1. Neuroscience

Satellite glia modulate sympathetic neuron survival, activity, and autonomic function

  1. Aurelia A Mapps
  2. Erica Boehm
  3. Corinne Beier
  4. William T Keenan
  5. Jennifer Langel
  6. Michael Liu
  7. Michael B Thomsen
  8. Samer Hattar
  9. Haiqing Zhao
  10. Emmanouil Tampakakis
  11. Rejji Kuruvilla  Is a corresponding author
  1. Johns Hopkins University, United States
  2. National Institute of Mental Health, United States
https://doi.org/10.7554/eLife.74295
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  1. Aurelia A Mapps
  2. Erica Boehm
  3. Corinne Beier
  4. William T Keenan
  5. Jennifer Langel
  6. Michael Liu
  7. Michael B Thomsen
  8. Samer Hattar
  9. Haiqing Zhao
  10. Emmanouil Tampakakis
  11. Rejji Kuruvilla
(2022)
Satellite glia modulate sympathetic neuron survival, activity, and autonomic function
eLife 11:e74295.
https://doi.org/10.7554/eLife.74295
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Abstract

Satellite glia are the major glial cells in sympathetic ganglia, enveloping neuronal cell bodies. Despite this intimate association, the extent to which sympathetic functions are influenced by satellite glia in vivo remains unclear. Here, we show that satellite glia are critical for metabolism, survival, and activity of sympathetic neurons and modulate autonomic behaviors in mice. Adult ablation of satellite glia results in impaired mTOR signaling, soma atrophy, reduced noradrenergic enzymes, and loss of sympathetic neurons. However, persisting neurons have elevated activity, and satellite glia-ablated mice show increased pupil dilation and heart rate, indicative of enhanced sympathetic tone. Satellite glia-specific deletion of Kir4.1, an inward-rectifying potassium channel, largely recapitulates the cellular defects observed in glia-ablated mice, suggesting that satellite glia act in part via K+-dependent mechanisms. These findings highlight neuron-satellite glia as functional units in regulating sympathetic output, with implications for disorders linked to sympathetic hyper-activity such as cardiovascular disease and hypertension.

Data availability

All data generated or analysed during this study are included in the manuscript (Results, Materials and Methods, and Figure Legends).

Article and author information

Author details

  1. Aurelia A Mapps

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7956-2465

  2. Erica Boehm

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Corinne Beier

    Section on Light and Circadian Rhythms (SLCR), National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0698-7219

  4. William T Keenan

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Jennifer Langel

    Section on Light and Circadian Rhythms (SLCR), National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Michael Liu

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Michael B Thomsen

    Section on Light and Circadian Rhythms (SLCR), National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.

  8. Samer Hattar

    Section on Light and Circadian Rhythms (SLCR), National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3124-9525

  9. Haiqing Zhao

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4275-9843

  10. Emmanouil Tampakakis

    Department of Medicine, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.

  11. Rejji Kuruvilla

    Department of Biology, Johns Hopkins University, Baltimore, United States
    For correspondence
    rkuruvilla@jhu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2851-675X

Funding

National Institutes of Health (NS073751)

  • Rejji Kuruvilla

National Institutes of Health (NS107342)

  • Rejji Kuruvilla

National Science Foundation (DGE-1746891)

  • Aurelia A Mapps

National Institutes of Health (DC016065)

  • Haiqing Zhao

National Institutes of Health (EY027202)

  • Haiqing Zhao

National Institutes of Health (ZIAMH002964)

  • Samer Hattar

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

Reviewing Editor

  1. Moses V Chao, New York University Langone Medical Center, United States

Ethics

Animal experimentation: All procedures relating to animal care and treatment conformed to The Johns Hopkins University Animal Care and Use Committee (ACUC, protocol#MO19A488) and NIH guidelines.

Version history

  1. Preprint posted: September 23, 2021 (view preprint)
  2. Received: September 28, 2021
  3. Accepted: August 22, 2022
  4. Accepted Manuscript published: August 23, 2022 (version 1)
  5. Accepted Manuscript updated: August 25, 2022 (version 2)
  6. Version of Record published: August 31, 2022 (version 3)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Aurelia A Mapps
  2. Erica Boehm
  3. Corinne Beier
  4. William T Keenan
  5. Jennifer Langel
  6. Michael Liu
  7. Michael B Thomsen
  8. Samer Hattar
  9. Haiqing Zhao
  10. Emmanouil Tampakakis
  11. Rejji Kuruvilla
(2022)
Satellite glia modulate sympathetic neuron survival, activity, and autonomic function
eLife 11:e74295.
https://doi.org/10.7554/eLife.74295

Share this article

https://doi.org/10.7554/eLife.74295

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