‘Dicty dynamics’: Dictyostelium motility as persistent random motion

We model the motility of Dictyostelium cells in a systematic data-driven manner. We deduce a minimal dynamical model that reproduces the statistical features of experimental trajectories. These are trajectories of the centroid of the cell perimeter, which is more sensitive to pseudopod activity than the usual tracking by centroid or nucleus. Our data account for cell individuality and dictate a model that extends the cell-type specific models recently derived for mammalian cells. Two generalized Langevin equations model stochastic periodic pseudopod motion parallel and orthogonal to the amoeba's direction of motion. This motion propels the amoeba with a random periodic left-right waddle in a direction that has a long persistence time. The model fully accounts for the statistics of the experimental trajectories, including velocity power spectra and auto-correlations, non-Gaussian velocity distributions, and multiplicative noise. Thus, we find neither need nor place in our data for an interpretation in terms of anomalous diffusion. The model faithfully captures cell individuality as different parameter values in the model, and serves as a basis for integrating the local mechanics of cell motion with our observed long-term behavior.

[1]  Pablo A Iglesias,et al.  Cells navigate with a local-excitation, global-inhibition-biased excitable network , 2010, Proceedings of the National Academy of Sciences.

[2]  S. Leibler,et al.  Kinetics of self-assembling microtubules: an "inverse problem" in biochemistry. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[3]  R. Mazo On the theory of brownian motion , 1973 .

[4]  G. Borisy,et al.  Cell Migration: Integrating Signals from Front to Back , 2003, Science.

[5]  R. Preuss,et al.  Anomalous dynamics of cell migration , 2008, Proceedings of the National Academy of Sciences.

[6]  T. Coates,et al.  The fundamental motor of the human neutrophil is not random: evidence for local non-Markov movement in neutrophils. , 1994, Biophysical journal.

[7]  J. Spudich,et al.  The unconventional myosin encoded by the myoA gene plays a role in Dictyostelium motility. , 1993, Molecular biology of the cell.

[8]  M H Gail,et al.  The locomotion of mouse fibroblasts in tissue culture. , 1970, Biophysical journal.

[9]  Chuan-Hsiang Huang,et al.  Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. , 2010, Annual review of biophysics.

[10]  Edward C. Cox,et al.  Cell motility as random motion: A review , 2008 .

[11]  H. Berg,et al.  Chemotaxis in Escherichia coli analysed by Three-dimensional Tracking , 1972, Nature.

[12]  D R Soll,et al.  "DMS," a computer-assisted system for quantitating motility, the dynamics of cytoplasmic flow, and pseudopod formation: its application to Dictyostelium chemotaxis. , 1988, Cell motility and the cytoskeleton.

[13]  Hiroaki Takagi,et al.  Functional Analysis of Spontaneous Cell Movement under Different Physiological Conditions , 2008, PloS one.

[14]  H. Flyvbjerg,et al.  Power spectrum analysis for optical tweezers , 2004 .

[15]  Henrik Flyvbjerg,et al.  Harmonic oscillator in heat bath: exact simulation of time-lapse-recorded data and exact analytical benchmark statistics. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[16]  Natalie Andrew,et al.  Chemotaxis in shallow gradients is mediated independently of PtdIns 3-kinase by biased choices between random protrusions , 2007, Nature Cell Biology.

[17]  P. Mazur On the theory of brownian motion , 1959 .

[18]  P. V. van Haastert,et al.  The Ordered Extension of Pseudopodia by Amoeboid Cells in the Absence of External Cues , 2009, PloS one.

[19]  G. Uhlenbeck,et al.  On the Theory of the Brownian Motion , 1930 .

[20]  Alberto Aliseda,et al.  Spatio-temporal analysis of eukaryotic cell motility by improved force cytometry , 2007, Proceedings of the National Academy of Sciences.

[21]  Jerome T. Mettetal,et al.  Cellular asymmetry and individuality in directional sensing. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Erik S. Welf,et al.  Directional persistence of cell migration coincides with stability of asymmetric intracellular signaling. , 2010, Biophysical journal.

[23]  Julie A. Theriot,et al.  Intracellular fluid flow in rapidly moving cells , 2009, Nature Cell Biology.

[24]  D. Soll The use of computers in understanding how animal cells crawl. , 1995, International review of cytology.

[25]  Julie A. Theriot,et al.  Mechanism of shape determination in motile cells , 2008, Nature.

[26]  D. Soll,et al.  Motion Analysis of Living Cells , 1997 .

[27]  H. Flyvbjerg,et al.  Power spectrum analysis with least-squares fitting: amplitude bias and its elimination, with application to optical tweezers and atomic force microscope cantilevers. , 2009, Review of Scientific Instruments.

[28]  D R Soll,et al.  “Dynamic morphology system”: A method for quantitating changes in shape, pseudopod formation, and motion in normal and mutant amoebae of Dictyostelium discoideum , 1988, Journal of cellular biochemistry.

[29]  D. Soll,et al.  Targeted disruption of the ABP-120 gene leads to cells with altered motility , 1992, The Journal of cell biology.

[30]  Liang Li,et al.  Persistent Cell Motion in the Absence of External Signals: A Search Strategy for Eukaryotic Cells , 2008, PloS one.

[31]  M. Sheetz,et al.  Inversely correlated cycles in speed and turning in an ameba: an oscillatory model of cell locomotion. , 1997, Biophysical journal.

[32]  R. Fürth,et al.  Die Brownsche Bewegung bei Berücksichtigung einer Persistenz der Bewegungsrichtung. Mit Anwendungen auf die Bewegung lebender Infusorien , 1920 .

[33]  Y. Sawada,et al.  Anomalous diffusion and non-Gaussian velocity distribution of Hydra cells in cellular aggregates , 2001 .

[34]  Yoshiaki Iwadate,et al.  Actin-based propulsive forces and myosin-II-based contractile forces in migrating Dictyostelium cells , 2008, Journal of Cell Science.

[35]  Henrik Flyvbjerg,et al.  Cell motility as persistent random motion: theories from experiments. , 2005, Biophysical journal.

[36]  Juan C. del Álamo,et al.  Myosin II Is Essential for the Spatiotemporal Organization of Traction Forces during Cell Motility , 2010, Molecular biology of the cell.

[37]  Joachim Goedhart,et al.  Sensitization of Dictyostelium chemotaxis by phosphoinositide-3-kinase-mediated self-organizing signalling patches , 2004, Journal of Cell Science.

[38]  Fernando Peruani,et al.  Self-propelled particles with fluctuating speed and direction of motion in two dimensions. , 2007, Physical review letters.

[39]  T. Frank,et al.  Quantitative analysis of random ameboid motion , 2010 .

[40]  W. Rappel,et al.  Physical limits on cellular sensing of spatial gradients. , 2010, Physical review letters.

[41]  P. V. van Haastert,et al.  Food Searching Strategy of Amoeboid Cells by Starvation Induced Run Length Extension , 2009, PloS one.