Distinct cell shapes determine accurate chemotaxis

The behaviour of an organism often reflects a strategy for coping with its environment. Such behaviour in higher organisms can often be reduced to a few stereotyped modes of movement due to physiological limitations, but finding such modes in amoeboid cells is more difficult as they lack these constraints. Here, we examine cell shape and movement in starved Dictyostelium amoebae during migration toward a chemoattractant in a microfluidic chamber. We show that the incredible variety in amoeboid shape across a population can be reduced to a few modes of variation. Interestingly, cells use distinct modes depending on the applied chemical gradient, with specific cell shapes associated with shallow, difficult-to-sense gradients. Modelling and drug treatment reveals that these behaviours are intrinsically linked with accurate sensing at the physical limit. Since similar behaviours are observed in a diverse range of cell types, we propose that cell shape and behaviour are conserved traits.

[1]  M. Ueda,et al.  Stochastic signal processing and transduction in chemotactic response of eukaryotic cells. , 2007, Biophysical journal.

[2]  P. V. van Haastert,et al.  Essential role of PI3-kinase and phospholipase A2 in Dictyostelium discoideum chemotaxis , 2007, The Journal of cell biology.

[3]  P. V. van Haastert,et al.  A stochastic model for chemotaxis based on the ordered extension of pseudopods. , 2010, Biophysical journal.

[4]  H. Meinhardt Orientation of chemotactic cells and growth cones: models and mechanisms. , 1999, Journal of cell science.

[5]  E. Raz,et al.  Control of Receptor Internalization, Signaling Level, and Precise Arrival at the Target in Guided Cell Migration , 2007, Current Biology.

[6]  W. Uttal On models and mechanisms , 1992, Behavioral and Brain Sciences.

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

[8]  Robert H. Insall,et al.  Understanding eukaryotic chemotaxis: a pseudopod-centred view , 2010, Nature Reviews Molecular Cell Biology.

[9]  John F. Canny,et al.  A Computational Approach to Edge Detection , 1986, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[10]  Eberhard Bodenschatz,et al.  Control parameter description of eukaryotic chemotaxis. , 2012, Physical review letters.

[11]  P. V. van Haastert,et al.  Biased random walk by stochastic fluctuations of chemoattractant-receptor interactions at the lower limit of detection. , 2007, Biophysical journal.

[12]  Robert F Murphy,et al.  Deformation‐based nuclear morphometry: Capturing nuclear shape variation in HeLa cells , 2008, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[13]  D. Soll,et al.  Phosphorylation of the Dictyostelium myosin II heavy chain is necessary for maintaining cellular polarity and suppressing turning during chemotaxis. , 1998, Cell motility and the cytoskeleton.

[14]  Alain Trouvé,et al.  Computing Large Deformation Metric Mappings via Geodesic Flows of Diffeomorphisms , 2005, International Journal of Computer Vision.

[15]  N. Wingreen,et al.  Accuracy of direct gradient sensing by single cells , 2008, Proceedings of the National Academy of Sciences.

[16]  F. Siegert,et al.  Null mutations of the Dictyostelium cyclic nucleotide phosphodiesterase gene block chemotactic cell movement in developing aggregates. , 1997, Developmental biology.

[17]  B. Bonati,et al.  Predatory behaviour of common kestrels (Falco tinnunculus) in the wild , 2009, Journal of Ethology.

[18]  John A. Mackenzie,et al.  Chemotaxis: A Feedback-Based Computational Model Robustly Predicts Multiple Aspects of Real Cell Behaviour , 2011, PLoS biology.

[19]  Monica L. Skoge,et al.  Gradient sensing in defined chemotactic fields. , 2010, Integrative biology : quantitative biosciences from nano to macro.

[20]  Jean-Paul Laumond,et al.  The formation of trajectories during goal‐oriented locomotion in humans. II. A maximum smoothness model , 2007, The European journal of neuroscience.

[21]  Miki Y. Matsuo,et al.  Ordered Patterns of Cell Shape and Orientational Correlation during Spontaneous Cell Migration , 2008, PloS one.

[22]  J. Rädler,et al.  Chemotactic cell trapping in controlled alternating gradient fields , 2011, Proceedings of the National Academy of Sciences.

[23]  Amy L. Gryshuk,et al.  Cell-Phone-Based Platform for Biomedical Device Development and Education Applications , 2011, PloS one.

[24]  D. Checkley,et al.  Comparisons of herring otoliths using Fourier series shape analysis , 1986 .

[25]  C. Parent,et al.  Real-time measurements of cAMP production in live Dictyostelium cells , 2009, Journal of Cell Science.

[26]  Michael I. Miller,et al.  Deformable templates using large deformation kinematics , 1996, IEEE Trans. Image Process..

[27]  H. K. Mebatsion,et al.  Evaluation of variations in the shape of grain types using principal components analysis of the elliptic Fourier descriptors , 2012 .

[28]  Timothy F. Cootes,et al.  Active Shape Models-Their Training and Application , 1995, Comput. Vis. Image Underst..

[29]  S. Ward,et al.  Caenorhabditis elegans spermatozoan locomotion: amoeboid movement with almost no actin , 1982, The Journal of cell biology.

[30]  G. Diaz,et al.  Elliptic fourier analysis of cell and nuclear shapes. , 1989, Computers and biomedical research, an international journal.

[31]  D. Murphy,et al.  G Protein Signaling Events Are Activated at the Leading Edge of Chemotactic Cells , 1998, Cell.

[32]  P. Dayan,et al.  A Bayesian model predicts the response of axons to molecular gradients , 2009, Proceedings of the National Academy of Sciences.

[33]  W. Rappel,et al.  Receptor noise and directional sensing in eukaryotic chemotaxis. , 2008, Physical review letters.

[34]  W. Bialek,et al.  Emergence of long timescales and stereotyped behaviors in Caenorhabditis elegans , 2011, Proceedings of the National Academy of Sciences.

[35]  Pablo A. Iglesias,et al.  Automated characterization of cell shape changes during amoeboid motility by skeletonization , 2010, BMC Systems Biology.

[36]  Pablo A. Iglesias,et al.  Interaction of Motility, Directional Sensing, and Polarity Modules Recreates the Behaviors of Chemotaxing Cells , 2013, PLoS Comput. Biol..

[37]  C. Parent,et al.  Localization of the G Protein βγ Complex in Living Cells During Chemotaxis , 2000 .

[38]  Alain Trouvé,et al.  Geodesic Shooting for Computational Anatomy , 2006, Journal of Mathematical Imaging and Vision.

[39]  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.

[40]  P. V. van Haastert,et al.  Navigation of Chemotactic Cells by Parallel Signaling to Pseudopod Persistence and Orientation , 2009, PloS one.

[41]  H. Berg,et al.  Physics of chemoreception. , 1977, Biophysical journal.

[42]  Pablo A Iglesias,et al.  Chemoattractant signaling in dictyostelium discoideum. , 2004, Annual review of cell and developmental biology.

[43]  M. Titus,et al.  A Dictyostelium myosin I plays a crucial role in regulating the frequency of pseudopods formed on the substratum. , 1996, Cell motility and the cytoskeleton.

[44]  J. Laumond,et al.  The formation of trajectories during goal‐oriented locomotion in humans. I. A stereotyped behaviour , 2007, The European journal of neuroscience.

[45]  P. V. van Haastert,et al.  Guanylyl cyclase protein and cGMP product independently control front and back of chemotaxing Dictyostelium cells. , 2006, Molecular biology of the cell.