Cargando…
Axons in the Chick Embryo Follow Soft Pathways Through Developing Somite Segments
During patterning of the peripheral nervous system, motor axons grow sequentially out of the neural tube in a segmented fashion to ensure functional integration of the motor roots between the surrounding cartilage and bones of the developing vertebrae. This segmented outgrowth is regulated by the in...
Autores principales: | , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9304555/ https://www.ncbi.nlm.nih.gov/pubmed/35874821 http://dx.doi.org/10.3389/fcell.2022.917589 |
_version_ | 1784752113412210688 |
---|---|
author | Schaeffer, Julia Weber, Isabell P. Thompson, Amelia J. Keynes, Roger J. Franze, Kristian |
author_facet | Schaeffer, Julia Weber, Isabell P. Thompson, Amelia J. Keynes, Roger J. Franze, Kristian |
author_sort | Schaeffer, Julia |
collection | PubMed |
description | During patterning of the peripheral nervous system, motor axons grow sequentially out of the neural tube in a segmented fashion to ensure functional integration of the motor roots between the surrounding cartilage and bones of the developing vertebrae. This segmented outgrowth is regulated by the intrinsic properties of each segment (somite) adjacent to the neural tube, and in particular by chemical repulsive guidance cues expressed in the posterior half. Yet, knockout models for such repulsive cues still display initial segmentation of outgrowing motor axons, suggesting the existence of additional, yet unknown regulatory mechanisms of axon growth segmentation. As neuronal growth is not only regulated by chemical but also by mechanical signals, we here characterized the mechanical environment of outgrowing motor axons. Using atomic force microscopy-based indentation measurements on chick embryo somite strips, we identified stiffness gradients in each segment, which precedes motor axon growth. Axon growth was restricted to the anterior, softer tissue, which showed lower cell body densities than the repulsive stiffer posterior parts at later stages. As tissue stiffness is known to regulate axon growth during development, our results suggest that motor axons also respond to periodic stiffness gradients imposed by the intrinsic mechanical properties of somites. |
format | Online Article Text |
id | pubmed-9304555 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-93045552022-07-23 Axons in the Chick Embryo Follow Soft Pathways Through Developing Somite Segments Schaeffer, Julia Weber, Isabell P. Thompson, Amelia J. Keynes, Roger J. Franze, Kristian Front Cell Dev Biol Cell and Developmental Biology During patterning of the peripheral nervous system, motor axons grow sequentially out of the neural tube in a segmented fashion to ensure functional integration of the motor roots between the surrounding cartilage and bones of the developing vertebrae. This segmented outgrowth is regulated by the intrinsic properties of each segment (somite) adjacent to the neural tube, and in particular by chemical repulsive guidance cues expressed in the posterior half. Yet, knockout models for such repulsive cues still display initial segmentation of outgrowing motor axons, suggesting the existence of additional, yet unknown regulatory mechanisms of axon growth segmentation. As neuronal growth is not only regulated by chemical but also by mechanical signals, we here characterized the mechanical environment of outgrowing motor axons. Using atomic force microscopy-based indentation measurements on chick embryo somite strips, we identified stiffness gradients in each segment, which precedes motor axon growth. Axon growth was restricted to the anterior, softer tissue, which showed lower cell body densities than the repulsive stiffer posterior parts at later stages. As tissue stiffness is known to regulate axon growth during development, our results suggest that motor axons also respond to periodic stiffness gradients imposed by the intrinsic mechanical properties of somites. Frontiers Media S.A. 2022-07-08 /pmc/articles/PMC9304555/ /pubmed/35874821 http://dx.doi.org/10.3389/fcell.2022.917589 Text en Copyright © 2022 Schaeffer, Weber, Thompson, Keynes and Franze. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Cell and Developmental Biology Schaeffer, Julia Weber, Isabell P. Thompson, Amelia J. Keynes, Roger J. Franze, Kristian Axons in the Chick Embryo Follow Soft Pathways Through Developing Somite Segments |
title | Axons in the Chick Embryo Follow Soft Pathways Through Developing Somite Segments |
title_full | Axons in the Chick Embryo Follow Soft Pathways Through Developing Somite Segments |
title_fullStr | Axons in the Chick Embryo Follow Soft Pathways Through Developing Somite Segments |
title_full_unstemmed | Axons in the Chick Embryo Follow Soft Pathways Through Developing Somite Segments |
title_short | Axons in the Chick Embryo Follow Soft Pathways Through Developing Somite Segments |
title_sort | axons in the chick embryo follow soft pathways through developing somite segments |
topic | Cell and Developmental Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9304555/ https://www.ncbi.nlm.nih.gov/pubmed/35874821 http://dx.doi.org/10.3389/fcell.2022.917589 |
work_keys_str_mv | AT schaefferjulia axonsinthechickembryofollowsoftpathwaysthroughdevelopingsomitesegments AT weberisabellp axonsinthechickembryofollowsoftpathwaysthroughdevelopingsomitesegments AT thompsonameliaj axonsinthechickembryofollowsoftpathwaysthroughdevelopingsomitesegments AT keynesrogerj axonsinthechickembryofollowsoftpathwaysthroughdevelopingsomitesegments AT franzekristian axonsinthechickembryofollowsoftpathwaysthroughdevelopingsomitesegments |