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Coordination of contractility, adhesion and flow in migrating Physarum amoebae
This work examines the relationship between spatio-temporal coordination of intracellular flow and traction stress and the speed of amoeboid locomotion of microplasmodia of Physarum polycephalum. We simultaneously perform particle image velocimetry and traction stress microscopy to measure the veloc...
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Published in: | Journal of the Royal Society interface 2015-05, Vol.12 (106), p.20141359-20141359 |
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container_end_page | 20141359 |
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creator | Lewis, Owen L. Zhang, Shun Guy, Robert D. del Álamo, Juan C. |
description | This work examines the relationship between spatio-temporal coordination of intracellular flow and traction stress and the speed of amoeboid locomotion of microplasmodia of Physarum polycephalum. We simultaneously perform particle image velocimetry and traction stress microscopy to measure the velocity of cytoplasmic flow and the stresses applied to the substrate by migrating Physarum microamoebae. In parallel, we develop a mathematical model of a motile cell which includes forces from the viscous cytosol, a poro-elastic, contractile cytoskeleton and adhesive interactions with the substrate. Our experiments show that flow and traction stress exhibit back-to-front-directed waves with a distinct phase difference. The model demonstrates that the direction and speed of locomotion are determined by this coordination between contraction, flow and adhesion. Using the model, we identify forms of coordination that generate model predictions consistent with experiments. We demonstrate that this coordination produces near optimal migration speed and is insensitive to heterogeneity in substrate adhesiveness. While it is generally thought that amoeboid motility is robust to changes in extracellular geometry and the nature of extracellular adhesion, our results demonstrate that coordination of adhesive forces is essential to producing robust migration. |
doi_str_mv | 10.1098/rsif.2014.1359 |
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We simultaneously perform particle image velocimetry and traction stress microscopy to measure the velocity of cytoplasmic flow and the stresses applied to the substrate by migrating Physarum microamoebae. In parallel, we develop a mathematical model of a motile cell which includes forces from the viscous cytosol, a poro-elastic, contractile cytoskeleton and adhesive interactions with the substrate. Our experiments show that flow and traction stress exhibit back-to-front-directed waves with a distinct phase difference. The model demonstrates that the direction and speed of locomotion are determined by this coordination between contraction, flow and adhesion. Using the model, we identify forms of coordination that generate model predictions consistent with experiments. We demonstrate that this coordination produces near optimal migration speed and is insensitive to heterogeneity in substrate adhesiveness. While it is generally thought that amoeboid motility is robust to changes in extracellular geometry and the nature of extracellular adhesion, our results demonstrate that coordination of adhesive forces is essential to producing robust migration.</description><identifier>ISSN: 1742-5689</identifier><identifier>EISSN: 1742-5662</identifier><identifier>DOI: 10.1098/rsif.2014.1359</identifier><identifier>PMID: 25904525</identifier><language>eng</language><publisher>England: The Royal Society</publisher><subject>Amoeboid Motility ; Cell Adhesion - physiology ; Cell Locomotion ; Cell Movement - physiology ; Computer Simulation ; Contractile Proteins - physiology ; Cytoplasmic Streaming ; Mechanotransduction, Cellular - physiology ; Microfluidics - methods ; Models, Biological ; Particle Image Velocimetry ; Physarum ; Physarum polycephalum ; Shear Strength - physiology ; Traction Force Microscopy</subject><ispartof>Journal of the Royal Society interface, 2015-05, Vol.12 (106), p.20141359-20141359</ispartof><rights>2015 The Author(s) Published by the Royal Society. All rights reserved.</rights><rights>2015 The Author(s) Published by the Royal Society. All rights reserved. 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c427t-6661508e839374f9a31acbdb9a515ecb727532cad8ec1fd4d3318c8c9e2e947f3</citedby><cites>FETCH-LOGICAL-c427t-6661508e839374f9a31acbdb9a515ecb727532cad8ec1fd4d3318c8c9e2e947f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4424669/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4424669/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25904525$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lewis, Owen L.</creatorcontrib><creatorcontrib>Zhang, Shun</creatorcontrib><creatorcontrib>Guy, Robert D.</creatorcontrib><creatorcontrib>del Álamo, Juan C.</creatorcontrib><title>Coordination of contractility, adhesion and flow in migrating Physarum amoebae</title><title>Journal of the Royal Society interface</title><addtitle>J. R. Soc. Interface</addtitle><addtitle>J R Soc Interface</addtitle><description>This work examines the relationship between spatio-temporal coordination of intracellular flow and traction stress and the speed of amoeboid locomotion of microplasmodia of Physarum polycephalum. We simultaneously perform particle image velocimetry and traction stress microscopy to measure the velocity of cytoplasmic flow and the stresses applied to the substrate by migrating Physarum microamoebae. In parallel, we develop a mathematical model of a motile cell which includes forces from the viscous cytosol, a poro-elastic, contractile cytoskeleton and adhesive interactions with the substrate. Our experiments show that flow and traction stress exhibit back-to-front-directed waves with a distinct phase difference. The model demonstrates that the direction and speed of locomotion are determined by this coordination between contraction, flow and adhesion. Using the model, we identify forms of coordination that generate model predictions consistent with experiments. We demonstrate that this coordination produces near optimal migration speed and is insensitive to heterogeneity in substrate adhesiveness. While it is generally thought that amoeboid motility is robust to changes in extracellular geometry and the nature of extracellular adhesion, our results demonstrate that coordination of adhesive forces is essential to producing robust migration.</description><subject>Amoeboid Motility</subject><subject>Cell Adhesion - physiology</subject><subject>Cell Locomotion</subject><subject>Cell Movement - physiology</subject><subject>Computer Simulation</subject><subject>Contractile Proteins - physiology</subject><subject>Cytoplasmic Streaming</subject><subject>Mechanotransduction, Cellular - physiology</subject><subject>Microfluidics - methods</subject><subject>Models, Biological</subject><subject>Particle Image Velocimetry</subject><subject>Physarum</subject><subject>Physarum polycephalum</subject><subject>Shear Strength - physiology</subject><subject>Traction Force Microscopy</subject><issn>1742-5689</issn><issn>1742-5662</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNqFkTtPwzAURi0EoqWwMqKMDLTEr9hekFDFS0LAALPlOE7rKrGLnYDy70nUUsGAmGzrnnt0fT8ATmE6g6nglyHacoZSSGYQU7EHxpARNKVZhvZ3dy5G4CjGVZpihik9BCNERUooomPwNPc-FNapxnqX-DLR3jVB6cZWtukuElUsTRxKyhVJWfnPxLqktovQN7hF8rLsogptnajam1yZY3BQqiqak-05AW-3N6_z--nj893D_PpxqglizTTLMkhTbjgWmJFSKAyVzotcKAqp0TlDjGKkVcGNhmVBCowh11wLg4wgrMQTcLXxrtu8NoU2w9CVXAdbq9BJr6z8XXF2KRf-QxKCSJaJXnC-FQT_3prYyNpGbapKOePbKCGHYtgohP-jGaOccYJxj842qA4-xmDK3UQwlUNecshLDnnJwd43nP38xw7_DqgH8AYIvusX6rU1TSdXvg2uf_6l_QLmAaR4</recordid><startdate>20150506</startdate><enddate>20150506</enddate><creator>Lewis, Owen L.</creator><creator>Zhang, Shun</creator><creator>Guy, Robert D.</creator><creator>del Álamo, Juan C.</creator><general>The Royal Society</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>7X8</scope><scope>7QG</scope><scope>5PM</scope></search><sort><creationdate>20150506</creationdate><title>Coordination of contractility, adhesion and flow in migrating Physarum amoebae</title><author>Lewis, Owen L. ; Zhang, Shun ; Guy, Robert D. ; del Álamo, Juan C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c427t-6661508e839374f9a31acbdb9a515ecb727532cad8ec1fd4d3318c8c9e2e947f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Amoeboid Motility</topic><topic>Cell Adhesion - physiology</topic><topic>Cell Locomotion</topic><topic>Cell Movement - physiology</topic><topic>Computer Simulation</topic><topic>Contractile Proteins - physiology</topic><topic>Cytoplasmic Streaming</topic><topic>Mechanotransduction, Cellular - physiology</topic><topic>Microfluidics - methods</topic><topic>Models, Biological</topic><topic>Particle Image Velocimetry</topic><topic>Physarum</topic><topic>Physarum polycephalum</topic><topic>Shear Strength - physiology</topic><topic>Traction Force Microscopy</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lewis, Owen L.</creatorcontrib><creatorcontrib>Zhang, Shun</creatorcontrib><creatorcontrib>Guy, Robert D.</creatorcontrib><creatorcontrib>del Álamo, Juan C.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Animal Behavior Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of the Royal Society interface</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lewis, Owen L.</au><au>Zhang, Shun</au><au>Guy, Robert D.</au><au>del Álamo, Juan C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Coordination of contractility, adhesion and flow in migrating Physarum amoebae</atitle><jtitle>Journal of the Royal Society interface</jtitle><stitle>J. R. Soc. Interface</stitle><addtitle>J R Soc Interface</addtitle><date>2015-05-06</date><risdate>2015</risdate><volume>12</volume><issue>106</issue><spage>20141359</spage><epage>20141359</epage><pages>20141359-20141359</pages><issn>1742-5689</issn><eissn>1742-5662</eissn><abstract>This work examines the relationship between spatio-temporal coordination of intracellular flow and traction stress and the speed of amoeboid locomotion of microplasmodia of Physarum polycephalum. We simultaneously perform particle image velocimetry and traction stress microscopy to measure the velocity of cytoplasmic flow and the stresses applied to the substrate by migrating Physarum microamoebae. In parallel, we develop a mathematical model of a motile cell which includes forces from the viscous cytosol, a poro-elastic, contractile cytoskeleton and adhesive interactions with the substrate. Our experiments show that flow and traction stress exhibit back-to-front-directed waves with a distinct phase difference. The model demonstrates that the direction and speed of locomotion are determined by this coordination between contraction, flow and adhesion. Using the model, we identify forms of coordination that generate model predictions consistent with experiments. We demonstrate that this coordination produces near optimal migration speed and is insensitive to heterogeneity in substrate adhesiveness. While it is generally thought that amoeboid motility is robust to changes in extracellular geometry and the nature of extracellular adhesion, our results demonstrate that coordination of adhesive forces is essential to producing robust migration.</abstract><cop>England</cop><pub>The Royal Society</pub><pmid>25904525</pmid><doi>10.1098/rsif.2014.1359</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amoeboid Motility Cell Adhesion - physiology Cell Locomotion Cell Movement - physiology Computer Simulation Contractile Proteins - physiology Cytoplasmic Streaming Mechanotransduction, Cellular - physiology Microfluidics - methods Models, Biological Particle Image Velocimetry Physarum Physarum polycephalum Shear Strength - physiology Traction Force Microscopy |
title | Coordination of contractility, adhesion and flow in migrating Physarum amoebae |
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