Axon tension regulates fasciculation/defasciculation through the control of axon shaft zippering
- Czech Academy of Sciences, Czech Republic
- Sorbonne Université, UPMC Univ Paris 06, INSERM, CNRS, France
- Laboratoire de Physique Statistique, Ecole Normale Superieure, PSL Research University, France
Abstract
While axon fasciculation plays a key role in the development of neural networks, very little is known about its dynamics and the underlying biophysical mechanisms. In a model system composed of neurons grown ex vivo from explants of embryonic mouse olfactory epithelia, we observed that axons dynamically interact with each other through their shafts, leading to zippering and unzippering behaviour that regulates their fasciculation. Taking advantage of this new preparation suitable for studying such interactions, we carried out a detailed biophysical analysis of zippering, occurring either spontaneously or induced by micromanipulations and pharmacological treatments. We show that zippering arises from the competition of axon-axon adhesion and mechanical tension in the axons, and provide the first quantification of the force of axon-axon adhesion. Furthermore, we introduce a biophysical model of the zippering dynamics, and we quantitatively relate the individual zipper properties to global characteristics of the developing axon network. Our study uncovers a new role of mechanical tension in neural development: the regulation of axon fasciculation.
Article and author information
Author details
Funding
Université Pierre et Marie Curie
- Frédéric Pincet
- Alain Trembleau
Czech Science Foundation (14-16755S)
- Martin Zapotocky
Institut National de la Santé et de la Recherche Médicale
- Alain Trembleau
Centre National de la Recherche Scientifique
- Frédéric Pincet
- Alain Trembleau
Agence Nationale de la Recherche (ANR-2010-BLAN-1401-01)
- Alain Trembleau
National Institutes of Health (5R01DC012441)
- Alain Trembleau
First Faculty of Medicine at Charles University (GAUK 396213)
- Martin Zapotocky
Agence Nationale de la Recherche (ANR-11-IDEX-0004-02)
- Alain Trembleau
Barrande Czech-French Cooperation program (7AMB12FR002)
- Alain Trembleau
Czech Academy of Sciences (RVO#67985823)
- Martin Zapotocky
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Procedures involving animals and their care were conducted according to European Parliament Directive 2010/63/EU and the 22 September 2010 Council on the protection of animals.
Copyright
© 2017, Šmít 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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Axon tension regulates fasciculation/defasciculation through the control of axon shaft zippering
eLife 6:e19907.
https://doi.org/10.7554/eLife.19907
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