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Axial segmentation by iterative mechanical signaling

In bony fishes, formation of the vertebral column, or spine, is guided by a metameric blueprint established in the epithelial sheath of the notochord. Generation of the notochord template begins days after somitogenesis and even occurs in the absence of somite segmentation. However, patterning defec...

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Autores principales: Wopat, Susan, Adhyapok, Priyom, Daga, Bijoy, Crawford, Janice M., Peskin, Brianna, Norman, James, Bagwell, Jennifer, Fogerson, Stephanie M., Di Talia, Stefano, Kiehart, Daniel P., Charbonneau, Patrick, Bagnat, Michel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10081202/
https://www.ncbi.nlm.nih.gov/pubmed/37034817
http://dx.doi.org/10.1101/2023.03.27.534101
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author Wopat, Susan
Adhyapok, Priyom
Daga, Bijoy
Crawford, Janice M.
Peskin, Brianna
Norman, James
Bagwell, Jennifer
Fogerson, Stephanie M.
Di Talia, Stefano
Kiehart, Daniel P.
Charbonneau, Patrick
Bagnat, Michel
author_facet Wopat, Susan
Adhyapok, Priyom
Daga, Bijoy
Crawford, Janice M.
Peskin, Brianna
Norman, James
Bagwell, Jennifer
Fogerson, Stephanie M.
Di Talia, Stefano
Kiehart, Daniel P.
Charbonneau, Patrick
Bagnat, Michel
author_sort Wopat, Susan
collection PubMed
description In bony fishes, formation of the vertebral column, or spine, is guided by a metameric blueprint established in the epithelial sheath of the notochord. Generation of the notochord template begins days after somitogenesis and even occurs in the absence of somite segmentation. However, patterning defects in the somites lead to imprecise notochord segmentation, suggesting these processes are linked. Here, we reveal that spatial coordination between the notochord and the axial musculature is necessary to ensure segmentation of the zebrafish spine both in time and space. We find that the connective tissues that anchor the axial skeletal musculature, known as the myosepta in zebrafish, transmit spatial patterning cues necessary to initiate notochord segment formation, a critical pre-patterning step in spine morphogenesis. When an irregular pattern of muscle segments and myosepta interact with the notochord sheath, segments form non-sequentially, initiate at atypical locations, and eventually display altered morphology later in development. We determine that locations of myoseptum-notochord connections are hubs for mechanical signal transmission, which are characterized by localized sites of deformation of the extracellular matrix (ECM) layer encasing the notochord. The notochord sheath responds to the external mechanical changes by locally augmenting focal adhesion machinery to define the initiation site for segmentation. Using a coarse-grained mathematical model that captures the spatial patterns of myoseptum-notochord interactions, we find that a fixed-length scale of external cues is critical for driving sequential segment patterning in the notochord. Together, this work identifies a robust segmentation mechanism that hinges upon mechanical coupling of adjacent tissues to control patterning dynamics.
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spelling pubmed-100812022023-04-08 Axial segmentation by iterative mechanical signaling Wopat, Susan Adhyapok, Priyom Daga, Bijoy Crawford, Janice M. Peskin, Brianna Norman, James Bagwell, Jennifer Fogerson, Stephanie M. Di Talia, Stefano Kiehart, Daniel P. Charbonneau, Patrick Bagnat, Michel bioRxiv Article In bony fishes, formation of the vertebral column, or spine, is guided by a metameric blueprint established in the epithelial sheath of the notochord. Generation of the notochord template begins days after somitogenesis and even occurs in the absence of somite segmentation. However, patterning defects in the somites lead to imprecise notochord segmentation, suggesting these processes are linked. Here, we reveal that spatial coordination between the notochord and the axial musculature is necessary to ensure segmentation of the zebrafish spine both in time and space. We find that the connective tissues that anchor the axial skeletal musculature, known as the myosepta in zebrafish, transmit spatial patterning cues necessary to initiate notochord segment formation, a critical pre-patterning step in spine morphogenesis. When an irregular pattern of muscle segments and myosepta interact with the notochord sheath, segments form non-sequentially, initiate at atypical locations, and eventually display altered morphology later in development. We determine that locations of myoseptum-notochord connections are hubs for mechanical signal transmission, which are characterized by localized sites of deformation of the extracellular matrix (ECM) layer encasing the notochord. The notochord sheath responds to the external mechanical changes by locally augmenting focal adhesion machinery to define the initiation site for segmentation. Using a coarse-grained mathematical model that captures the spatial patterns of myoseptum-notochord interactions, we find that a fixed-length scale of external cues is critical for driving sequential segment patterning in the notochord. Together, this work identifies a robust segmentation mechanism that hinges upon mechanical coupling of adjacent tissues to control patterning dynamics. Cold Spring Harbor Laboratory 2023-03-28 /pmc/articles/PMC10081202/ /pubmed/37034817 http://dx.doi.org/10.1101/2023.03.27.534101 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Wopat, Susan
Adhyapok, Priyom
Daga, Bijoy
Crawford, Janice M.
Peskin, Brianna
Norman, James
Bagwell, Jennifer
Fogerson, Stephanie M.
Di Talia, Stefano
Kiehart, Daniel P.
Charbonneau, Patrick
Bagnat, Michel
Axial segmentation by iterative mechanical signaling
title Axial segmentation by iterative mechanical signaling
title_full Axial segmentation by iterative mechanical signaling
title_fullStr Axial segmentation by iterative mechanical signaling
title_full_unstemmed Axial segmentation by iterative mechanical signaling
title_short Axial segmentation by iterative mechanical signaling
title_sort axial segmentation by iterative mechanical signaling
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10081202/
https://www.ncbi.nlm.nih.gov/pubmed/37034817
http://dx.doi.org/10.1101/2023.03.27.534101
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