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Multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis

Embryogenesis requires cells to change shape and move without disrupting epithelial integrity. This requires robust, responsive linkage between adherens junctions and the actomyosin cytoskeleton. Using Drosophila morphogenesis, we define molecular mechanisms mediating junction–cytoskeletal linkage a...

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Autores principales: Perez-Vale, Kia Z., Yow, Kristi D., Johnson, Ruth I., Byrnes, Amy E., Finegan, Tara M., Slep, Kevin C., Peifer, Mark
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8590279/
https://www.ncbi.nlm.nih.gov/pubmed/34762121
http://dx.doi.org/10.1083/jcb.202104087
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author Perez-Vale, Kia Z.
Yow, Kristi D.
Johnson, Ruth I.
Byrnes, Amy E.
Finegan, Tara M.
Slep, Kevin C.
Peifer, Mark
author_facet Perez-Vale, Kia Z.
Yow, Kristi D.
Johnson, Ruth I.
Byrnes, Amy E.
Finegan, Tara M.
Slep, Kevin C.
Peifer, Mark
author_sort Perez-Vale, Kia Z.
collection PubMed
description Embryogenesis requires cells to change shape and move without disrupting epithelial integrity. This requires robust, responsive linkage between adherens junctions and the actomyosin cytoskeleton. Using Drosophila morphogenesis, we define molecular mechanisms mediating junction–cytoskeletal linkage and explore the role of mechanosensing. We focus on the junction–cytoskeletal linker Canoe, a multidomain protein. We engineered the canoe locus to define how its domains mediate its mechanism of action. To our surprise, the PDZ and FAB domains, which we thought connected junctions and F-actin, are not required for viability or mechanosensitive recruitment to junctions under tension. The FAB domain stabilizes junctions experiencing elevated force, but in its absence, most cells recover, suggesting redundant interactions. In contrast, the Rap1-binding RA domains are critical for all Cno functions and enrichment at junctions under tension. This supports a model in which junctional robustness derives from a large protein network assembled via multivalent interactions, with proteins at network nodes and some node connections more critical than others.
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spelling pubmed-85902792022-06-06 Multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis Perez-Vale, Kia Z. Yow, Kristi D. Johnson, Ruth I. Byrnes, Amy E. Finegan, Tara M. Slep, Kevin C. Peifer, Mark J Cell Biol Article Embryogenesis requires cells to change shape and move without disrupting epithelial integrity. This requires robust, responsive linkage between adherens junctions and the actomyosin cytoskeleton. Using Drosophila morphogenesis, we define molecular mechanisms mediating junction–cytoskeletal linkage and explore the role of mechanosensing. We focus on the junction–cytoskeletal linker Canoe, a multidomain protein. We engineered the canoe locus to define how its domains mediate its mechanism of action. To our surprise, the PDZ and FAB domains, which we thought connected junctions and F-actin, are not required for viability or mechanosensitive recruitment to junctions under tension. The FAB domain stabilizes junctions experiencing elevated force, but in its absence, most cells recover, suggesting redundant interactions. In contrast, the Rap1-binding RA domains are critical for all Cno functions and enrichment at junctions under tension. This supports a model in which junctional robustness derives from a large protein network assembled via multivalent interactions, with proteins at network nodes and some node connections more critical than others. Rockefeller University Press 2021-11-11 /pmc/articles/PMC8590279/ /pubmed/34762121 http://dx.doi.org/10.1083/jcb.202104087 Text en © 2021 Perez-Vale et al. https://creativecommons.org/licenses/by-nc-sa/4.0/http://www.rupress.org/terms/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Article
Perez-Vale, Kia Z.
Yow, Kristi D.
Johnson, Ruth I.
Byrnes, Amy E.
Finegan, Tara M.
Slep, Kevin C.
Peifer, Mark
Multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis
title Multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis
title_full Multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis
title_fullStr Multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis
title_full_unstemmed Multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis
title_short Multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis
title_sort multivalent interactions make adherens junction–cytoskeletal linkage robust during morphogenesis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8590279/
https://www.ncbi.nlm.nih.gov/pubmed/34762121
http://dx.doi.org/10.1083/jcb.202104087
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