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Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra

Mechanical input shapes cell fate decisions during development and regeneration in many systems, yet the mechanisms of this cross-talk are often unclear. In regenerating Hydra tissue spheroids, periodic osmotically driven inflation and deflation cycles generate mechanical stimuli in the form of tiss...

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Autores principales: Ferenc, Jaroslav, Papasaikas, Panagiotis, Ferralli, Jacqueline, Nakamura, Yukio, Smallwood, Sebastien, Tsiairis, Charisios D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8664257/
https://www.ncbi.nlm.nih.gov/pubmed/34890235
http://dx.doi.org/10.1126/sciadv.abj6897
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author Ferenc, Jaroslav
Papasaikas, Panagiotis
Ferralli, Jacqueline
Nakamura, Yukio
Smallwood, Sebastien
Tsiairis, Charisios D.
author_facet Ferenc, Jaroslav
Papasaikas, Panagiotis
Ferralli, Jacqueline
Nakamura, Yukio
Smallwood, Sebastien
Tsiairis, Charisios D.
author_sort Ferenc, Jaroslav
collection PubMed
description Mechanical input shapes cell fate decisions during development and regeneration in many systems, yet the mechanisms of this cross-talk are often unclear. In regenerating Hydra tissue spheroids, periodic osmotically driven inflation and deflation cycles generate mechanical stimuli in the form of tissue stretching. Here, we demonstrate that tissue stretching during inflation is important for the appearance of the head organizer—a group of cells that secrete the Wnt3 ligand. Exploiting time series RNA expression profiles, we identify the up-regulation of Wnt signaling as a key readout of the mechanical input. In this system, the levels of Wnt3 expression correspond to the levels of stretching, and Wnt3 overexpression alone enables successful regeneration in the absence of mechanical stimulation. Our findings enable the incorporation of mechanical signals in the framework of Hydra patterning and highlight the broad significance of mechanochemical feedback loops for patterning epithelial lumens.
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spelling pubmed-86642572021-12-16 Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra Ferenc, Jaroslav Papasaikas, Panagiotis Ferralli, Jacqueline Nakamura, Yukio Smallwood, Sebastien Tsiairis, Charisios D. Sci Adv Biomedicine and Life Sciences Mechanical input shapes cell fate decisions during development and regeneration in many systems, yet the mechanisms of this cross-talk are often unclear. In regenerating Hydra tissue spheroids, periodic osmotically driven inflation and deflation cycles generate mechanical stimuli in the form of tissue stretching. Here, we demonstrate that tissue stretching during inflation is important for the appearance of the head organizer—a group of cells that secrete the Wnt3 ligand. Exploiting time series RNA expression profiles, we identify the up-regulation of Wnt signaling as a key readout of the mechanical input. In this system, the levels of Wnt3 expression correspond to the levels of stretching, and Wnt3 overexpression alone enables successful regeneration in the absence of mechanical stimulation. Our findings enable the incorporation of mechanical signals in the framework of Hydra patterning and highlight the broad significance of mechanochemical feedback loops for patterning epithelial lumens. American Association for the Advancement of Science 2021-12-10 /pmc/articles/PMC8664257/ /pubmed/34890235 http://dx.doi.org/10.1126/sciadv.abj6897 Text en Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY). https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Biomedicine and Life Sciences
Ferenc, Jaroslav
Papasaikas, Panagiotis
Ferralli, Jacqueline
Nakamura, Yukio
Smallwood, Sebastien
Tsiairis, Charisios D.
Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra
title Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra
title_full Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra
title_fullStr Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra
title_full_unstemmed Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra
title_short Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra
title_sort mechanical oscillations orchestrate axial patterning through wnt activation in hydra
topic Biomedicine and Life Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8664257/
https://www.ncbi.nlm.nih.gov/pubmed/34890235
http://dx.doi.org/10.1126/sciadv.abj6897
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