Dystroglycan is a scaffold for extracellular axon guidance decisions

Axon guidance requires interactions between extracellular signaling molecules and transmembrane receptors, but how appropriate context-dependent decisions are coordinated outside the cell remains unclear. Here we show that the transmembrane glycoprotein Dystroglycan interacts with a changing set of...

Full description

Bibliographic Details
Main Authors: L Bailey Lindenmaier, Nicolas Parmentier, Caiying Guo, Fadel Tissir, Kevin M Wright
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/42143
_version_ 1811202709329543168
author L Bailey Lindenmaier
Nicolas Parmentier
Caiying Guo
Fadel Tissir
Kevin M Wright
author_facet L Bailey Lindenmaier
Nicolas Parmentier
Caiying Guo
Fadel Tissir
Kevin M Wright
author_sort L Bailey Lindenmaier
collection DOAJ
description Axon guidance requires interactions between extracellular signaling molecules and transmembrane receptors, but how appropriate context-dependent decisions are coordinated outside the cell remains unclear. Here we show that the transmembrane glycoprotein Dystroglycan interacts with a changing set of environmental cues that regulate the trajectories of extending axons throughout the mammalian brain and spinal cord. Dystroglycan operates primarily as an extracellular scaffold during axon guidance, as it functions non-cell autonomously and does not require signaling through its intracellular domain. We identify the transmembrane receptor Celsr3/Adgrc3 as a binding partner for Dystroglycan, and show that this interaction is critical for specific axon guidance events in vivo. These findings establish Dystroglycan as a multifunctional scaffold that coordinates extracellular matrix proteins, secreted cues, and transmembrane receptors to regulate axon guidance.
first_indexed 2024-04-12T02:42:55Z
format Article
id doaj.art-52f63657a94944cf9ba28737165c2ce4
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T02:42:55Z
publishDate 2019-02-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-52f63657a94944cf9ba28737165c2ce42022-12-22T03:51:16ZengeLife Sciences Publications LtdeLife2050-084X2019-02-01810.7554/eLife.42143Dystroglycan is a scaffold for extracellular axon guidance decisionsL Bailey Lindenmaier0Nicolas Parmentier1Caiying Guo2Fadel Tissir3Kevin M Wright4https://orcid.org/0000-0001-5094-5270Vollum Institute, Oregon Health & Science University, Portland, United StatesInstitiute of Neuroscience, Université Catholique de Louvain, Brussels, BelgiumJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesInstitiute of Neuroscience, Université Catholique de Louvain, Brussels, BelgiumVollum Institute, Oregon Health & Science University, Portland, United StatesAxon guidance requires interactions between extracellular signaling molecules and transmembrane receptors, but how appropriate context-dependent decisions are coordinated outside the cell remains unclear. Here we show that the transmembrane glycoprotein Dystroglycan interacts with a changing set of environmental cues that regulate the trajectories of extending axons throughout the mammalian brain and spinal cord. Dystroglycan operates primarily as an extracellular scaffold during axon guidance, as it functions non-cell autonomously and does not require signaling through its intracellular domain. We identify the transmembrane receptor Celsr3/Adgrc3 as a binding partner for Dystroglycan, and show that this interaction is critical for specific axon guidance events in vivo. These findings establish Dystroglycan as a multifunctional scaffold that coordinates extracellular matrix proteins, secreted cues, and transmembrane receptors to regulate axon guidance.https://elifesciences.org/articles/42143axon guidancedystroglycancelsr3commissural axoninternal capsuleextracellular matrix
spellingShingle L Bailey Lindenmaier
Nicolas Parmentier
Caiying Guo
Fadel Tissir
Kevin M Wright
Dystroglycan is a scaffold for extracellular axon guidance decisions
eLife
axon guidance
dystroglycan
celsr3
commissural axon
internal capsule
extracellular matrix
title Dystroglycan is a scaffold for extracellular axon guidance decisions
title_full Dystroglycan is a scaffold for extracellular axon guidance decisions
title_fullStr Dystroglycan is a scaffold for extracellular axon guidance decisions
title_full_unstemmed Dystroglycan is a scaffold for extracellular axon guidance decisions
title_short Dystroglycan is a scaffold for extracellular axon guidance decisions
title_sort dystroglycan is a scaffold for extracellular axon guidance decisions
topic axon guidance
dystroglycan
celsr3
commissural axon
internal capsule
extracellular matrix
url https://elifesciences.org/articles/42143
work_keys_str_mv AT lbaileylindenmaier dystroglycanisascaffoldforextracellularaxonguidancedecisions
AT nicolasparmentier dystroglycanisascaffoldforextracellularaxonguidancedecisions
AT caiyingguo dystroglycanisascaffoldforextracellularaxonguidancedecisions
AT fadeltissir dystroglycanisascaffoldforextracellularaxonguidancedecisions
AT kevinmwright dystroglycanisascaffoldforextracellularaxonguidancedecisions