

  • Ashley M Bourke

Institut National de la Santé et de la Recherche Médicale

  • Cyril Hanus

National Science Foundation (DGE-1553798)

  • Ashley M Bourke

Agence Nationale de la Recherche (ANR-16-CE16-0009-01)

  • Cyril Hanus

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All animal procedures were carried out in accordance with a protocol approved by the University of Colorado Denver Institutional Animal Care and Use Committee (protocol # B-98715(04)1E).

Reviewing Editor

  1. Graeme W Davis, University of California, San Francisco, United States

Publication history

  1. Received: April 3, 2017
  2. Accepted: August 30, 2017
  3. Accepted Manuscript published: September 6, 2017 (version 1)
  4. Version of Record published: October 2, 2017 (version 2)

Copyright

© 2017, Bowen 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. Aaron B Bowen
  2. Ashley M Bourke
  3. Brian G Hiester
  4. Cyril Hanus
  5. Matthew J Kennedy
(2017)
Golgi-independent secretory trafficking through recycling endosomes in neuronal dendrites and spines
eLife 6:e27362.
https://doi.org/10.7554/eLife.27362

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