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Cell ratcheting through the Sbf RabGEF directs force balancing and stepped apical constriction

During Drosophila melanogaster gastrulation, the invagination of the prospective mesoderm is driven by the pulsed constriction of apical surfaces. Here, we address the mechanisms by which the irreversibility of pulsed events is achieved while also permitting uniform epithelial behaviors to emerge. W...

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Autores principales: Miao, Hui, Vanderleest, Timothy E., Jewett, Cayla E., Loerke, Dinah, Blankenship, J. Todd
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6829657/
https://www.ncbi.nlm.nih.gov/pubmed/31562231
http://dx.doi.org/10.1083/jcb.201905082
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author Miao, Hui
Vanderleest, Timothy E.
Jewett, Cayla E.
Loerke, Dinah
Blankenship, J. Todd
author_facet Miao, Hui
Vanderleest, Timothy E.
Jewett, Cayla E.
Loerke, Dinah
Blankenship, J. Todd
author_sort Miao, Hui
collection PubMed
description During Drosophila melanogaster gastrulation, the invagination of the prospective mesoderm is driven by the pulsed constriction of apical surfaces. Here, we address the mechanisms by which the irreversibility of pulsed events is achieved while also permitting uniform epithelial behaviors to emerge. We use MSD-based analyses to identify contractile steps and find that when a trafficking pathway initiated by Sbf is disrupted, contractile steps become reversible. Sbf localizes to tubular, apical surfaces and associates with Rab35, where it promotes Rab GTP exchange. Interestingly, when Sbf/Rab35 function is compromised, the apical plasma membrane becomes deeply convoluted, and nonuniform cell behaviors begin to emerge. Consistent with this, Sbf/Rab35 appears to prefigure and organize the apical surface for efficient Myosin function. Finally, we show that Sbf/Rab35/CME directs the plasma membrane to Rab11 endosomes through a dynamic interaction with Rab5 endosomes. These results suggest that periodic ratcheting events shift excess membrane from cell apices into endosomal pathways to permit reshaping of actomyosin networks and the apical surface.
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spelling pubmed-68296572020-05-04 Cell ratcheting through the Sbf RabGEF directs force balancing and stepped apical constriction Miao, Hui Vanderleest, Timothy E. Jewett, Cayla E. Loerke, Dinah Blankenship, J. Todd J Cell Biol Research Articles During Drosophila melanogaster gastrulation, the invagination of the prospective mesoderm is driven by the pulsed constriction of apical surfaces. Here, we address the mechanisms by which the irreversibility of pulsed events is achieved while also permitting uniform epithelial behaviors to emerge. We use MSD-based analyses to identify contractile steps and find that when a trafficking pathway initiated by Sbf is disrupted, contractile steps become reversible. Sbf localizes to tubular, apical surfaces and associates with Rab35, where it promotes Rab GTP exchange. Interestingly, when Sbf/Rab35 function is compromised, the apical plasma membrane becomes deeply convoluted, and nonuniform cell behaviors begin to emerge. Consistent with this, Sbf/Rab35 appears to prefigure and organize the apical surface for efficient Myosin function. Finally, we show that Sbf/Rab35/CME directs the plasma membrane to Rab11 endosomes through a dynamic interaction with Rab5 endosomes. These results suggest that periodic ratcheting events shift excess membrane from cell apices into endosomal pathways to permit reshaping of actomyosin networks and the apical surface. Rockefeller University Press 2019-11-04 2019-09-27 /pmc/articles/PMC6829657/ /pubmed/31562231 http://dx.doi.org/10.1083/jcb.201905082 Text en © 2019 Miao et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/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 Research Articles
Miao, Hui
Vanderleest, Timothy E.
Jewett, Cayla E.
Loerke, Dinah
Blankenship, J. Todd
Cell ratcheting through the Sbf RabGEF directs force balancing and stepped apical constriction
title Cell ratcheting through the Sbf RabGEF directs force balancing and stepped apical constriction
title_full Cell ratcheting through the Sbf RabGEF directs force balancing and stepped apical constriction
title_fullStr Cell ratcheting through the Sbf RabGEF directs force balancing and stepped apical constriction
title_full_unstemmed Cell ratcheting through the Sbf RabGEF directs force balancing and stepped apical constriction
title_short Cell ratcheting through the Sbf RabGEF directs force balancing and stepped apical constriction
title_sort cell ratcheting through the sbf rabgef directs force balancing and stepped apical constriction
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6829657/
https://www.ncbi.nlm.nih.gov/pubmed/31562231
http://dx.doi.org/10.1083/jcb.201905082
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