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Cell patterning by secretion-induced plasma membrane flows

Cells self-organize using reaction-diffusion and fluid-flow principles. Whether bulk membrane flows contribute to cell patterning has not been established. Here, using mathematical modeling, optogenetics, and synthetic probes, we show that polarized exocytosis causes lateral membrane flows away from...

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Autores principales: Gerganova, Veneta, Lamas, Iker, Rutkowski, David M., Vještica, Aleksandar, Castro, Daniela Gallo, Vincenzetti, Vincent, Vavylonis, Dimitrios, Martin, Sophie G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8448446/
https://www.ncbi.nlm.nih.gov/pubmed/34533984
http://dx.doi.org/10.1126/sciadv.abg6718
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author Gerganova, Veneta
Lamas, Iker
Rutkowski, David M.
Vještica, Aleksandar
Castro, Daniela Gallo
Vincenzetti, Vincent
Vavylonis, Dimitrios
Martin, Sophie G.
author_facet Gerganova, Veneta
Lamas, Iker
Rutkowski, David M.
Vještica, Aleksandar
Castro, Daniela Gallo
Vincenzetti, Vincent
Vavylonis, Dimitrios
Martin, Sophie G.
author_sort Gerganova, Veneta
collection PubMed
description Cells self-organize using reaction-diffusion and fluid-flow principles. Whether bulk membrane flows contribute to cell patterning has not been established. Here, using mathematical modeling, optogenetics, and synthetic probes, we show that polarized exocytosis causes lateral membrane flows away from regions of membrane insertion. Plasma membrane–associated proteins with sufficiently low diffusion and/or detachment rates couple to the flows and deplete from areas of exocytosis. In rod-shaped fission yeast cells, zones of Cdc42 GTPase activity driving polarized exocytosis are limited by GTPase activating proteins (GAPs). We show that membrane flows pattern the GAP Rga4 distribution and that coupling of a synthetic GAP to membrane flows is sufficient to establish the rod shape. Thus, membrane flows induced by Cdc42-dependent exocytosis form a negative feedback restricting the zone of Cdc42 activity.
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spelling pubmed-84484462021-09-27 Cell patterning by secretion-induced plasma membrane flows Gerganova, Veneta Lamas, Iker Rutkowski, David M. Vještica, Aleksandar Castro, Daniela Gallo Vincenzetti, Vincent Vavylonis, Dimitrios Martin, Sophie G. Sci Adv Biomedicine and Life Sciences Cells self-organize using reaction-diffusion and fluid-flow principles. Whether bulk membrane flows contribute to cell patterning has not been established. Here, using mathematical modeling, optogenetics, and synthetic probes, we show that polarized exocytosis causes lateral membrane flows away from regions of membrane insertion. Plasma membrane–associated proteins with sufficiently low diffusion and/or detachment rates couple to the flows and deplete from areas of exocytosis. In rod-shaped fission yeast cells, zones of Cdc42 GTPase activity driving polarized exocytosis are limited by GTPase activating proteins (GAPs). We show that membrane flows pattern the GAP Rga4 distribution and that coupling of a synthetic GAP to membrane flows is sufficient to establish the rod shape. Thus, membrane flows induced by Cdc42-dependent exocytosis form a negative feedback restricting the zone of Cdc42 activity. American Association for the Advancement of Science 2021-09-17 /pmc/articles/PMC8448446/ /pubmed/34533984 http://dx.doi.org/10.1126/sciadv.abg6718 Text en Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Biomedicine and Life Sciences
Gerganova, Veneta
Lamas, Iker
Rutkowski, David M.
Vještica, Aleksandar
Castro, Daniela Gallo
Vincenzetti, Vincent
Vavylonis, Dimitrios
Martin, Sophie G.
Cell patterning by secretion-induced plasma membrane flows
title Cell patterning by secretion-induced plasma membrane flows
title_full Cell patterning by secretion-induced plasma membrane flows
title_fullStr Cell patterning by secretion-induced plasma membrane flows
title_full_unstemmed Cell patterning by secretion-induced plasma membrane flows
title_short Cell patterning by secretion-induced plasma membrane flows
title_sort cell patterning by secretion-induced plasma membrane flows
topic Biomedicine and Life Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8448446/
https://www.ncbi.nlm.nih.gov/pubmed/34533984
http://dx.doi.org/10.1126/sciadv.abg6718
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