Cargando…

Tension-dependent stabilization of E-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells

Tension of the actomyosin cell cortex plays a key role in determining cell–cell contact growth and size. The level of cortical tension outside of the cell–cell contact, when pulling at the contact edge, scales with the total size to which a cell–cell contact can grow [J.-L. Maître et al., Science 33...

Descripción completa

Detalles Bibliográficos
Autores principales: Slováková, Jana, Sikora, Mateusz, Arslan, Feyza Nur, Caballero-Mancebo, Silvia, Krens, S. F. Gabriel, Kaufmann, Walter A., Merrin, Jack, Heisenberg, Carl-Philipp
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8872771/
https://www.ncbi.nlm.nih.gov/pubmed/35165179
http://dx.doi.org/10.1073/pnas.2122030119
_version_ 1784657320343502848
author Slováková, Jana
Sikora, Mateusz
Arslan, Feyza Nur
Caballero-Mancebo, Silvia
Krens, S. F. Gabriel
Kaufmann, Walter A.
Merrin, Jack
Heisenberg, Carl-Philipp
author_facet Slováková, Jana
Sikora, Mateusz
Arslan, Feyza Nur
Caballero-Mancebo, Silvia
Krens, S. F. Gabriel
Kaufmann, Walter A.
Merrin, Jack
Heisenberg, Carl-Philipp
author_sort Slováková, Jana
collection PubMed
description Tension of the actomyosin cell cortex plays a key role in determining cell–cell contact growth and size. The level of cortical tension outside of the cell–cell contact, when pulling at the contact edge, scales with the total size to which a cell–cell contact can grow [J.-L. Maître et al., Science 338, 253–256 (2012)]. Here, we show in zebrafish primary germ-layer progenitor cells that this monotonic relationship only applies to a narrow range of cortical tension increase and that above a critical threshold, contact size inversely scales with cortical tension. This switch from cortical tension increasing to decreasing progenitor cell–cell contact size is caused by cortical tension promoting E-cadherin anchoring to the actomyosin cytoskeleton, thereby increasing clustering and stability of E-cadherin at the contact. After tension-mediated E-cadherin stabilization at the contact exceeds a critical threshold level, the rate by which the contact expands in response to pulling forces from the cortex sharply drops, leading to smaller contacts at physiologically relevant timescales of contact formation. Thus, the activity of cortical tension in expanding cell–cell contact size is limited by tension-stabilizing E-cadherin–actin complexes at the contact.
format Online
Article
Text
id pubmed-8872771
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-88727712022-02-25 Tension-dependent stabilization of E-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells Slováková, Jana Sikora, Mateusz Arslan, Feyza Nur Caballero-Mancebo, Silvia Krens, S. F. Gabriel Kaufmann, Walter A. Merrin, Jack Heisenberg, Carl-Philipp Proc Natl Acad Sci U S A Biological Sciences Tension of the actomyosin cell cortex plays a key role in determining cell–cell contact growth and size. The level of cortical tension outside of the cell–cell contact, when pulling at the contact edge, scales with the total size to which a cell–cell contact can grow [J.-L. Maître et al., Science 338, 253–256 (2012)]. Here, we show in zebrafish primary germ-layer progenitor cells that this monotonic relationship only applies to a narrow range of cortical tension increase and that above a critical threshold, contact size inversely scales with cortical tension. This switch from cortical tension increasing to decreasing progenitor cell–cell contact size is caused by cortical tension promoting E-cadherin anchoring to the actomyosin cytoskeleton, thereby increasing clustering and stability of E-cadherin at the contact. After tension-mediated E-cadherin stabilization at the contact exceeds a critical threshold level, the rate by which the contact expands in response to pulling forces from the cortex sharply drops, leading to smaller contacts at physiologically relevant timescales of contact formation. Thus, the activity of cortical tension in expanding cell–cell contact size is limited by tension-stabilizing E-cadherin–actin complexes at the contact. National Academy of Sciences 2022-02-14 2022-02-22 /pmc/articles/PMC8872771/ /pubmed/35165179 http://dx.doi.org/10.1073/pnas.2122030119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Slováková, Jana
Sikora, Mateusz
Arslan, Feyza Nur
Caballero-Mancebo, Silvia
Krens, S. F. Gabriel
Kaufmann, Walter A.
Merrin, Jack
Heisenberg, Carl-Philipp
Tension-dependent stabilization of E-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells
title Tension-dependent stabilization of E-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells
title_full Tension-dependent stabilization of E-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells
title_fullStr Tension-dependent stabilization of E-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells
title_full_unstemmed Tension-dependent stabilization of E-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells
title_short Tension-dependent stabilization of E-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells
title_sort tension-dependent stabilization of e-cadherin limits cell–cell contact expansion in zebrafish germ-layer progenitor cells
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8872771/
https://www.ncbi.nlm.nih.gov/pubmed/35165179
http://dx.doi.org/10.1073/pnas.2122030119
work_keys_str_mv AT slovakovajana tensiondependentstabilizationofecadherinlimitscellcellcontactexpansioninzebrafishgermlayerprogenitorcells
AT sikoramateusz tensiondependentstabilizationofecadherinlimitscellcellcontactexpansioninzebrafishgermlayerprogenitorcells
AT arslanfeyzanur tensiondependentstabilizationofecadherinlimitscellcellcontactexpansioninzebrafishgermlayerprogenitorcells
AT caballeromancebosilvia tensiondependentstabilizationofecadherinlimitscellcellcontactexpansioninzebrafishgermlayerprogenitorcells
AT krenssfgabriel tensiondependentstabilizationofecadherinlimitscellcellcontactexpansioninzebrafishgermlayerprogenitorcells
AT kaufmannwaltera tensiondependentstabilizationofecadherinlimitscellcellcontactexpansioninzebrafishgermlayerprogenitorcells
AT merrinjack tensiondependentstabilizationofecadherinlimitscellcellcontactexpansioninzebrafishgermlayerprogenitorcells
AT heisenbergcarlphilipp tensiondependentstabilizationofecadherinlimitscellcellcontactexpansioninzebrafishgermlayerprogenitorcells