Activity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome

  1. Anitha P Govind
  2. Okunola Jeyifous  Is a corresponding author
  3. Theron A Russell
  4. Zola Yi
  5. Aubrey V Weigel
  6. Abhijit Ramaprasad
  7. Luke Newell
  8. William Ramos
  9. Fernando M Valbuena
  10. Jason C Casler
  11. Jing-Zhi Yan
  12. Benjamin S Glick
  13. Geoffrey T Swanson
  14. Jennifer Lippincott-Schwartz  Is a corresponding author
  15. William N Green  Is a corresponding author
  1. University of Chicago, United States
  2. Janelia Research Campus, Howard Hughes Medical Institute, United States
  3. The University of Chicago, United States
  4. Northwestern University, Feinberg School of Medicine, United States

Abstract

Activity-driven changes in the neuronal surface glycoproteome are known to occur with synapse formation, plasticity and related diseases, but their mechanistic basis and significance are unclear. Here, we observed that N-glycans on surface glycoproteins of dendrites shift from immature to mature forms containing sialic acid in response to increased neuronal activation. In exploring the basis of these N-glycosylation alterations, we discovered they result from the growth and proliferation of Golgi satellites scattered throughout the dendrite. Golgi satellites that formed during neuronal excitation were in close association with ER exit sites and early endosomes and contained glycosylation machinery without the Golgi structural protein, GM130. They functioned as distal glycosylation stations in dendrites, terminally modifying sugars either on newly synthesized glycoproteins passing through the secretory pathway, or on surface glycoproteins taken up from the endocytic pathway. These activities led to major changes in the dendritic surface of excited neurons, impacting binding and uptake of lectins, as well as causing functional changes in neurotransmitter receptors such as nicotinic acetylcholine receptors. Neural activity thus boosts the activity of the dendrite’s satellite micro-secretory system by redistributing Golgi enzymes involved in glycan modifications into peripheral Golgi satellites. This remodeling of the neuronal surface has potential significance for synaptic plasticity, addiction and disease.

Data availability

Source data files for all quantitative data presented in the current study have been deposited at Dryad. These contain raw data values, statistical summaries, and raw gels for panels in Figs 1, 2, 5, 6, 7, 8, and supplemental figures, figure 1-figure supplement 2, figure 2-figure supplement 2, figure 4-figure supplements 1 and 2, and figure 7-figure supplement 2. The files can be accessed via Dryad (doi:10.5061/dryad.qjq2bvqg3):

The following data sets were generated

Article and author information

Author details

  1. Anitha P Govind

    Department of Neurobiology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5890-2395
  2. Okunola Jeyifous

    Department of Neurobiology, University of Chicago, Chicago, United States
    For correspondence
    ojeyifou@bsd.uchicago.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4176-4694
  3. Theron A Russell

    Department of Neurobiology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Zola Yi

    Department of Neurobiology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Aubrey V Weigel

    Lippincott-Schwartz Lab, Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1694-4420
  6. Abhijit Ramaprasad

    Department of Neurobiology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Luke Newell

    Department of Neurobiology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. William Ramos

    Department of Neurobiology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Fernando M Valbuena

    Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Jason C Casler

    Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9742-9978
  11. Jing-Zhi Yan

    Department of Pharmacology, Northwestern University, Feinberg School of Medicine, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Benjamin S Glick

    Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7921-1374
  13. Geoffrey T Swanson

    Department of Pharmacology, Northwestern University, Feinberg School of Medicine, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Jennifer Lippincott-Schwartz

    Lippincott-Schwartz Lab, Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    lippincottschwartzj@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8601-3501
  15. William N Green

    Department of Neurobiology, University of Chicago, Chicago, United States
    For correspondence
    wgreen@uchicago.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2167-1391

Funding

National Institutes of Health (DA035430)

  • William N Green

National Institutes of Health (DA044760)

  • William N Green

National Institutes of Health (DA043361)

  • William N Green

National Institutes of Health (GM104010)

  • Benjamin S Glick

National Institutes of Health (GM007183)

  • Fernando M Valbuena

Peter F McManus Foundation

  • William N Green

Howard Hughes Medical Institute

  • Jennifer Lippincott-Schwartz

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 procedures were approved by the University of Chicago Institutional Animal Care and Use Committee (protocol #72016) and are in accordance with the recommendations of the Panel on Euthanasia of the American Veterinary Medical Association. Strict adherence to AVMA guidelines was followed to prevent pain and suffering of animals.

Reviewing Editor

  1. Frederic A Bard, Institute of Molecular and Cell Biology (A*STAR), Singapore

Publication history

  1. Received: March 30, 2021
  2. Preprint posted: April 8, 2021 (view preprint)
  3. Accepted: September 20, 2021
  4. Accepted Manuscript published: September 21, 2021 (version 1)
  5. Version of Record published: October 6, 2021 (version 2)

Copyright

© 2021, Govind 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. Anitha P Govind
  2. Okunola Jeyifous
  3. Theron A Russell
  4. Zola Yi
  5. Aubrey V Weigel
  6. Abhijit Ramaprasad
  7. Luke Newell
  8. William Ramos
  9. Fernando M Valbuena
  10. Jason C Casler
  11. Jing-Zhi Yan
  12. Benjamin S Glick
  13. Geoffrey T Swanson
  14. Jennifer Lippincott-Schwartz
  15. William N Green
(2021)
Activity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome
eLife 10:e68910.
https://doi.org/10.7554/eLife.68910