Local Membrane Curvature Pins and Guides Excitable Membrane Waves in Chemotactic and Macropinocytic Cells - Biomedical Insights From an Innovative Simple Model
PIP3 dynamics observed in membranes are responsible for the protruding edge formation in cancer and amoeboid cells. The mechanisms that maintain those PIP3 domains in three-dimensional space remain elusive, due to limitations in observation and analysis techniques. Recently, a strong relation betwee...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-09-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2021.670943/full |
| _version_ | 1818717496388091904 |
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| author | Marcel Hörning Marcel Hörning Torsten Bullmann Tatsuo Shibata |
| author_facet | Marcel Hörning Marcel Hörning Torsten Bullmann Tatsuo Shibata |
| author_sort | Marcel Hörning |
| collection | DOAJ |
| description | PIP3 dynamics observed in membranes are responsible for the protruding edge formation in cancer and amoeboid cells. The mechanisms that maintain those PIP3 domains in three-dimensional space remain elusive, due to limitations in observation and analysis techniques. Recently, a strong relation between the cell geometry, the spatial confinement of the membrane, and the excitable signal transduction system has been revealed by Hörning and Shibata (2019) using a novel 3D spatiotemporal analysis methodology that enables the study of membrane signaling on the entire membrane (Hörning and Shibata, 2019). Here, using 3D spatial fluctuation and phase map analysis on actin polymerization inhibited Dictyostelium cells, we reveal a spatial asymmetry of PIP3 signaling on the membrane that is mediated by the contact perimeter of the plasma membrane — the spatial boundary around the cell-substrate adhered area on the plasma membrane. We show that the contact perimeter guides PIP3 waves and acts as a pinning site of PIP3 phase singularities, that is, the center point of spiral waves. The contact perimeter serves as a diffusion influencing boundary that is regulated by a cell size- and shape-dependent curvature. Our findings suggest an underlying mechanism that explains how local curvature can favor actin polymerization when PIP3 domains get pinned at the curved protrusive membrane edges in amoeboid cells. |
| first_indexed | 2024-12-17T19:36:05Z |
| format | Article |
| id | doaj.art-585b3f3e6a264b0eb7666af0c475b33d |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-12-17T19:36:05Z |
| publishDate | 2021-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-585b3f3e6a264b0eb7666af0c475b33d2022-12-21T21:35:09ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-09-01910.3389/fcell.2021.670943670943Local Membrane Curvature Pins and Guides Excitable Membrane Waves in Chemotactic and Macropinocytic Cells - Biomedical Insights From an Innovative Simple ModelMarcel Hörning0Marcel Hörning1Torsten Bullmann2Tatsuo Shibata3Institute of Biomaterials and Biomolecular Systems, University of Stuttgart, Stuttgart, GermanyLaboratory for Physical Biology, RIKEN Center for Biosystems Dynamics Research, Kobe, JapanCarl-Ludwig-Institute for Physiology, University of Leipzig, Leipzig, GermanyLaboratory for Physical Biology, RIKEN Center for Biosystems Dynamics Research, Kobe, JapanPIP3 dynamics observed in membranes are responsible for the protruding edge formation in cancer and amoeboid cells. The mechanisms that maintain those PIP3 domains in three-dimensional space remain elusive, due to limitations in observation and analysis techniques. Recently, a strong relation between the cell geometry, the spatial confinement of the membrane, and the excitable signal transduction system has been revealed by Hörning and Shibata (2019) using a novel 3D spatiotemporal analysis methodology that enables the study of membrane signaling on the entire membrane (Hörning and Shibata, 2019). Here, using 3D spatial fluctuation and phase map analysis on actin polymerization inhibited Dictyostelium cells, we reveal a spatial asymmetry of PIP3 signaling on the membrane that is mediated by the contact perimeter of the plasma membrane — the spatial boundary around the cell-substrate adhered area on the plasma membrane. We show that the contact perimeter guides PIP3 waves and acts as a pinning site of PIP3 phase singularities, that is, the center point of spiral waves. The contact perimeter serves as a diffusion influencing boundary that is regulated by a cell size- and shape-dependent curvature. Our findings suggest an underlying mechanism that explains how local curvature can favor actin polymerization when PIP3 domains get pinned at the curved protrusive membrane edges in amoeboid cells.https://www.frontiersin.org/articles/10.3389/fcell.2021.670943/fulldissipative structurebiochemical oscillationsmall systemssignal transductionchemotaxisPIP3 |
| spellingShingle | Marcel Hörning Marcel Hörning Torsten Bullmann Tatsuo Shibata Local Membrane Curvature Pins and Guides Excitable Membrane Waves in Chemotactic and Macropinocytic Cells - Biomedical Insights From an Innovative Simple Model Frontiers in Cell and Developmental Biology dissipative structure biochemical oscillation small systems signal transduction chemotaxis PIP3 |
| title | Local Membrane Curvature Pins and Guides Excitable Membrane Waves in Chemotactic and Macropinocytic Cells - Biomedical Insights From an Innovative Simple Model |
| title_full | Local Membrane Curvature Pins and Guides Excitable Membrane Waves in Chemotactic and Macropinocytic Cells - Biomedical Insights From an Innovative Simple Model |
| title_fullStr | Local Membrane Curvature Pins and Guides Excitable Membrane Waves in Chemotactic and Macropinocytic Cells - Biomedical Insights From an Innovative Simple Model |
| title_full_unstemmed | Local Membrane Curvature Pins and Guides Excitable Membrane Waves in Chemotactic and Macropinocytic Cells - Biomedical Insights From an Innovative Simple Model |
| title_short | Local Membrane Curvature Pins and Guides Excitable Membrane Waves in Chemotactic and Macropinocytic Cells - Biomedical Insights From an Innovative Simple Model |
| title_sort | local membrane curvature pins and guides excitable membrane waves in chemotactic and macropinocytic cells biomedical insights from an innovative simple model |
| topic | dissipative structure biochemical oscillation small systems signal transduction chemotaxis PIP3 |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2021.670943/full |
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