Three-dimensional cell migration does not follow a random walk

Cell migration through 3D extracellular matrices is critical to the normal development of tissues and organs and in disease processes, yet adequate analytical tools to characterize 3D migration are lacking. Here, we quantified the migration patterns of individual fibrosarcoma cells on 2D substrates...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2014-03, Vol.111 (11), p.3949-3954
Hauptverfasser: Wu, Pei-Hsun, Giri, Anjil, Sun, Sean X., Wirtz, Denis
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 3954
container_issue 11
container_start_page 3949
container_title Proceedings of the National Academy of Sciences - PNAS
container_volume 111
creator Wu, Pei-Hsun
Giri, Anjil
Sun, Sean X.
Wirtz, Denis
description Cell migration through 3D extracellular matrices is critical to the normal development of tissues and organs and in disease processes, yet adequate analytical tools to characterize 3D migration are lacking. Here, we quantified the migration patterns of individual fibrosarcoma cells on 2D substrates and in 3D collagen matrices and found that 3D migration does not follow a random walk. Both 2D and 3D migration features a non-Gaussian, exponential mean cell velocity distribution, which we show is primarily a result of cell-to-cell variations. Unlike in the 2D case, 3D cell migration is anisotropic: velocity profiles display different speed and self-correlation processes in different directions, rendering the classical persistent random walk (PRW) model of cell migration inadequate. By incorporating cell heterogeneity and local anisotropy to the PRW model, we predict 3D cell motility over a wide range of matrix densities, which identifies density-independent emerging migratory properties. This analysis also reveals the unexpected robust relation between cell speed and persistence of migration over a wide range of matrix densities.
doi_str_mv 10.1073/pnas.1318967111
format Article
fullrecord <record><control><sourceid>jstor_proqu</sourceid><recordid>TN_cdi_proquest_miscellaneous_1516742857</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>23770964</jstor_id><sourcerecordid>23770964</sourcerecordid><originalsourceid>FETCH-LOGICAL-c500t-dfb6e3d6cf6a271a41812c64b5f0f08e58ab5c1a527ae78b02c5c379947720673</originalsourceid><addsrcrecordid>eNqNkc1P3DAQxS1EBQvtuaeWSFy4BGb8GV-QEAJaCakXOFuO40C2Sby1syD-e7zdZWl76mFkafybp3nzCPmMcIqg2NlitOkUGVZaKkTcITMEjaXkGnbJDICqsuKU75ODlOYAoEUFe2SfcqG5BDYj53eP0fuy6QY_pi6Mti-c7_ti6B6inXKjaIJPxRimog19H54LW0Q7NmEonm3_8yP50No--U-b95DcX1_dXX4rb3_cfL-8uC2dAJjKpq2lZ410rbRUoeVYIXWS16KFFiovKlsLh1ZQZb2qaqBOOKa05kpRkIodkvO17mJZD75xfpyi7c0idoONLybYzvz9M3aP5iE8GaYlByGzwMlGIIZfS58mM3Rp5dSOPiyTQYFScVoJ9T8o51QITTN6_A86D8uYj_ibQqQcBWTqbE25GFKKvt3ujWBWMZpVjOY9xjzx9U-7W_4ttwwcbYDV5FYOMVf2zHUmvqyJeZpCfFdgSkG-CXsFDairkw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1511124150</pqid></control><display><type>article</type><title>Three-dimensional cell migration does not follow a random walk</title><source>MEDLINE</source><source>Jstor Complete Legacy</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Wu, Pei-Hsun ; Giri, Anjil ; Sun, Sean X. ; Wirtz, Denis</creator><creatorcontrib>Wu, Pei-Hsun ; Giri, Anjil ; Sun, Sean X. ; Wirtz, Denis</creatorcontrib><description>Cell migration through 3D extracellular matrices is critical to the normal development of tissues and organs and in disease processes, yet adequate analytical tools to characterize 3D migration are lacking. Here, we quantified the migration patterns of individual fibrosarcoma cells on 2D substrates and in 3D collagen matrices and found that 3D migration does not follow a random walk. Both 2D and 3D migration features a non-Gaussian, exponential mean cell velocity distribution, which we show is primarily a result of cell-to-cell variations. Unlike in the 2D case, 3D cell migration is anisotropic: velocity profiles display different speed and self-correlation processes in different directions, rendering the classical persistent random walk (PRW) model of cell migration inadequate. By incorporating cell heterogeneity and local anisotropy to the PRW model, we predict 3D cell motility over a wide range of matrix densities, which identifies density-independent emerging migratory properties. This analysis also reveals the unexpected robust relation between cell speed and persistence of migration over a wide range of matrix densities.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1318967111</identifier><identifier>PMID: 24594603</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Actinin - chemistry ; Anisotropy ; Biological Sciences ; Cell adhesion &amp; migration ; Cell Line, Tumor ; Cell motility ; Cell Movement - physiology ; Collagen ; Collagens ; Computer Simulation ; Correlation analysis ; Crk-Associated Substrate Protein - chemistry ; Diffusion coefficient ; Endothelial cells ; Extracellular Matrix ; Human migration ; Humans ; Modeling ; Models, Biological ; Physical Sciences ; Random walk ; Stochastic Processes ; Three dimensional modeling ; Tissues ; Trajectories ; Two dimensional modeling ; Zyxin - chemistry</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2014-03, Vol.111 (11), p.3949-3954</ispartof><rights>copyright © 1993—2008 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Mar 18, 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c500t-dfb6e3d6cf6a271a41812c64b5f0f08e58ab5c1a527ae78b02c5c379947720673</citedby><cites>FETCH-LOGICAL-c500t-dfb6e3d6cf6a271a41812c64b5f0f08e58ab5c1a527ae78b02c5c379947720673</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/111/11.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23770964$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23770964$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,724,777,781,800,882,27905,27906,53772,53774,57998,58231</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24594603$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wu, Pei-Hsun</creatorcontrib><creatorcontrib>Giri, Anjil</creatorcontrib><creatorcontrib>Sun, Sean X.</creatorcontrib><creatorcontrib>Wirtz, Denis</creatorcontrib><title>Three-dimensional cell migration does not follow a random walk</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Cell migration through 3D extracellular matrices is critical to the normal development of tissues and organs and in disease processes, yet adequate analytical tools to characterize 3D migration are lacking. Here, we quantified the migration patterns of individual fibrosarcoma cells on 2D substrates and in 3D collagen matrices and found that 3D migration does not follow a random walk. Both 2D and 3D migration features a non-Gaussian, exponential mean cell velocity distribution, which we show is primarily a result of cell-to-cell variations. Unlike in the 2D case, 3D cell migration is anisotropic: velocity profiles display different speed and self-correlation processes in different directions, rendering the classical persistent random walk (PRW) model of cell migration inadequate. By incorporating cell heterogeneity and local anisotropy to the PRW model, we predict 3D cell motility over a wide range of matrix densities, which identifies density-independent emerging migratory properties. This analysis also reveals the unexpected robust relation between cell speed and persistence of migration over a wide range of matrix densities.</description><subject>Actinin - chemistry</subject><subject>Anisotropy</subject><subject>Biological Sciences</subject><subject>Cell adhesion &amp; migration</subject><subject>Cell Line, Tumor</subject><subject>Cell motility</subject><subject>Cell Movement - physiology</subject><subject>Collagen</subject><subject>Collagens</subject><subject>Computer Simulation</subject><subject>Correlation analysis</subject><subject>Crk-Associated Substrate Protein - chemistry</subject><subject>Diffusion coefficient</subject><subject>Endothelial cells</subject><subject>Extracellular Matrix</subject><subject>Human migration</subject><subject>Humans</subject><subject>Modeling</subject><subject>Models, Biological</subject><subject>Physical Sciences</subject><subject>Random walk</subject><subject>Stochastic Processes</subject><subject>Three dimensional modeling</subject><subject>Tissues</subject><subject>Trajectories</subject><subject>Two dimensional modeling</subject><subject>Zyxin - chemistry</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>eNqNkc1P3DAQxS1EBQvtuaeWSFy4BGb8GV-QEAJaCakXOFuO40C2Sby1syD-e7zdZWl76mFkafybp3nzCPmMcIqg2NlitOkUGVZaKkTcITMEjaXkGnbJDICqsuKU75ODlOYAoEUFe2SfcqG5BDYj53eP0fuy6QY_pi6Mti-c7_ti6B6inXKjaIJPxRimog19H54LW0Q7NmEonm3_8yP50No--U-b95DcX1_dXX4rb3_cfL-8uC2dAJjKpq2lZ410rbRUoeVYIXWS16KFFiovKlsLh1ZQZb2qaqBOOKa05kpRkIodkvO17mJZD75xfpyi7c0idoONLybYzvz9M3aP5iE8GaYlByGzwMlGIIZfS58mM3Rp5dSOPiyTQYFScVoJ9T8o51QITTN6_A86D8uYj_ibQqQcBWTqbE25GFKKvt3ujWBWMZpVjOY9xjzx9U-7W_4ttwwcbYDV5FYOMVf2zHUmvqyJeZpCfFdgSkG-CXsFDairkw</recordid><startdate>20140318</startdate><enddate>20140318</enddate><creator>Wu, Pei-Hsun</creator><creator>Giri, Anjil</creator><creator>Sun, Sean X.</creator><creator>Wirtz, Denis</creator><general>National Academy of Sciences</general><general>National Acad Sciences</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>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>7ST</scope><scope>7U6</scope><scope>5PM</scope></search><sort><creationdate>20140318</creationdate><title>Three-dimensional cell migration does not follow a random walk</title><author>Wu, Pei-Hsun ; Giri, Anjil ; Sun, Sean X. ; Wirtz, Denis</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c500t-dfb6e3d6cf6a271a41812c64b5f0f08e58ab5c1a527ae78b02c5c379947720673</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Actinin - chemistry</topic><topic>Anisotropy</topic><topic>Biological Sciences</topic><topic>Cell adhesion &amp; migration</topic><topic>Cell Line, Tumor</topic><topic>Cell motility</topic><topic>Cell Movement - physiology</topic><topic>Collagen</topic><topic>Collagens</topic><topic>Computer Simulation</topic><topic>Correlation analysis</topic><topic>Crk-Associated Substrate Protein - chemistry</topic><topic>Diffusion coefficient</topic><topic>Endothelial cells</topic><topic>Extracellular Matrix</topic><topic>Human migration</topic><topic>Humans</topic><topic>Modeling</topic><topic>Models, Biological</topic><topic>Physical Sciences</topic><topic>Random walk</topic><topic>Stochastic Processes</topic><topic>Three dimensional modeling</topic><topic>Tissues</topic><topic>Trajectories</topic><topic>Two dimensional modeling</topic><topic>Zyxin - chemistry</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Pei-Hsun</creatorcontrib><creatorcontrib>Giri, Anjil</creatorcontrib><creatorcontrib>Sun, Sean X.</creatorcontrib><creatorcontrib>Wirtz, Denis</creatorcontrib><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 &amp; 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>Environment Abstracts</collection><collection>Sustainability Science Abstracts</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>Wu, Pei-Hsun</au><au>Giri, Anjil</au><au>Sun, Sean X.</au><au>Wirtz, Denis</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Three-dimensional cell migration does not follow a random walk</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2014-03-18</date><risdate>2014</risdate><volume>111</volume><issue>11</issue><spage>3949</spage><epage>3954</epage><pages>3949-3954</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Cell migration through 3D extracellular matrices is critical to the normal development of tissues and organs and in disease processes, yet adequate analytical tools to characterize 3D migration are lacking. Here, we quantified the migration patterns of individual fibrosarcoma cells on 2D substrates and in 3D collagen matrices and found that 3D migration does not follow a random walk. Both 2D and 3D migration features a non-Gaussian, exponential mean cell velocity distribution, which we show is primarily a result of cell-to-cell variations. Unlike in the 2D case, 3D cell migration is anisotropic: velocity profiles display different speed and self-correlation processes in different directions, rendering the classical persistent random walk (PRW) model of cell migration inadequate. By incorporating cell heterogeneity and local anisotropy to the PRW model, we predict 3D cell motility over a wide range of matrix densities, which identifies density-independent emerging migratory properties. This analysis also reveals the unexpected robust relation between cell speed and persistence of migration over a wide range of matrix densities.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>24594603</pmid><doi>10.1073/pnas.1318967111</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0027-8424
ispartof Proceedings of the National Academy of Sciences - PNAS, 2014-03, Vol.111 (11), p.3949-3954
issn 0027-8424
1091-6490
language eng
recordid cdi_proquest_miscellaneous_1516742857
source MEDLINE; Jstor Complete Legacy; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry
subjects Actinin - chemistry
Anisotropy
Biological Sciences
Cell adhesion & migration
Cell Line, Tumor
Cell motility
Cell Movement - physiology
Collagen
Collagens
Computer Simulation
Correlation analysis
Crk-Associated Substrate Protein - chemistry
Diffusion coefficient
Endothelial cells
Extracellular Matrix
Human migration
Humans
Modeling
Models, Biological
Physical Sciences
Random walk
Stochastic Processes
Three dimensional modeling
Tissues
Trajectories
Two dimensional modeling
Zyxin - chemistry
title Three-dimensional cell migration does not follow a random walk
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-17T12%3A12%3A54IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Three-dimensional%20cell%20migration%20does%20not%20follow%20a%20random%20walk&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Wu,%20Pei-Hsun&rft.date=2014-03-18&rft.volume=111&rft.issue=11&rft.spage=3949&rft.epage=3954&rft.pages=3949-3954&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.1318967111&rft_dat=%3Cjstor_proqu%3E23770964%3C/jstor_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1511124150&rft_id=info:pmid/24594603&rft_jstor_id=23770964&rfr_iscdi=true