1. Biochemistry and Chemical Biology
  2. Neuroscience

Glia-neuron coupling via a bipartite sialylation pathway promotes neural transmission and stress tolerance in Drosophila

  1. Hilary Scott
  2. Boris Novikov
  3. Berrak Ugur
  4. Brooke Allen
  5. Ilya Mertsalov
  6. Pedro Monagas-Valentin
  7. Melissa Koff
  8. Sarah Baas Robinson
  9. Kazuhiro Aoki
  10. Raisa Veizaj
  11. Dirk Lefeber
  12. Michael Tiemeyer
  13. Hugo J Bellen
  14. Vladislav Panin  Is a corresponding author
  1. Texas A&M University, United States
  2. Baylor College of Medicine, United States
  3. University of Georgia, United States
  4. Radboud University Nijmegen Medical Centre, Netherlands
https://doi.org/10.7554/eLife.78280
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  1. Hilary Scott
  2. Boris Novikov
  3. Berrak Ugur
  4. Brooke Allen
  5. Ilya Mertsalov
  6. Pedro Monagas-Valentin
  7. Melissa Koff
  8. Sarah Baas Robinson
  9. Kazuhiro Aoki
  10. Raisa Veizaj
  11. Dirk Lefeber
  12. Michael Tiemeyer
  13. Hugo J Bellen
  14. Vladislav Panin
(2023)
Glia-neuron coupling via a bipartite sialylation pathway promotes neural transmission and stress tolerance in Drosophila
eLife 12:e78280.
https://doi.org/10.7554/eLife.78280
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Abstract

Modification by sialylated glycans can affect protein functions, underlying mechanisms that control animal development and physiology. Sialylation relies on a dedicated pathway involving evolutionarily conserved enzymes, including CMP-sialic acid synthetase (CSAS) and sialyltransferase (SiaT) that mediate the activation of sialic acid and its transfer onto glycan termini, respectively. In Drosophila, CSAS and DSiaT genes function in the nervous system, affecting neural transmission and excitability. We found that these genes function in different cells: the function of CSAS is restricted to glia, while DSiaT functions in neurons. This partition of the sialylation pathway allows for regulation of neural functions via a glia-mediated control of neural sialylation. The sialylation genes were shown to be required for tolerance to heat and oxidative stress and for maintenance of the normal level of voltage-gated sodium channels. Our results uncovered a unique bipartite sialylation pathway that mediates glia-neuron coupling and regulates neural excitability and stress tolerance.

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All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been uploaded to a public repository for Tables 1 and Supplementary Table 3

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Author details

  1. Hilary Scott

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    No competing interests declared.

  2. Boris Novikov

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    No competing interests declared.

  3. Berrak Ugur

    Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4806-8891

  4. Brooke Allen

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    No competing interests declared.

  5. Ilya Mertsalov

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    No competing interests declared.

  6. Pedro Monagas-Valentin

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    No competing interests declared.

  7. Melissa Koff

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    No competing interests declared.

  8. Sarah Baas Robinson

    Complex Carbohydrate Research Center, University of Georgia, Athens, United States
    Competing interests
    No competing interests declared.

  9. Kazuhiro Aoki

    Complex Carbohydrate Research Center, University of Georgia, Athens, United States
    Competing interests
    No competing interests declared.

  10. Raisa Veizaj

    Department of Laboratory Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, Netherlands
    Competing interests
    No competing interests declared.

  11. Dirk Lefeber

    Department of Laboratory Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, Netherlands
    Competing interests
    No competing interests declared.

  12. Michael Tiemeyer

    Complex Carbohydrate Research Center, University of Georgia, Athens, United States
    Competing interests
    No competing interests declared.

  13. Hugo J Bellen

    Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, United States
    Competing interests
    Hugo J Bellen, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5992-5989

  14. Vladislav Panin

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    For correspondence
    panin@tamu.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9126-1481

Funding

National Institutes of Health (NS099409)

  • Vladislav Panin

National Institutes of Health (NS075534)

  • Vladislav Panin

TAMU-COANCYT (2012-037(S))

  • Vladislav Panin

TAMU AgriLife IHA

  • Vladislav Panin

National Institutes of Health (GM103490)

  • Michael Tiemeyer

Radboud Consortium for Glycoscience

  • Dirk Lefeber

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

Copyright

© 2023, Scott 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. Hilary Scott
  2. Boris Novikov
  3. Berrak Ugur
  4. Brooke Allen
  5. Ilya Mertsalov
  6. Pedro Monagas-Valentin
  7. Melissa Koff
  8. Sarah Baas Robinson
  9. Kazuhiro Aoki
  10. Raisa Veizaj
  11. Dirk Lefeber
  12. Michael Tiemeyer
  13. Hugo J Bellen
  14. Vladislav Panin
(2023)
Glia-neuron coupling via a bipartite sialylation pathway promotes neural transmission and stress tolerance in Drosophila
eLife 12:e78280.
https://doi.org/10.7554/eLife.78280

Share this article

https://doi.org/10.7554/eLife.78280

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