Activated membrane patches guide chemotactic cell motility
Many eukaryotic cells are able to crawl on surfaces and guide their motility based on environmental cues. These cues are interpreted by signaling systems which couple to cell mechanics; indeed membrane protrusions in crawling cells are often accompanied by activated membrane patches, which are local...
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description | Many eukaryotic cells are able to crawl on surfaces and guide their motility based on environmental cues. These cues are interpreted by signaling systems which couple to cell mechanics; indeed membrane protrusions in crawling cells are often accompanied by activated membrane patches, which are localized areas of increased concentration of one or more signaling components. To determine how these patches are related to cell motion, we examine the spatial localization of RasGTP in chemotaxing Dictyostelium discoideum cells under conditions where the vertical extent of the cell was restricted. Quantitative analyses of the data reveal a high degree of spatial correlation between patches of activated Ras and membrane protrusions. Based on these findings, we formulate a model for amoeboid cell motion that consists of two coupled modules. The first module utilizes a recently developed two-component reaction diffusion model that generates transient and localized areas of elevated concentration of one of the components along the membrane. The activated patches determine the location of membrane protrusions (and overall cell motion) that are computed in the second module, which also takes into account the cortical tension and the availability of protrusion resources. We show that our model is able to produce realistic amoeboid-like motion and that our numerical results are consistent with experimentally observed pseudopod dynamics. Specifically, we show that the commonly observed splitting of pseudopods can result directly from the dynamics of the signaling patches. |
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These cues are interpreted by signaling systems which couple to cell mechanics; indeed membrane protrusions in crawling cells are often accompanied by activated membrane patches, which are localized areas of increased concentration of one or more signaling components. To determine how these patches are related to cell motion, we examine the spatial localization of RasGTP in chemotaxing Dictyostelium discoideum cells under conditions where the vertical extent of the cell was restricted. Quantitative analyses of the data reveal a high degree of spatial correlation between patches of activated Ras and membrane protrusions. Based on these findings, we formulate a model for amoeboid cell motion that consists of two coupled modules. The first module utilizes a recently developed two-component reaction diffusion model that generates transient and localized areas of elevated concentration of one of the components along the membrane. The activated patches determine the location of membrane protrusions (and overall cell motion) that are computed in the second module, which also takes into account the cortical tension and the availability of protrusion resources. We show that our model is able to produce realistic amoeboid-like motion and that our numerical results are consistent with experimentally observed pseudopod dynamics. Specifically, we show that the commonly observed splitting of pseudopods can result directly from the dynamics of the signaling patches.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1002044</identifier><identifier>PMID: 21738453</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Biology ; Cell membranes ; Cell Movement - physiology ; Cells ; Cellular signal transduction ; Chemotaxis - physiology ; Computer Simulation ; Dictyostelium - cytology ; Dictyostelium - physiology ; Guanosine Triphosphate ; Mechanics ; Microfluidic Analytical Techniques ; Models, Biological ; Motility ; Physiological aspects ; Proteins ; Pseudopodia - physiology ; ras Proteins ; Signal Transduction ; Single-Cell Analysis</subject><ispartof>PLoS computational biology, 2011-06, Vol.7 (6), p.e1002044-e1002044</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>Hecht et al. 2011</rights><rights>2011 Hecht et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Hecht I, Skoge ML, Charest PG, Ben-Jacob E, Firtel RA, et al. (2011) Activated Membrane Patches Guide Chemotactic Cell Motility. 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These cues are interpreted by signaling systems which couple to cell mechanics; indeed membrane protrusions in crawling cells are often accompanied by activated membrane patches, which are localized areas of increased concentration of one or more signaling components. To determine how these patches are related to cell motion, we examine the spatial localization of RasGTP in chemotaxing Dictyostelium discoideum cells under conditions where the vertical extent of the cell was restricted. Quantitative analyses of the data reveal a high degree of spatial correlation between patches of activated Ras and membrane protrusions. Based on these findings, we formulate a model for amoeboid cell motion that consists of two coupled modules. The first module utilizes a recently developed two-component reaction diffusion model that generates transient and localized areas of elevated concentration of one of the components along the membrane. The activated patches determine the location of membrane protrusions (and overall cell motion) that are computed in the second module, which also takes into account the cortical tension and the availability of protrusion resources. We show that our model is able to produce realistic amoeboid-like motion and that our numerical results are consistent with experimentally observed pseudopod dynamics. Specifically, we show that the commonly observed splitting of pseudopods can result directly from the dynamics of the signaling patches.</description><subject>Biology</subject><subject>Cell membranes</subject><subject>Cell Movement - physiology</subject><subject>Cells</subject><subject>Cellular signal transduction</subject><subject>Chemotaxis - physiology</subject><subject>Computer Simulation</subject><subject>Dictyostelium - cytology</subject><subject>Dictyostelium - physiology</subject><subject>Guanosine Triphosphate</subject><subject>Mechanics</subject><subject>Microfluidic Analytical Techniques</subject><subject>Models, Biological</subject><subject>Motility</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Pseudopodia - physiology</subject><subject>ras Proteins</subject><subject>Signal Transduction</subject><subject>Single-Cell Analysis</subject><issn>1553-7358</issn><issn>1553-734X</issn><issn>1553-7358</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVkktv1DAQxyMEoqXwDRDkhjjs4mfscEBaVTxWqkDicbbGzjj1KomXOKnot8fLplX3iHzwePybv2fGUxQvKVlTrui7XZzHAbr13tmwpoQwIsSj4pxKyVeKS_34gX1WPEtpR0g26-ppccao4lpIfl6837gp3MCETdljb0cYsNzD5K4xle0cGiyz2ccJMuZKh11X5lPownT7vHjioUv4Ytkvil-fPv68_LK6-vZ5e7m5WrlKkWklhGM1p0RZVYu6VhIQGkUdSm9lzYW0hBCESnuBXiuKDTRUWQ2ceQmy4hfF66PuvovJLGUnQ3lemnKtM7E9Ek2EndmPoYfx1kQI5p8jjq2BMeffoQFvGYLQTHEQRHhorCcWGRBWKcVo1vqwvDbbHhuHwzRCdyJ6ejOEa9PGG8MpU5qSLPBmERjj7xnTZPqQDo3LrY1zMlpJxXgleSbXR7KFnFkYfMyCLq8G--DigD5k_4ZVpBb5xw_Sb08CMjPhn6mFOSWz_fH9P9ivp6w4sm6MKY3o78ulxByG7a7r5jBsZhm2HPbqYavug-6mi_8FsVfQ7Q</recordid><startdate>20110601</startdate><enddate>20110601</enddate><creator>Hecht, Inbal</creator><creator>Skoge, Monica L</creator><creator>Charest, Pascale G</creator><creator>Ben-Jacob, Eshel</creator><creator>Firtel, Richard A</creator><creator>Loomis, William F</creator><creator>Levine, Herbert</creator><creator>Rappel, Wouter-Jan</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20110601</creationdate><title>Activated membrane patches guide chemotactic cell motility</title><author>Hecht, Inbal ; Skoge, Monica L ; Charest, Pascale G ; Ben-Jacob, Eshel ; Firtel, Richard A ; Loomis, William F ; Levine, Herbert ; Rappel, Wouter-Jan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c670t-44c293107b7949975aead71ce5fb59345b000ea68f4ef871edad17b8a32f5a563</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Biology</topic><topic>Cell membranes</topic><topic>Cell Movement - physiology</topic><topic>Cells</topic><topic>Cellular signal transduction</topic><topic>Chemotaxis - physiology</topic><topic>Computer Simulation</topic><topic>Dictyostelium - cytology</topic><topic>Dictyostelium - physiology</topic><topic>Guanosine Triphosphate</topic><topic>Mechanics</topic><topic>Microfluidic Analytical Techniques</topic><topic>Models, Biological</topic><topic>Motility</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>Pseudopodia - physiology</topic><topic>ras Proteins</topic><topic>Signal Transduction</topic><topic>Single-Cell Analysis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hecht, Inbal</creatorcontrib><creatorcontrib>Skoge, Monica L</creatorcontrib><creatorcontrib>Charest, Pascale G</creatorcontrib><creatorcontrib>Ben-Jacob, Eshel</creatorcontrib><creatorcontrib>Firtel, Richard A</creatorcontrib><creatorcontrib>Loomis, William F</creatorcontrib><creatorcontrib>Levine, Herbert</creatorcontrib><creatorcontrib>Rappel, Wouter-Jan</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hecht, Inbal</au><au>Skoge, Monica L</au><au>Charest, Pascale G</au><au>Ben-Jacob, Eshel</au><au>Firtel, Richard A</au><au>Loomis, William F</au><au>Levine, Herbert</au><au>Rappel, Wouter-Jan</au><au>Bourne, Philip E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Activated membrane patches guide chemotactic cell motility</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2011-06-01</date><risdate>2011</risdate><volume>7</volume><issue>6</issue><spage>e1002044</spage><epage>e1002044</epage><pages>e1002044-e1002044</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>Many eukaryotic cells are able to crawl on surfaces and guide their motility based on environmental cues. These cues are interpreted by signaling systems which couple to cell mechanics; indeed membrane protrusions in crawling cells are often accompanied by activated membrane patches, which are localized areas of increased concentration of one or more signaling components. To determine how these patches are related to cell motion, we examine the spatial localization of RasGTP in chemotaxing Dictyostelium discoideum cells under conditions where the vertical extent of the cell was restricted. Quantitative analyses of the data reveal a high degree of spatial correlation between patches of activated Ras and membrane protrusions. Based on these findings, we formulate a model for amoeboid cell motion that consists of two coupled modules. The first module utilizes a recently developed two-component reaction diffusion model that generates transient and localized areas of elevated concentration of one of the components along the membrane. The activated patches determine the location of membrane protrusions (and overall cell motion) that are computed in the second module, which also takes into account the cortical tension and the availability of protrusion resources. We show that our model is able to produce realistic amoeboid-like motion and that our numerical results are consistent with experimentally observed pseudopod dynamics. Specifically, we show that the commonly observed splitting of pseudopods can result directly from the dynamics of the signaling patches.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21738453</pmid><doi>10.1371/journal.pcbi.1002044</doi><oa>free_for_read</oa></addata></record> |
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subjects | Biology Cell membranes Cell Movement - physiology Cells Cellular signal transduction Chemotaxis - physiology Computer Simulation Dictyostelium - cytology Dictyostelium - physiology Guanosine Triphosphate Mechanics Microfluidic Analytical Techniques Models, Biological Motility Physiological aspects Proteins Pseudopodia - physiology ras Proteins Signal Transduction Single-Cell Analysis |
title | Activated membrane patches guide chemotactic cell motility |
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