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Title: Lévy-like movement patterns of metastatic cancer cells revealed in microfabricated systems and implicated in vivo

Abstract

Metastatic cancer cells differ from their non-metastatic counterparts not only in terms of molecular composition and genetics, but also by the very strategy they employ for locomotion. Here, we analyzed large-scale statistics for cells migrating on linear microtracks to show that metastatic cancer cells follow a qualitatively different movement strategy than their non-invasive counterparts. The trajectories of metastatic cells display clusters of small steps that are interspersed with long “flights”. Such movements are characterized by heavy-tailed, truncated power law distributions of persistence times and are consistent with the Lévy walks that are also often employed by animal predators searching for scarce prey or food sources. In contrast, non-metastatic cancerous cells perform simple diffusive movements. These findings are supported by preliminary experiments with cancer cells migrating away from primary tumors in vivo. The use of chemical inhibitors targeting actin-binding proteins allows for “reprogramming” the Lévy walks into either diffusive or ballistic movements.

Authors:
 [1];  [2];  [3];  [4];  [5];  [1];  [6];  [1];  [4];  [7];  [1];  [1];  [1];  [1];  [2];  [8];  [5]; ORCiD logo [5]
  1. Northwestern Univ., Evanston, IL (United States)
  2. Radboud Univ. Medical Centre, Nijmegen (Netherlands); Univ. of Texas MD Cancer Genomics Center, Houston, TX (United States)
  3. Radboud Univ. Medical Centre, Nijmegen (Netherlands)
  4. Polish Academy of Sciences, Poznań (Poland)
  5. Ulsan National Inst. of Science and Technology (UNIST) (South Korea)
  6. Aichi Univ. (Japan)
  7. Adam Mickiewicz Univ., Poznań (Poland)
  8. Forsyth Inst., Cambridge, MA (United States)
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Bio-Inspired Energy Science (CBES); Northwestern Univ., Evanston, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)
OSTI Identifier:
1566603
Grant/Contract Number:  
SC0000989
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; catalysis (homogeneous); solar (photovoltaic); bio-inspired; charge transport; mesostructured materials; materials and chemistry by design; synthesis (novel materials); synthesis (self-assembly)

Citation Formats

Huda, Sabil, Weigelin, Bettina, Wolf, Katarina, Tretiakov, Konstantin V., Polev, Konstantin, Wilk, Gary, Iwasa, Masatomo, Emami, Fateme S., Narojczyk, Jakub W., Banaszak, Michal, Soh, Siowling, Pilans, Didzis, Vahid, Amir, Makurath, Monika, Friedl, Peter, Borisy, Gary G., Kandere-Grzybowska, Kristiana, and Grzybowski, Bartosz A. Lévy-like movement patterns of metastatic cancer cells revealed in microfabricated systems and implicated in vivo. United States: N. p., 2018. Web. doi:10.1038/s41467-018-06563-w.
Huda, Sabil, Weigelin, Bettina, Wolf, Katarina, Tretiakov, Konstantin V., Polev, Konstantin, Wilk, Gary, Iwasa, Masatomo, Emami, Fateme S., Narojczyk, Jakub W., Banaszak, Michal, Soh, Siowling, Pilans, Didzis, Vahid, Amir, Makurath, Monika, Friedl, Peter, Borisy, Gary G., Kandere-Grzybowska, Kristiana, & Grzybowski, Bartosz A. Lévy-like movement patterns of metastatic cancer cells revealed in microfabricated systems and implicated in vivo. United States. https://doi.org/10.1038/s41467-018-06563-w
Huda, Sabil, Weigelin, Bettina, Wolf, Katarina, Tretiakov, Konstantin V., Polev, Konstantin, Wilk, Gary, Iwasa, Masatomo, Emami, Fateme S., Narojczyk, Jakub W., Banaszak, Michal, Soh, Siowling, Pilans, Didzis, Vahid, Amir, Makurath, Monika, Friedl, Peter, Borisy, Gary G., Kandere-Grzybowska, Kristiana, and Grzybowski, Bartosz A. Wed . "Lévy-like movement patterns of metastatic cancer cells revealed in microfabricated systems and implicated in vivo". United States. https://doi.org/10.1038/s41467-018-06563-w. https://www.osti.gov/servlets/purl/1566603.
@article{osti_1566603,
title = {Lévy-like movement patterns of metastatic cancer cells revealed in microfabricated systems and implicated in vivo},
author = {Huda, Sabil and Weigelin, Bettina and Wolf, Katarina and Tretiakov, Konstantin V. and Polev, Konstantin and Wilk, Gary and Iwasa, Masatomo and Emami, Fateme S. and Narojczyk, Jakub W. and Banaszak, Michal and Soh, Siowling and Pilans, Didzis and Vahid, Amir and Makurath, Monika and Friedl, Peter and Borisy, Gary G. and Kandere-Grzybowska, Kristiana and Grzybowski, Bartosz A.},
abstractNote = {Metastatic cancer cells differ from their non-metastatic counterparts not only in terms of molecular composition and genetics, but also by the very strategy they employ for locomotion. Here, we analyzed large-scale statistics for cells migrating on linear microtracks to show that metastatic cancer cells follow a qualitatively different movement strategy than their non-invasive counterparts. The trajectories of metastatic cells display clusters of small steps that are interspersed with long “flights”. Such movements are characterized by heavy-tailed, truncated power law distributions of persistence times and are consistent with the Lévy walks that are also often employed by animal predators searching for scarce prey or food sources. In contrast, non-metastatic cancerous cells perform simple diffusive movements. These findings are supported by preliminary experiments with cancer cells migrating away from primary tumors in vivo. The use of chemical inhibitors targeting actin-binding proteins allows for “reprogramming” the Lévy walks into either diffusive or ballistic movements.},
doi = {10.1038/s41467-018-06563-w},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {Wed Oct 31 00:00:00 EDT 2018},
month = {Wed Oct 31 00:00:00 EDT 2018}
}

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Motility efficiency and spatiotemporal synchronization in non-metastatic vs. metastatic breast cancer cells
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Three-dimensional cell migration does not follow a random walk
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Comment on "Levy Walks Evolve Through Interaction Between Movement and Environmental Complexity"
journal, February 2012


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Persistence and Adaptation in Immunity: T Cells Balance the Extent and Thoroughness of Search
journal, March 2016

  • Fricke, G. Matthew; Letendre, Kenneth A.; Moses, Melanie E.
  • PLOS Computational Biology, Vol. 12, Issue 3
  • DOI: 10.1371/journal.pcbi.1004818

The evolutionary origins of Lévy walk foraging
journal, October 2017

  • Wosniack, Marina E.; Santos, Marcos C.; Raposo, Ernesto P.
  • PLOS Computational Biology, Vol. 13, Issue 10
  • DOI: 10.1371/journal.pcbi.1005774

Functional Analysis of Spontaneous Cell Movement under Different Physiological Conditions
journal, July 2008


Adaptive Lévy Walks in Foraging Fallow Deer
journal, August 2009


Lévy foraging patterns of rural humans
journal, June 2018


Applications, Properties and Synthesis of ω-Functionalized n-Alkanethiols and Disulfides - the Building Blocks of Self-Assembled Monolayers
journal, December 2004


Power-law distributions in empirical data
text, January 2007


Persistent Cell Motion in the Absence of External Signals: A Search Strategy for Eukaryotic Cells
text, January 2008


Anomalous dynamics of cell migration
text, January 2009


Works referencing / citing this record:

A Lévy expansion strategy optimizes early dune building by beach grasses
journal, June 2019


Immature dendritic cells navigate microscopic mazes to find tumor cells
journal, January 2019

  • Um, Eujin; Oh, Jung Min; Park, Juhee
  • Lab on a Chip, Vol. 19, Issue 9
  • DOI: 10.1039/c9lc00150f