Drosophila neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to wrapper

Wilm Tobias Stork, Silke Thomas, Floriano Rodrigues, Marion Silies, Elke Naffin, Stephanie Wenderdel, Christian Klämbt

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

Ensheathment of axons by glial membranes is a key feature of complex nervous systems ensuring the separation of single axons or axonal fascicles. Nevertheless, the molecules that mediate the recognition and specific adhesion of glial and axonal membranes are largely unknown. We use the Drosophila midline of the embryonic central nervous system as a model to investigate these neuron glia interactions. During development, the midline glial cells acquire close contact to commissural axons and eventually extend processes into the commissures to wrap individual axon fascicles. Here, we show that this wrapping of axons depends on the interaction of the neuronal transmembrane protein Neurexin IV with the glial Ig-domain protein Wrapper. Although Neurexin IV has been previously described to be an essential component of epithelial septate junctions (SJ), we show that its function in mediating glial wrapping at the CNS midline is independent of SJ formation. Moreover, differential splicing generates two different Neurexin IV isoforms. One mRNA is enriched in septate junction-forming tissues, whereas the other mRNA is expressed by neurons and recruited to the midline by Wrapper. Although both Neurexin IV isoforms are able to bind Wrapper, the neuronal isoform has a higher affinity for Wrapper. We conclude that Neurexin IV can mediate different adhesive cell-cell contacts depending on the isoforms expressed and the context of its interaction partners.

Original languageEnglish (US)
Pages (from-to)1251-1261
Number of pages11
JournalDevelopment
Volume136
Issue number8
DOIs
StatePublished - Apr 15 2009
Externally publishedYes

Fingerprint

Neuroglia
Drosophila
Axons
Neurons
Protein Isoforms
Messenger RNA
Membranes
Adhesives
Nervous System
Proteins
Central Nervous System

Keywords

  • Drosphila
  • Midline glia.
  • Neurexin IV
  • Neuron-glia interaction
  • Wrapper

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

Cite this

Stork, W. T., Thomas, S., Rodrigues, F., Silies, M., Naffin, E., Wenderdel, S., & Klämbt, C. (2009). Drosophila neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to wrapper. Development, 136(8), 1251-1261. https://doi.org/10.1242/dev.032847

Drosophila neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to wrapper. / Stork, Wilm Tobias; Thomas, Silke; Rodrigues, Floriano; Silies, Marion; Naffin, Elke; Wenderdel, Stephanie; Klämbt, Christian.

In: Development, Vol. 136, No. 8, 15.04.2009, p. 1251-1261.

Research output: Contribution to journalArticle

Stork, WT, Thomas, S, Rodrigues, F, Silies, M, Naffin, E, Wenderdel, S & Klämbt, C 2009, 'Drosophila neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to wrapper', Development, vol. 136, no. 8, pp. 1251-1261. https://doi.org/10.1242/dev.032847
Stork, Wilm Tobias ; Thomas, Silke ; Rodrigues, Floriano ; Silies, Marion ; Naffin, Elke ; Wenderdel, Stephanie ; Klämbt, Christian. / Drosophila neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to wrapper. In: Development. 2009 ; Vol. 136, No. 8. pp. 1251-1261.
@article{ab8c682ec266440c9b164923dcd5cdad,
title = "Drosophila neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to wrapper",
abstract = "Ensheathment of axons by glial membranes is a key feature of complex nervous systems ensuring the separation of single axons or axonal fascicles. Nevertheless, the molecules that mediate the recognition and specific adhesion of glial and axonal membranes are largely unknown. We use the Drosophila midline of the embryonic central nervous system as a model to investigate these neuron glia interactions. During development, the midline glial cells acquire close contact to commissural axons and eventually extend processes into the commissures to wrap individual axon fascicles. Here, we show that this wrapping of axons depends on the interaction of the neuronal transmembrane protein Neurexin IV with the glial Ig-domain protein Wrapper. Although Neurexin IV has been previously described to be an essential component of epithelial septate junctions (SJ), we show that its function in mediating glial wrapping at the CNS midline is independent of SJ formation. Moreover, differential splicing generates two different Neurexin IV isoforms. One mRNA is enriched in septate junction-forming tissues, whereas the other mRNA is expressed by neurons and recruited to the midline by Wrapper. Although both Neurexin IV isoforms are able to bind Wrapper, the neuronal isoform has a higher affinity for Wrapper. We conclude that Neurexin IV can mediate different adhesive cell-cell contacts depending on the isoforms expressed and the context of its interaction partners.",
keywords = "Drosphila, Midline glia., Neurexin IV, Neuron-glia interaction, Wrapper",
author = "Stork, {Wilm Tobias} and Silke Thomas and Floriano Rodrigues and Marion Silies and Elke Naffin and Stephanie Wenderdel and Christian Kl{\"a}mbt",
year = "2009",
month = "4",
day = "15",
doi = "10.1242/dev.032847",
language = "English (US)",
volume = "136",
pages = "1251--1261",
journal = "Development (Cambridge)",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "8",

}

TY - JOUR

T1 - Drosophila neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to wrapper

AU - Stork, Wilm Tobias

AU - Thomas, Silke

AU - Rodrigues, Floriano

AU - Silies, Marion

AU - Naffin, Elke

AU - Wenderdel, Stephanie

AU - Klämbt, Christian

PY - 2009/4/15

Y1 - 2009/4/15

N2 - Ensheathment of axons by glial membranes is a key feature of complex nervous systems ensuring the separation of single axons or axonal fascicles. Nevertheless, the molecules that mediate the recognition and specific adhesion of glial and axonal membranes are largely unknown. We use the Drosophila midline of the embryonic central nervous system as a model to investigate these neuron glia interactions. During development, the midline glial cells acquire close contact to commissural axons and eventually extend processes into the commissures to wrap individual axon fascicles. Here, we show that this wrapping of axons depends on the interaction of the neuronal transmembrane protein Neurexin IV with the glial Ig-domain protein Wrapper. Although Neurexin IV has been previously described to be an essential component of epithelial septate junctions (SJ), we show that its function in mediating glial wrapping at the CNS midline is independent of SJ formation. Moreover, differential splicing generates two different Neurexin IV isoforms. One mRNA is enriched in septate junction-forming tissues, whereas the other mRNA is expressed by neurons and recruited to the midline by Wrapper. Although both Neurexin IV isoforms are able to bind Wrapper, the neuronal isoform has a higher affinity for Wrapper. We conclude that Neurexin IV can mediate different adhesive cell-cell contacts depending on the isoforms expressed and the context of its interaction partners.

AB - Ensheathment of axons by glial membranes is a key feature of complex nervous systems ensuring the separation of single axons or axonal fascicles. Nevertheless, the molecules that mediate the recognition and specific adhesion of glial and axonal membranes are largely unknown. We use the Drosophila midline of the embryonic central nervous system as a model to investigate these neuron glia interactions. During development, the midline glial cells acquire close contact to commissural axons and eventually extend processes into the commissures to wrap individual axon fascicles. Here, we show that this wrapping of axons depends on the interaction of the neuronal transmembrane protein Neurexin IV with the glial Ig-domain protein Wrapper. Although Neurexin IV has been previously described to be an essential component of epithelial septate junctions (SJ), we show that its function in mediating glial wrapping at the CNS midline is independent of SJ formation. Moreover, differential splicing generates two different Neurexin IV isoforms. One mRNA is enriched in septate junction-forming tissues, whereas the other mRNA is expressed by neurons and recruited to the midline by Wrapper. Although both Neurexin IV isoforms are able to bind Wrapper, the neuronal isoform has a higher affinity for Wrapper. We conclude that Neurexin IV can mediate different adhesive cell-cell contacts depending on the isoforms expressed and the context of its interaction partners.

KW - Drosphila

KW - Midline glia.

KW - Neurexin IV

KW - Neuron-glia interaction

KW - Wrapper

UR - http://www.scopus.com/inward/record.url?scp=67650733293&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=67650733293&partnerID=8YFLogxK

U2 - 10.1242/dev.032847

DO - 10.1242/dev.032847

M3 - Article

VL - 136

SP - 1251

EP - 1261

JO - Development (Cambridge)

JF - Development (Cambridge)

SN - 0950-1991

IS - 8

ER -