Glial-dependent clustering of voltage-gated ion channels in Drosophila precedes myelin formation

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Abstract

Neuronal information conductance often involves the transmission of action potentials. The spreading of action potentials along the axonal process of a neuron is based on three physical parameters: The axial resistance of the axon, the axonal insulation by glial membranes, and the positioning of voltage-gated ion channels. In vertebrates, myelin and channel clustering allow fast saltatory conductance. Here we show that in Drosophila melanogaster voltage-gated sodium and potassium channels, Para and Shal, co-localize and cluster in an area resembling the axon initial segment. The local enrichment of Para but not of Shal localization depends on the presence of peripheral wrapping glial cells. In larvae, relatively low levels of Para channels are needed to allow proper signal transduction and nerves are simply wrapped by glial cells. In adults, the concentration of Para increases and is prominently found at the axon initial segment of motor neurons. Concomitantly, these axon domains are covered by a mesh of glial processes forming a lacunar structure that possibly serves as an ion reservoir. Directly flanking this domain glial processes forming the lacunar area appear to collapse and closely apposed stacks of glial cell processes can be detected, resembling a myelin-like insulation. Thus, Drosophila development may reflect the evolution of myelin which forms in response to increased levels of clustered voltage-gated ion channels.

Data availability

All imaging and source data are available through: https://omero-imaging.uni-muenster.de/openlink/rn_12EIW4OO3WCT_2607_ReyOhm_Elife_2023/ (To be replaced by a DOI upon final acceptance). All Drosophila strains reported are available upon request to C.K..

The following data sets were generated

1. Henrike Ohm
2. Simone Rey
(2023) Raw image data of all publication figures
https://doi.org/10.57860/min_prj_000008.

https://omero-imaging.uni-muenster.de/webclient/?show=project-4452

Article and author information

Author details

Simone Rey

University of Münster, Münster, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-0130-6744
Henrike Ohm

University of Münster, Münster, Germany

Competing interests
The authors declare that no competing interests exist.
Frederieke Moschref

Max-Planck Institut für Multidisziplinäre Naturwissenschaften, Göttingen, Germany

Competing interests
The authors declare that no competing interests exist.
Dagmar Zeuschner

Max Planck Institute for Molecular Biomedicine, Muenster, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6712-0192
Marit Praetz

University of Münster, Münster, Germany

Competing interests
The authors declare that no competing interests exist.
Christian Klämbt

University of Münster, Münster, Germany

For correspondence
klaembt@uni-muenster.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6349-5800

Funding

DFG (SFB 1348 B5)

Christian Klämbt

DFG (Kl 588 / 29)

Christian Klämbt

Open access funding provided by Max Planck Society.The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

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.