Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila

Swati Banerjee, Anilkumar M. Pillai, Raehum Paik, Jingjun Li, Manzoor Bhat

Research output: Contribution to journalArticle

76 Citations (Scopus)

Abstract

Axonal insulation is critical for efficient action potential propagation and normal functioning of the nervous system. In Drosophila, the underlying basis of nerve ensheathment is the axonal insulation by glial cells and the establishment of septate junctions (SJs) between glial cell membranes. However, the details of the cellular and molecular mechanisms underlying axonal insulation and SJ formation are still obscure. Here, we report the characterization of axonal insulation in the Drosophila peripheral nervous system (PNS). Targeted expression of tau-green fluorescent protein in the glial cells and ultrastructural analysis of the peripheral nerves allowed us to visualize the glial ensheathment of axons. We show that individual or a group of axons are ensheathed by inner glial processes, which in turn are ensheathed by the outer perineurial glial cells. SJs are formed between the inner and outer glial membranes. We also show that Neurexin IV, Contactin, and Neuroglian are coexpressed in the peripheral glial membranes and that these proteins exist as a complex in the Drosophila nervous system. Mutations in neurexin IV, contactin, and neuroglian result in the disruption of blood-nerve barrier function in the PNS, and ultrastructural analyses of the mutant embryonic peripheral nerves show loss of glial SJs. Interestingly, the murine homologs of Neurexin IV, Contactin, and Neuroglian are expressed at the paranodal SJs and play a key role in axon-glial interactions of myelinated axons. Together, our data suggest that the molecular machinery underlying axonal insulation and axon-glial interactions may be conserved across species.

Original languageEnglish (US)
Pages (from-to)3319-3329
Number of pages11
JournalJournal of Neuroscience
Volume26
Issue number12
DOIs
StatePublished - Mar 22 2006
Externally publishedYes

Fingerprint

Peripheral Nervous System
Neuroglia
Drosophila
Contactins
Axons
Peripheral Nerves
Nervous System
Blood-Nerve Barrier
Green Fluorescent Proteins
Action Potentials
Membrane Proteins
Cell Membrane
Mutation

Keywords

  • Blood-nerve barrier
  • Cell adhesion
  • Chordotonal organs
  • Glial septate junctions
  • Neuron-glial interactions
  • Peripheral glia

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila. / Banerjee, Swati; Pillai, Anilkumar M.; Paik, Raehum; Li, Jingjun; Bhat, Manzoor.

In: Journal of Neuroscience, Vol. 26, No. 12, 22.03.2006, p. 3319-3329.

Research output: Contribution to journalArticle

Banerjee, Swati ; Pillai, Anilkumar M. ; Paik, Raehum ; Li, Jingjun ; Bhat, Manzoor. / Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila. In: Journal of Neuroscience. 2006 ; Vol. 26, No. 12. pp. 3319-3329.
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