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Cell–Fibronectin Interactions and Actomyosin Contractility Regulate the Segmentation Clock and Spatio-Temporal Somite Cleft Formation during Chick Embryo Somitogenesis

Fibronectin is essential for somite formation in the vertebrate embryo. Fibronectin matrix assembly starts as cells emerge from the primitive streak and ingress in the unsegmented presomitic mesoderm (PSM). PSM cells undergo cyclic waves of segmentation clock gene expression, followed by Notch-depen...

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Autores principales: Gomes de Almeida, Patrícia, Rifes, Pedro, Martins-Jesus, Ana P., Pinheiro, Gonçalo G., Andrade, Raquel P., Thorsteinsdóttir, Sólveig
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9266262/
https://www.ncbi.nlm.nih.gov/pubmed/35805087
http://dx.doi.org/10.3390/cells11132003
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author Gomes de Almeida, Patrícia
Rifes, Pedro
Martins-Jesus, Ana P.
Pinheiro, Gonçalo G.
Andrade, Raquel P.
Thorsteinsdóttir, Sólveig
author_facet Gomes de Almeida, Patrícia
Rifes, Pedro
Martins-Jesus, Ana P.
Pinheiro, Gonçalo G.
Andrade, Raquel P.
Thorsteinsdóttir, Sólveig
author_sort Gomes de Almeida, Patrícia
collection PubMed
description Fibronectin is essential for somite formation in the vertebrate embryo. Fibronectin matrix assembly starts as cells emerge from the primitive streak and ingress in the unsegmented presomitic mesoderm (PSM). PSM cells undergo cyclic waves of segmentation clock gene expression, followed by Notch-dependent upregulation of meso1 in the rostral PSM which induces somite cleft formation. However, the relevance of the fibronectin matrix for these molecular processes remains unknown. Here, we assessed the role of the PSM fibronectin matrix in the spatio-temporal regulation of chick embryo somitogenesis by perturbing (1) extracellular fibronectin matrix assembly, (2) integrin–fibronectin binding, (3) Rho-associated protein kinase (ROCK) activity and (4) non-muscle myosin II (NM II) function. We found that integrin–fibronectin engagement and NM II activity are required for cell polarization in the nascent somite. All treatments resulted in defective somitic clefts and significantly perturbed meso1 and segmentation clock gene expression in the PSM. Importantly, inhibition of actomyosin-mediated contractility increased the period of hairy1/hes4 oscillations from 90 to 120 min. Together, our work strongly suggests that the fibronectin–integrin–ROCK–NM II axis regulates segmentation clock dynamics and dictates the spatio-temporal localization of somitic clefts.
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spelling pubmed-92662622022-07-09 Cell–Fibronectin Interactions and Actomyosin Contractility Regulate the Segmentation Clock and Spatio-Temporal Somite Cleft Formation during Chick Embryo Somitogenesis Gomes de Almeida, Patrícia Rifes, Pedro Martins-Jesus, Ana P. Pinheiro, Gonçalo G. Andrade, Raquel P. Thorsteinsdóttir, Sólveig Cells Article Fibronectin is essential for somite formation in the vertebrate embryo. Fibronectin matrix assembly starts as cells emerge from the primitive streak and ingress in the unsegmented presomitic mesoderm (PSM). PSM cells undergo cyclic waves of segmentation clock gene expression, followed by Notch-dependent upregulation of meso1 in the rostral PSM which induces somite cleft formation. However, the relevance of the fibronectin matrix for these molecular processes remains unknown. Here, we assessed the role of the PSM fibronectin matrix in the spatio-temporal regulation of chick embryo somitogenesis by perturbing (1) extracellular fibronectin matrix assembly, (2) integrin–fibronectin binding, (3) Rho-associated protein kinase (ROCK) activity and (4) non-muscle myosin II (NM II) function. We found that integrin–fibronectin engagement and NM II activity are required for cell polarization in the nascent somite. All treatments resulted in defective somitic clefts and significantly perturbed meso1 and segmentation clock gene expression in the PSM. Importantly, inhibition of actomyosin-mediated contractility increased the period of hairy1/hes4 oscillations from 90 to 120 min. Together, our work strongly suggests that the fibronectin–integrin–ROCK–NM II axis regulates segmentation clock dynamics and dictates the spatio-temporal localization of somitic clefts. MDPI 2022-06-22 /pmc/articles/PMC9266262/ /pubmed/35805087 http://dx.doi.org/10.3390/cells11132003 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Gomes de Almeida, Patrícia
Rifes, Pedro
Martins-Jesus, Ana P.
Pinheiro, Gonçalo G.
Andrade, Raquel P.
Thorsteinsdóttir, Sólveig
Cell–Fibronectin Interactions and Actomyosin Contractility Regulate the Segmentation Clock and Spatio-Temporal Somite Cleft Formation during Chick Embryo Somitogenesis
title Cell–Fibronectin Interactions and Actomyosin Contractility Regulate the Segmentation Clock and Spatio-Temporal Somite Cleft Formation during Chick Embryo Somitogenesis
title_full Cell–Fibronectin Interactions and Actomyosin Contractility Regulate the Segmentation Clock and Spatio-Temporal Somite Cleft Formation during Chick Embryo Somitogenesis
title_fullStr Cell–Fibronectin Interactions and Actomyosin Contractility Regulate the Segmentation Clock and Spatio-Temporal Somite Cleft Formation during Chick Embryo Somitogenesis
title_full_unstemmed Cell–Fibronectin Interactions and Actomyosin Contractility Regulate the Segmentation Clock and Spatio-Temporal Somite Cleft Formation during Chick Embryo Somitogenesis
title_short Cell–Fibronectin Interactions and Actomyosin Contractility Regulate the Segmentation Clock and Spatio-Temporal Somite Cleft Formation during Chick Embryo Somitogenesis
title_sort cell–fibronectin interactions and actomyosin contractility regulate the segmentation clock and spatio-temporal somite cleft formation during chick embryo somitogenesis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9266262/
https://www.ncbi.nlm.nih.gov/pubmed/35805087
http://dx.doi.org/10.3390/cells11132003
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