Polarity mechanisms such as contact inhibition of locomotion regulate persistent rotational motion of mammalian cells on micropatterns
Significance During the growth of an embryo or the spreading of a tumor, cells may travel collectively. We study a computational model of a simple example of collective migration: two cells confined to a square adhesive pattern. In this confinement, some cell types rotate, whereas others do not. We...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2014-10, Vol.111 (41), p.14770-14775 |
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creator | Camley, Brian A. Zhang, Yunsong Zhao, Yanxiang Li, Bo Ben-Jacob, Eshel Levine, Herbert Rappel, Wouter-Jan |
description | Significance During the growth of an embryo or the spreading of a tumor, cells may travel collectively. We study a computational model of a simple example of collective migration: two cells confined to a square adhesive pattern. In this confinement, some cell types rotate, whereas others do not. We model these crawling cells, the forces between them, and several possible ways that the cells could choose what direction they will crawl—their “polarity mechanism.” We show that the cell polarity mechanism can control whether the pairs of cells rotate or remain fixed. This suggests that we can learn about how large groups of cells choose their direction by studying the rotation of pairs.
Pairs of endothelial cells on adhesive micropatterns rotate persistently, but pairs of fibroblasts do not; coherent rotation is present in normal mammary acini and kidney cells but absent in cancerous cells. Why? To answer this question, we develop a computational model of pairs of mammalian cells on adhesive micropatterns using a phase field method and study the conditions under which persistent rotational motion (PRM) emerges. Our model couples the shape of the cell, the cell’s internal chemical polarity, and interactions between cells such as volume exclusion and adhesion. We show that PRM can emerge from this minimal model and that the cell-cell interface may be influenced by the nucleus. We study the effect of various cell polarity mechanisms on rotational motion, including contact inhibition of locomotion, neighbor alignment, and velocity alignment, where cells align their polarity to their velocity. These polarity mechanisms strongly regulate PRM: Small differences in polarity mechanisms can create significant differences in collective rotation. We argue that the existence or absence of rotation under confinement may lead to insight into the cell’s methods for coordinating collective cell motility. |
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Pairs of endothelial cells on adhesive micropatterns rotate persistently, but pairs of fibroblasts do not; coherent rotation is present in normal mammary acini and kidney cells but absent in cancerous cells. Why? To answer this question, we develop a computational model of pairs of mammalian cells on adhesive micropatterns using a phase field method and study the conditions under which persistent rotational motion (PRM) emerges. Our model couples the shape of the cell, the cell’s internal chemical polarity, and interactions between cells such as volume exclusion and adhesion. We show that PRM can emerge from this minimal model and that the cell-cell interface may be influenced by the nucleus. We study the effect of various cell polarity mechanisms on rotational motion, including contact inhibition of locomotion, neighbor alignment, and velocity alignment, where cells align their polarity to their velocity. These polarity mechanisms strongly regulate PRM: Small differences in polarity mechanisms can create significant differences in collective rotation. We argue that the existence or absence of rotation under confinement may lead to insight into the cell’s methods for coordinating collective cell motility.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1414498111</identifier><identifier>PMID: 25258412</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animal migration behavior ; Animals ; Biological Sciences ; Cell adhesion ; Cell adhesion & migration ; Cell Count ; Cell membranes ; Cell motility ; Cell Movement ; Cell Polarity ; Cells ; Cellular biology ; Contact Inhibition ; Endothelial cells ; Endothelium ; Epithelial cells ; Kinetics ; Locomotion ; Mammals ; Mammals - metabolism ; Mathematical models ; Models, Biological ; Motility ; Physical Sciences ; Rotation</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2014-10, Vol.111 (41), p.14770-14775</ispartof><rights>copyright © 1993–2008 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Oct 14, 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c562t-40a216d62197a70068cf117eabc6630b22f621d714fc3a3470a231908811ab0c3</citedby><cites>FETCH-LOGICAL-c562t-40a216d62197a70068cf117eabc6630b22f621d714fc3a3470a231908811ab0c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/111/41.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/43190152$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/43190152$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,729,782,786,805,887,27931,27932,53798,53800,58024,58257</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25258412$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Camley, Brian A.</creatorcontrib><creatorcontrib>Zhang, Yunsong</creatorcontrib><creatorcontrib>Zhao, Yanxiang</creatorcontrib><creatorcontrib>Li, Bo</creatorcontrib><creatorcontrib>Ben-Jacob, Eshel</creatorcontrib><creatorcontrib>Levine, Herbert</creatorcontrib><creatorcontrib>Rappel, Wouter-Jan</creatorcontrib><title>Polarity mechanisms such as contact inhibition of locomotion regulate persistent rotational motion of mammalian cells on micropatterns</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Significance During the growth of an embryo or the spreading of a tumor, cells may travel collectively. We study a computational model of a simple example of collective migration: two cells confined to a square adhesive pattern. In this confinement, some cell types rotate, whereas others do not. We model these crawling cells, the forces between them, and several possible ways that the cells could choose what direction they will crawl—their “polarity mechanism.” We show that the cell polarity mechanism can control whether the pairs of cells rotate or remain fixed. This suggests that we can learn about how large groups of cells choose their direction by studying the rotation of pairs.
Pairs of endothelial cells on adhesive micropatterns rotate persistently, but pairs of fibroblasts do not; coherent rotation is present in normal mammary acini and kidney cells but absent in cancerous cells. Why? To answer this question, we develop a computational model of pairs of mammalian cells on adhesive micropatterns using a phase field method and study the conditions under which persistent rotational motion (PRM) emerges. Our model couples the shape of the cell, the cell’s internal chemical polarity, and interactions between cells such as volume exclusion and adhesion. We show that PRM can emerge from this minimal model and that the cell-cell interface may be influenced by the nucleus. We study the effect of various cell polarity mechanisms on rotational motion, including contact inhibition of locomotion, neighbor alignment, and velocity alignment, where cells align their polarity to their velocity. These polarity mechanisms strongly regulate PRM: Small differences in polarity mechanisms can create significant differences in collective rotation. We argue that the existence or absence of rotation under confinement may lead to insight into the cell’s methods for coordinating collective cell motility.</description><subject>Animal migration behavior</subject><subject>Animals</subject><subject>Biological Sciences</subject><subject>Cell adhesion</subject><subject>Cell adhesion & migration</subject><subject>Cell Count</subject><subject>Cell membranes</subject><subject>Cell motility</subject><subject>Cell Movement</subject><subject>Cell Polarity</subject><subject>Cells</subject><subject>Cellular biology</subject><subject>Contact Inhibition</subject><subject>Endothelial cells</subject><subject>Endothelium</subject><subject>Epithelial cells</subject><subject>Kinetics</subject><subject>Locomotion</subject><subject>Mammals</subject><subject>Mammals - metabolism</subject><subject>Mathematical models</subject><subject>Models, Biological</subject><subject>Motility</subject><subject>Physical Sciences</subject><subject>Rotation</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUtv1DAUhSMEokNhzQqwxIZN2nsdx042lVDFS6oEEnRt3XicGY-SeLAdpP4BfjdOZxgeK8s-3z26PqconiNcIKjqcj9RvECBQrQNIj4oVggtllK08LBYAXBVNoKLs-JJjDsAaOsGHhdnvOZ1I5Cvip9f_EDBpTs2WrOlycUxsjibLaPIjJ8SmcTctHWdS85PzPds8MaP_v4W7GYeKFm2tyG6mOyUWPCJFpEGdqTyzEjjSIOjiRk7DJHl19GZ4PeUkg1TfFo86mmI9tnxPC9u37_7dv2xvPn84dP125vS1JKnUgBxlGvJsVWkAGRjekRlqTNSVtBx3mdtrVD0pqJKqMxX2EKTw6EOTHVeXB1893M32rXJCwca9D64kcKd9uT0v8rktnrjf2jBoZaA2eDN0SD477ONSY8uLn-iyfo5apTI20YqaDL6-j905-eQc7mnqhpb2daZujxQOY0Yg-1PyyDopWO9dKz_dJwnXv79hxP_u9QMsCOwTJ7sELXAbKQUZOTFAdnF5MOJEUtYWC8Wrw56T17TJriob79yQAmAAlDV1S_rEMLF</recordid><startdate>20141014</startdate><enddate>20141014</enddate><creator>Camley, Brian A.</creator><creator>Zhang, Yunsong</creator><creator>Zhao, Yanxiang</creator><creator>Li, Bo</creator><creator>Ben-Jacob, Eshel</creator><creator>Levine, Herbert</creator><creator>Rappel, Wouter-Jan</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20141014</creationdate><title>Polarity mechanisms such as contact inhibition of locomotion regulate persistent rotational motion of mammalian cells on micropatterns</title><author>Camley, Brian A. ; Zhang, Yunsong ; Zhao, Yanxiang ; Li, Bo ; Ben-Jacob, Eshel ; Levine, Herbert ; Rappel, Wouter-Jan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c562t-40a216d62197a70068cf117eabc6630b22f621d714fc3a3470a231908811ab0c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animal migration behavior</topic><topic>Animals</topic><topic>Biological Sciences</topic><topic>Cell adhesion</topic><topic>Cell adhesion & migration</topic><topic>Cell Count</topic><topic>Cell membranes</topic><topic>Cell motility</topic><topic>Cell Movement</topic><topic>Cell Polarity</topic><topic>Cells</topic><topic>Cellular biology</topic><topic>Contact Inhibition</topic><topic>Endothelial cells</topic><topic>Endothelium</topic><topic>Epithelial cells</topic><topic>Kinetics</topic><topic>Locomotion</topic><topic>Mammals</topic><topic>Mammals - metabolism</topic><topic>Mathematical models</topic><topic>Models, Biological</topic><topic>Motility</topic><topic>Physical Sciences</topic><topic>Rotation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Camley, Brian A.</creatorcontrib><creatorcontrib>Zhang, Yunsong</creatorcontrib><creatorcontrib>Zhao, Yanxiang</creatorcontrib><creatorcontrib>Li, Bo</creatorcontrib><creatorcontrib>Ben-Jacob, Eshel</creatorcontrib><creatorcontrib>Levine, Herbert</creatorcontrib><creatorcontrib>Rappel, Wouter-Jan</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Camley, Brian A.</au><au>Zhang, Yunsong</au><au>Zhao, Yanxiang</au><au>Li, Bo</au><au>Ben-Jacob, Eshel</au><au>Levine, Herbert</au><au>Rappel, Wouter-Jan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Polarity mechanisms such as contact inhibition of locomotion regulate persistent rotational motion of mammalian cells on micropatterns</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2014-10-14</date><risdate>2014</risdate><volume>111</volume><issue>41</issue><spage>14770</spage><epage>14775</epage><pages>14770-14775</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Significance During the growth of an embryo or the spreading of a tumor, cells may travel collectively. We study a computational model of a simple example of collective migration: two cells confined to a square adhesive pattern. In this confinement, some cell types rotate, whereas others do not. We model these crawling cells, the forces between them, and several possible ways that the cells could choose what direction they will crawl—their “polarity mechanism.” We show that the cell polarity mechanism can control whether the pairs of cells rotate or remain fixed. This suggests that we can learn about how large groups of cells choose their direction by studying the rotation of pairs.
Pairs of endothelial cells on adhesive micropatterns rotate persistently, but pairs of fibroblasts do not; coherent rotation is present in normal mammary acini and kidney cells but absent in cancerous cells. Why? To answer this question, we develop a computational model of pairs of mammalian cells on adhesive micropatterns using a phase field method and study the conditions under which persistent rotational motion (PRM) emerges. Our model couples the shape of the cell, the cell’s internal chemical polarity, and interactions between cells such as volume exclusion and adhesion. We show that PRM can emerge from this minimal model and that the cell-cell interface may be influenced by the nucleus. We study the effect of various cell polarity mechanisms on rotational motion, including contact inhibition of locomotion, neighbor alignment, and velocity alignment, where cells align their polarity to their velocity. These polarity mechanisms strongly regulate PRM: Small differences in polarity mechanisms can create significant differences in collective rotation. We argue that the existence or absence of rotation under confinement may lead to insight into the cell’s methods for coordinating collective cell motility.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>25258412</pmid><doi>10.1073/pnas.1414498111</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animal migration behavior Animals Biological Sciences Cell adhesion Cell adhesion & migration Cell Count Cell membranes Cell motility Cell Movement Cell Polarity Cells Cellular biology Contact Inhibition Endothelial cells Endothelium Epithelial cells Kinetics Locomotion Mammals Mammals - metabolism Mathematical models Models, Biological Motility Physical Sciences Rotation |
title | Polarity mechanisms such as contact inhibition of locomotion regulate persistent rotational motion of mammalian cells on micropatterns |
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