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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Rockefeller University Press
2015
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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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institution | Massachusetts Institute of Technology |
language | en_US |
last_indexed | 2024-09-23T13:38:10Z |
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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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