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High Resolution Tracking of Cell Membrane Dynamics in MovingCells: an Electrifying Approach

Published online by Cambridge University Press:  03 February 2010

R.A. Tyson
Affiliation:
University of Warwick, Warwick Systems Biology Centre, Coventry, UK
D.B.A. Epstein
Affiliation:
University of Warwick, Warwick Mathematics Institute, Coventry, UK
K.I. Anderson
Affiliation:
Beatson Institute for Cancer Research, Glasgow, UK
T. Bretschneider*
Affiliation:
University of Warwick, Warwick Systems Biology Centre, Coventry, UK
*
* Corresponding author. E-mail:[email protected]
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Abstract

Cell motility is an integral part of a diverse set of biological processes. The quest formathematical models of cell motility has prompted the development of automated approachesfor gathering quantitative data on cell morphology, and the distribution of molecularplayers involved in cell motility. Here we review recent approaches for quantifying cellmotility, including automated cell segmentation and tracking. Secondly, we present our ownnovel method for tracking cell boundaries of moving cells, the Electrostatic ContourMigration Method (ECMM), as an alternative to the generally accepted level set method(LSM). ECMM smoothly tracks regions of the cell boundary over time to compute localmembrane displacements using the simple underlying concept of electrostatics. It offerssubstantial speed increases and reduced computational overheads in comparison to the LSM.We conclude with general considerations regarding boundary tracking in the context ofmathematical modelling.

Type
Research Article
Copyright
© EDP Sciences, 2010

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References

Affolter, M., Weijer., C. Signaling to cytoskeletal dynamics during chemotaxis . Developmental Cell, 9 (2005), No. 1 , 1934 CrossRefGoogle ScholarPubMed
Andrew, N., Insall., R. Chemotaxis in shallow gradients is mediated independently of PtdIns 3-kinase by biased choices between random protrusions . Nature cell biology, 9 (2007), No. 2, 193200 CrossRefGoogle ScholarPubMed
Al-Kofahi, O., Radke, R., Goderie, S., Shen, Q., Temple, S. Roysam., B. Automated cell lineage construction: A rapid method to analyze clonal development established with murine neural progenitor cells . Cell Cycle, 5 (2006), No. 3, 327335 CrossRefGoogle ScholarPubMed
B. Bollobas. Modern graph theory. Springer Verlag, 1998.
Bosgraaf, L., van Haastert, P. Bretschneider., T. Analysis of cell movement by simultaneous quantification of local membrane displacement and fluorescent intensities using Quimp2 . Cell Motility and the Cytoskeleton, 66 (2009), No. 3, 156165 CrossRefGoogle ScholarPubMed
D. Bray. Cell movements: from molecules to motility. Routledge, 2001.
Chan, F., Lam, F., Zhu, H.. Adaptive thresholding by variational method . IEEE Transactions on Image Processing, 7 (1998), No. 3, 468473. CrossRefGoogle ScholarPubMed
Cohen., L. On active contour models and balloons . CVGIP: Image understanding, 53 (1991), No. 2, 211218 CrossRefGoogle Scholar
Dalous, J., Burghardt, E., Muller-Taubenberger, A., Bruckert, F., Gerisch, G. Bretschneider., T. Reversal of cell polarity and actin-myosin cytoskeleton reorganization under mechanical and chemical stimulation . Biophysical journal, 94 (2008), No. 3, 10631074 CrossRefGoogle ScholarPubMed
Debeir, O., Camby, I., Kiss, R., Van Ham, P. Decaestecker., C. A model-based approach for automated in vitro cell tracking and chemotaxis analyses . Cytometry Part A, 60 (2004), 2940 CrossRefGoogle ScholarPubMed
Decaestecker, C., Debeir, O., Van Ham, P., Kiss, R.. Can anti-migratory drugs be screened in vitro? A review of 2D and 3D assays for the quantitative analysis of cell migration . Medicinal Research Reviews, 27 (2007), No. 2. CrossRefGoogle ScholarPubMed
Dormann, D., Libotte, T., Weijer, C. Bretschneider., T. Simultaneous quantification of cell motility and protein-membrane-association using active contours . Cell Motil Cytoskeleton, 52 (2002), No. 4, 22130 CrossRefGoogle ScholarPubMed
T. Driscoll. The Schwarz-Christoffel Toolbox for MATLAB. Available at: http://www.math.udel.edu/ driscoll/software/ . (Accessed: 21 Sep. 2009).
Dufour, A., Shinin, V., Tajbakhsh, S., Guillen-Aghion, N., Olivo-Marin, J. Zimmer., C. Segmenting and tracking fluorescent cells in dynamic 3-D microscopy with coupled active surfaces . IEEE Transactions on Image Proc., 14 (2005), No. 9, 13961410 CrossRefGoogle ScholarPubMed
Friedl, P., Weigelin, B.. Interstitial leukocyte migration and immune function . Nature Immunology, 9 (2008), No. 9, 960969. CrossRefGoogle ScholarPubMed
Friedl, P., Hegerfeldt, Y. Tusch., M. Collective cell migration in morphogenesis and cancer . Int. J. Dev. Biol., 48 (2004), 441449 CrossRefGoogle ScholarPubMed
Heid, P., Geiger, J., Wessels, D., Voss, E. Soll., D. Computer-assisted analysis of filopod formation and the role of myosin II heavy chain phosphorylation in Dictyostelium . Journal of cell science, 118 (2005), No. 10, 22252237 CrossRefGoogle ScholarPubMed
Hou, Z. Han., C. Force field analysis snake: an improved parametric active contour model . Pattern Recognition Letters, 26 (2005), No. 5, 513526 CrossRefGoogle Scholar
Ji, L., Lim, J., Danuser, G.. Fluctuations of intracellular forces during cell protrusion . Nature cell biology, 10 (2008), No. 12, 13931400. CrossRefGoogle ScholarPubMed
Kass, M., Witkin, A., Terzopoulos, D.. Snakes: Active contour models . International Journal of Computer Vision, (1988), No. 1 , 321331. CrossRefGoogle Scholar
Kay, R., Langridge, P., Traynor, D. Hoeller., O. Changing directions in the study of chemotaxis . Nat. Rev. Mol. Cell Bio, 9 (2008), No. 6, 455463 CrossRefGoogle Scholar
Libotte, T., Kaiser, H., Alt, W., Bretschneider, T. . Polarity, protrusion–retraction dynamics and their interplay during keratinocyte cell migration . Experimental Cell Research, 270 2001, No. 2, 129137. CrossRefGoogle ScholarPubMed
Machacek, M. Danuser., G. Morphodynamic Profiling of Protrusion Phenotypes Biophysical Journal . Biophysical Soc., 90 (2006), No. 4, 14391452 CrossRefGoogle Scholar
Machacek, M., Hodgson, L., Welch, C., Elliott, H., Pertz, O., Nalbant, P., Abell, A., Johnson, G., Hahn, K., Danuser, G.. Coordination of Rho GTPase activities during cell protrusion . Nature, 461 (2009), No. 7260, 99103. CrossRefGoogle ScholarPubMed
Meili, R., Ellsworth, C., Lee, S., Reddy, T., Ma, H. Firtel., R. Chemoattractant-mediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium . The EMBO Journal, 18 (1999), No. 8, 20922105 CrossRefGoogle ScholarPubMed
Miura., K. Tracking movement in cell biology . Advances in Biochemical Engineering Biotechnology, 95 (2005), 267296 Google ScholarPubMed
Osher, S. Sethian., J. Fronts propagating with curvature dependent speed: algorithms based on Hamilton-Jacobi formulations . Journal of computational physics, 79 (1988), 1249 CrossRefGoogle Scholar
A. Ridley, M. Peckham, P. Clark. Cell motility: from molecules to organisms. John Wiley & Sons Inc, 2004.
Ridley, A., Schwartz, M., Burridge, K., Firtel, R., Ginsberg, M., Borisy, G., Parsons, J. Horwitz., A. Cell Migration: Integrating Signals from Front to Back . Science, 302 (2003), No. 5651, 17041709 CrossRefGoogle ScholarPubMed
Sarti, A., Ortiz de Solorzano, C., Lockett, S. Malladi., R. A geometric model for 3-D confocal image analysis . IEEE Transactions on Biomedical Engineering, 47 (2000), No. 12, 16001609 Google ScholarPubMed
J. Sethian. Level set methods and fast marching methods: evolving interfaces in computational geometry, fluid mechanics, computer vision, and materials science. Cambridge Univ Pr, (1999).
Shutt, D., Jenkins, L., Carolan, E., Stapleton, J., Daniels, K., Kennedy, R. Soll., D. T cell syncytia induced by HIV release. T cell chemoattractants: demonstration with a newly developed single cell chemotaxis chamber . J. Cell Sci., 111 (1998), No. 1 , 99109 Google ScholarPubMed
Soll., D. Computer-assisted three-dimensional reconstruction and motion analysis of living, crawling cells . Computerized medical imaging and graphics, 23 (1999), No. 1 , 314 CrossRefGoogle ScholarPubMed
Soll., D. The use of computers in understanding how animal cells crawl . International review of cytology, 163 (1995), 43104 CrossRefGoogle ScholarPubMed
B. Sumengen. A Matlab toolbox implementing Level Set Methods. Available at: http://barissumengen.com/level_set_methods/. (Accessed: 21 Sep. 2009)
Tsukada, Y., Aoki, K., Nakamura, T., Sakumura, Y., Matsuda, M., Ishii, S.. Quantification of local morphodynamics and local GTPase activity by edge evolution tracking . PLoS Comp. Bio., 4 (2008), No. 11. CrossRefGoogle ScholarPubMed
Vallotton, P., Ponti, A., Waterman-Storer, C., Salmon, E. Danuser., G. Recovery, visualization, and analysis of actin and tubulin polymer flow in live cells: a fluorescent speckle microscopy study . Biophysical journal, 85 (2003), No. 2, 12891306 CrossRefGoogle ScholarPubMed
Veltman, D., Keizer-Gunnik, I. Haastert., P. Van Four key signaling pathways mediating chemotaxis in Dictyostelium discoideum . Journal of Cell Biology, 180 (2008), No. 4, 747753 CrossRefGoogle ScholarPubMed
Wessels, D., Voss, E., Bergen, N. Von, Burns, R., Stites, J. Soll., D. A computer-assisted system for reconstructing and interpreting the dynamic three-dimensional relationships of the outer surface, nucleus and pseudopods of crawling cells . Cell motility and the cytoskeleton, 41 (1998), No. 3, 225246 3.0.CO;2-I>CrossRefGoogle ScholarPubMed
Wu, K., Gauthier, D., Levine, M.. Live cell image segmentation IEEE Transactions on Biomedical Engineering, 42 (1995), 42, 112. Google ScholarPubMed
Xu, C., Prince, J.. Snakes, shapes, and gradient vector flow IEEE Transactions on image Processing , IEEE Transactions on image proc., 7 (1998), No. 3, 359369. Google Scholar
Yang, L., Effler, J., Kutscher, B., Sullivan, S., Robinson, D. Iglesias., P. Modeling cellular deformations using the level set formalism . BMC Systems Biology, 2 (2008), No. 1 , 68 CrossRefGoogle ScholarPubMed
Zhang, B., Zimmer, C. Olivo-Marin., J. Tracking fluorescent cells with coupled geometric active contours . IEEE Inter. Symp. on Biomedical Imaging: Nano to Macro, 1 (2004), 476479 Google Scholar