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

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  • Liang Li
  • Simon F Nørrelykke
  • Edward C Cox

Abstract

Background: Eukaryotic cells are large enough to detect signals and then orient to them by differentiating the signal strength across the length and breadth of the cell. Amoebae, fibroblasts, neutrophils and growth cones all behave in this way. Little is known however about cell motion and searching behavior in the absence of a signal. Is individual cell motion best characterized as a random walk? Do individual cells have a search strategy when they are beyond the range of the signal they would otherwise move toward? Here we ask if single, isolated, Dictyostelium and Polysphondylium amoebae bias their motion in the absence of external cues. Methodology: We placed single well-isolated Dictyostelium and Polysphondylium cells on a nutrient-free agar surface and followed them at 10 sec intervals for ∼10 hr, then analyzed their motion with respect to velocity, turning angle, persistence length, and persistence time, comparing the results to the expectation for a variety of different types of random motion. Conclusions: We find that amoeboid behavior is well described by a special kind of random motion: Amoebae show a long persistence time (∼10 min) beyond which they start to lose their direction; they move forward in a zig-zag manner; and they make turns every 1–2 min on average. They bias their motion by remembering the last turn and turning away from it. Interpreting the motion as consisting of runs and turns, the duration of a run and the amplitude of a turn are both found to be exponentially distributed. We show that this behavior greatly improves their chances of finding a target relative to performing a random walk. We believe that other eukaryotic cells may employ a strategy similar to Dictyostelium when seeking conditions or signal sources not yet within range of their detection system.

Suggested Citation

  • Liang Li & Simon F Nørrelykke & Edward C Cox, 2008. "Persistent Cell Motion in the Absence of External Signals: A Search Strategy for Eukaryotic Cells," PLOS ONE, Public Library of Science, vol. 3(5), pages 1-11, May.
  • Handle: RePEc:plo:pone00:0002093
    DOI: 10.1371/journal.pone.0002093
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    References listed on IDEAS

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    1. Priscila C A da Silva & Tiago V Rosembach & Anésia A Santos & Márcio S Rocha & Marcelo L Martins, 2014. "Normal and Tumoral Melanocytes Exhibit q-Gaussian Random Search Patterns," PLOS ONE, Public Library of Science, vol. 9(9), pages 1-13, September.
    2. Azevedo, T.N. & Rizzi, L.G., 2022. "Time-correlated forces and biological variability in cell motility," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 604(C).
    3. Murguía, J.S. & Rosu, H.C. & Jimenez, A. & Gutiérrez-Medina, B. & García-Meza, J.V., 2015. "The Hurst exponents of Nitzschia sp. diatom trajectories observed by light microscopy," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 417(C), pages 176-184.
    4. Laurent Golé & Charlotte Rivière & Yoshinori Hayakawa & Jean-Paul Rieu, 2011. "A Quorum-Sensing Factor in Vegetative Dictyostelium Discoideum Cells Revealed by Quantitative Migration Analysis," PLOS ONE, Public Library of Science, vol. 6(11), pages 1-9, November.
    5. de Almeida, Rita M.C. & Giardini, Guilherme S.Y. & Vainstein, Mendeli & Glazier, James A. & Thomas, Gilberto L., 2022. "Exact solution for the Anisotropic Ornstein–Uhlenbeck process," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 587(C).
    6. Taeseok Daniel Yang & Jin-Sung Park & Youngwoon Choi & Wonshik Choi & Tae-Wook Ko & Kyoung J Lee, 2011. "Zigzag Turning Preference of Freely Crawling Cells," PLOS ONE, Public Library of Science, vol. 6(6), pages 1-9, June.
    7. Hélia Serrano & Ramón F. Álvarez-Estrada, 2023. "Characterization of the Mean First-Passage Time Function Subject to Advection in Annular-like Domains," Mathematics, MDPI, vol. 11(24), pages 1-17, December.
    8. Peter J M Van Haastert, 2010. "A Model for a Correlated Random Walk Based on the Ordered Extension of Pseudopodia," PLOS Computational Biology, Public Library of Science, vol. 6(8), pages 1-11, August.
    9. Robert M Cooper & Ned S Wingreen & Edward C Cox, 2012. "An Excitable Cortex and Memory Model Successfully Predicts New Pseudopod Dynamics," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-12, March.
    10. Oliver Nagel & Can Guven & Matthias Theves & Meghan Driscoll & Wolfgang Losert & Carsten Beta, 2014. "Geometry-Driven Polarity in Motile Amoeboid Cells," PLOS ONE, Public Library of Science, vol. 9(12), pages 1-20, December.
    11. Sui Huang, 2016. "Where to Go: Breaking the Symmetry in Cell Motility," PLOS Biology, Public Library of Science, vol. 14(5), pages 1-10, May.
    12. Can Guven & Erin Rericha & Edward Ott & Wolfgang Losert, 2013. "Modeling and Measuring Signal Relay in Noisy Directed Migration of Cell Groups," PLOS Computational Biology, Public Library of Science, vol. 9(5), pages 1-13, May.
    13. Yusuke T Maeda & Junya Inose & Miki Y Matsuo & Suguru Iwaya & Masaki Sano, 2008. "Ordered Patterns of Cell Shape and Orientational Correlation during Spontaneous Cell Migration," PLOS ONE, Public Library of Science, vol. 3(11), pages 1-14, November.
    14. Toman, Kellan & Voulgarakis, Nikolaos K., 2022. "Stochastic pursuit-evasion curves for foraging dynamics," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 597(C).
    15. Chopra, Abha & Nanjundiah, Vidyanand, 2013. "The precision with which single cells of Dictyostelium discoideum can locate a source of cyclic AMP," Chaos, Solitons & Fractals, Elsevier, vol. 50(C), pages 3-12.

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