Dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis

Apical constriction is a cell shape change that promotes epithelial bending. Activation of nonmuscle myosin II (Myo-II) by kinases such as Rho-associated kinase (Rok) is important to generate contractile force during apical constriction. Cycles of Myo-II assembly and disassembly, or pulses, are asso...

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Main Authors: Tworoger, Michael B., Vasquez, Claudia G, Martin, Adam C
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:en_US
Published: Rockefeller University Press 2015
Online Access:http://hdl.handle.net/1721.1/96347
https://orcid.org/0000-0002-8987-7508
https://orcid.org/0000-0001-8060-2607
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author Tworoger, Michael B.
Vasquez, Claudia G
Martin, Adam C
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Tworoger, Michael B.
Vasquez, Claudia G
Martin, Adam C
author_sort Tworoger, Michael B.
collection MIT
description Apical constriction is a cell shape change that promotes epithelial bending. Activation of nonmuscle myosin II (Myo-II) by kinases such as Rho-associated kinase (Rok) is important to generate contractile force during apical constriction. Cycles of Myo-II assembly and disassembly, or pulses, are associated with apical constriction during Drosophila melanogaster gastrulation. It is not understood whether Myo-II phosphoregulation organizes contractile pulses or whether pulses are important for tissue morphogenesis. Here, we show that Myo-II pulses are associated with pulses of apical Rok. Mutants that mimic Myo-II light chain phosphorylation or depletion of myosin phosphatase inhibit Myo-II contractile pulses, disrupting both actomyosin coalescence into apical foci and cycles of Myo-II assembly/disassembly. Thus, coupling dynamic Myo-II phosphorylation to upstream signals organizes contractile Myo-II pulses in both space and time. Mutants that mimic Myo-II phosphorylation undergo continuous, rather than incremental, apical constriction. These mutants fail to maintain intercellular actomyosin network connections during tissue invagination, suggesting that Myo-II pulses are required for tissue integrity during morphogenesis.
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spelling mit-1721.1/963472022-09-28T15:11:44Z Dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis Tworoger, Michael B. Vasquez, Claudia G Martin, Adam C Massachusetts Institute of Technology. Department of Biology Vasquez, Claudia G. Tworoger, Michael B. Martin, Adam C. Apical constriction is a cell shape change that promotes epithelial bending. Activation of nonmuscle myosin II (Myo-II) by kinases such as Rho-associated kinase (Rok) is important to generate contractile force during apical constriction. Cycles of Myo-II assembly and disassembly, or pulses, are associated with apical constriction during Drosophila melanogaster gastrulation. It is not understood whether Myo-II phosphoregulation organizes contractile pulses or whether pulses are important for tissue morphogenesis. Here, we show that Myo-II pulses are associated with pulses of apical Rok. Mutants that mimic Myo-II light chain phosphorylation or depletion of myosin phosphatase inhibit Myo-II contractile pulses, disrupting both actomyosin coalescence into apical foci and cycles of Myo-II assembly/disassembly. Thus, coupling dynamic Myo-II phosphorylation to upstream signals organizes contractile Myo-II pulses in both space and time. Mutants that mimic Myo-II phosphorylation undergo continuous, rather than incremental, apical constriction. These mutants fail to maintain intercellular actomyosin network connections during tissue invagination, suggesting that Myo-II pulses are required for tissue integrity during morphogenesis. National Institute of General Medical Sciences (U.S.) (Transgenic RNAi Project at Harvard Medical School, (R01-GM084947)) 2015-04-02T18:26:02Z 2015-04-02T18:26:02Z 2014-08 2014-02 Article http://purl.org/eprint/type/JournalArticle 0021-9525 1540-8140 http://hdl.handle.net/1721.1/96347 Vasquez, C. G., M. Tworoger, and A. C. Martin. “Dynamic Myosin Phosphorylation Regulates Contractile Pulses and Tissue Integrity During Epithelial Morphogenesis.” The Journal of Cell Biology 206, no. 3 (August 4, 2014): 435–450. https://orcid.org/0000-0002-8987-7508 https://orcid.org/0000-0001-8060-2607 en_US http://dx.doi.org/10.1083/jcb.201402004 Journal of Cell Biology Creative Commons Attribution http://creativecommons.org/licenses/by-nc-sa/3.0/ application/pdf Rockefeller University Press Rockefeller University Press
spellingShingle Tworoger, Michael B.
Vasquez, Claudia G
Martin, Adam C
Dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis
title Dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis
title_full Dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis
title_fullStr Dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis
title_full_unstemmed Dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis
title_short Dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis
title_sort dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis
url http://hdl.handle.net/1721.1/96347
https://orcid.org/0000-0002-8987-7508
https://orcid.org/0000-0001-8060-2607
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