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      Cell patterning by secretion-induced plasma membrane flows

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          Abstract

          Abstract

          Exocytosis causes bulk membrane flows that drag associated proteins and form a negative feedback restricting the exocytic site.

          Abstract

          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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          Most cited references94

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          TrackMate: An open and extensible platform for single-particle tracking.

          We present TrackMate, an open source Fiji plugin for the automated, semi-automated, and manual tracking of single-particles. It offers a versatile and modular solution that works out of the box for end users, through a simple and intuitive user interface. It is also easily scriptable and adaptable, operating equally well on 1D over time, 2D over time, 3D over time, or other single and multi-channel image variants. TrackMate provides several visualization and analysis tools that aid in assessing the relevance of results. The utility of TrackMate is further enhanced through its ability to be readily customized to meet specific tracking problems. TrackMate is an extensible platform where developers can easily write their own detection, particle linking, visualization or analysis algorithms within the TrackMate environment. This evolving framework provides researchers with the opportunity to quickly develop and optimize new algorithms based on existing TrackMate modules without the need of having to write de novo user interfaces, including visualization, analysis and exporting tools. The current capabilities of TrackMate are presented in the context of three different biological problems. First, we perform Caenorhabditis-elegans lineage analysis to assess how light-induced damage during imaging impairs its early development. Our TrackMate-based lineage analysis indicates the lack of a cell-specific light-sensitive mechanism. Second, we investigate the recruitment of NEMO (NF-κB essential modulator) clusters in fibroblasts after stimulation by the cytokine IL-1 and show that photodamage can generate artifacts in the shape of TrackMate characterized movements that confuse motility analysis. Finally, we validate the use of TrackMate for quantitative lifetime analysis of clathrin-mediated endocytosis in plant cells.
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            Exact stochastic simulation of coupled chemical reactions

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              Mechanics of membrane fusion

              Diverse membrane fusion reactions in biology involve close contact between two lipid bilayers, followed by the local distortion of the individual bilayers and reformation into a single, merged membrane. We consider the structures and energies of the fusion intermediates identified in experimental and theoretical work on protein-free lipid bilayers. On the basis of this analysis, we then discuss the conserved fusion-through-hemifusion pathway of merger between biological membranes and propose that the entire progression, from the close juxtaposition of membrane bilayers to the expansion of a fusion pore, is controlled by protein-generated membrane stresses.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ValidationRole: VisualizationRole: Writing - review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing - review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Resources
                Role: Investigation
                Role: InvestigationRole: ResourcesRole: Validation
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing
                Journal
                Sci Adv
                sciadv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                September 2021
                17 September 2021
                : 7
                : 38
                : eabg6718
                Affiliations
                [1 ]Department of Fundamental Microbiology, University of Lausanne, CH-1015, Switzerland.
                [2 ]Department of Physics, Lehigh University, Bethlehem, PA 18015, USA.
                Author notes
                [* ]Corresponding author. Email: sophie.martin@ 123456unil.ch (S.G.M.); vavylonis@ 123456lehigh.edu (D.V.)
                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-1491-1249
                https://orcid.org/0000-0001-6027-0377
                https://orcid.org/0000-0003-0430-9163
                https://orcid.org/0000-0002-3095-4169
                https://orcid.org/0000-0003-1802-3262
                https://orcid.org/0000-0002-5317-2557
                Article
                abg6718
                10.1126/sciadv.abg6718
                8448446
                34533984
                8c356592-3ab9-4b60-bca5-3078a84795f2
                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).

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, 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.

                History
                : 20 January 2021
                : 26 July 2021
                Funding
                Funded by: doi http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R01GM114201
                Funded by: doi http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R35GM136372
                Funded by: doi http://dx.doi.org/10.13039/100010663, H2020 European Research Council;
                Award ID: CellFusion
                Funded by: doi http://dx.doi.org/10.13039/501100001711, Swiss National Science Foundation;
                Award ID: 310030B_176396
                Categories
                Research Article
                Biomedicine and Life Sciences
                SciAdv r-articles
                Biophysics
                Cell Biology
                Cell Biology
                Custom metadata
                Fritzie Benzon

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