0
Review Article

Cytoskeletal Mechanics Regulating Amoeboid Cell Locomotion

[+] Author and Article Information
Begoña Álvarez-González

Research Assistant
Mechanical and Aerospace
Engineering Department,
University of California, San Diego,
La Jolla, CA 92093-0411
e-mail: bealvare@ucsd.edu

Effie Bastounis

Postdoctoral Fellow
Division of Cell and Developmental Biology,
University of California, San Diego,
La Jolla, CA 92093-0411

Ruedi Meili

Research Scientist
Mechanical and Aerospace
Engineering Department,
Division of Cell and Developmental Biology,
University of California, San Diego,
La Jolla, CA 92093-0411

Juan C. del Álamo

Associate Professor
Mechanical and Aerospace
Engineering Department,
Institute for Engineering in Medicine,
University of California, San Diego,
La Jolla, CA 92093-0411

Richard Firtel

Distinguished Professor
Division of Cell and Developmental Biology,
University of California, San Diego,
La Jolla, CA 92093-0411

Juan C. Lasheras

Distinguished Professor
Mechanical and Aerospace
Engineering Department,
Institute for Engineering in Medicine,
Bioengineering Department,
University of California, San Diego,
La Jolla, CA 92093-0411
e-mail: jlasheras@ucsd.edu

Cells secrete metalo-proteases at the front to degrade the extracellular matrix.

Opposite side to the leading edge in polarized leukocytes.

1Corresponding author.

Manuscript received July 7, 2013; final manuscript received October 9, 2013; published online June 5, 2014. Assoc. Editor: Ellen Kuhl.

Appl. Mech. Rev 66(5), 050804 (Jun 05, 2014) (14 pages) Paper No: AMR-13-1047; doi: 10.1115/1.4026249 History: Received July 07, 2013; Revised October 09, 2013

Migrating cells exert traction forces when moving. Amoeboid cell migration is a common type of cell migration that appears in many physiological and pathological processes and is performed by a wide variety of cell types. Understanding the coupling of the biochemistry and mechanics underlying the process of migration has the potential to guide the development of pharmacological treatment or genetic manipulations to treat a wide range of diseases. The measurement of the spatiotemporal evolution of the traction forces that produce the movement is an important aspect for the characterization of the locomotion mechanics. There are several methods to calculate the traction forces exerted by the cells. Currently the most commonly used ones are traction force microscopy methods based on the measurement of the deformation induced by the cells on elastic substrate on which they are moving. Amoeboid cells migrate by implementing a motility cycle based on the sequential repetition of four phases. In this paper, we review the role that specific cytoskeletal components play in the regulation of the cell migration mechanics. We investigate the role of specific cytoskeletal components regarding the ability of the cells to perform the motility cycle effectively and the generation of traction forces. The actin nucleation in the leading edge of the cell, carried by the ARP2/3 complex activated through the SCAR/WAVE complex, has shown to be fundamental to the execution of the cyclic movement and to the generation of the traction forces. The protein PIR121, a member of the SCAR/WAVE complex, is essential to the proper regulation of the periodic movement and the protein SCAR, also included in the SCAR/WAVE complex, is necessary for the generation of the traction forces during migration. The protein Myosin II, an important F-actin cross-linker and motor protein, is essential to cytoskeletal contractility and to the generation and proper organization of the traction forces during migration.

FIGURES IN THIS ARTICLE
<>
Copyright © 2014 by ASME
Topics: Traction , Cycles , Stress
Your Session has timed out. Please sign back in to continue.

References

Ausprunk, D. H., and Folkman, J., 1977, “Migration and Proliferation of Endothelial Cells in Preformed and Newly Formed Blood Vessels During Tumor Angiogenesis,” Microvasc. Res., 14(1), pp. 53–65. [CrossRef] [PubMed]
Bagorda, A., Mihaylov, V., and Parent, C. A., 2006, “Chemotaxis: Moving Forward and Holding on to the Past,” Thromb. Haemos., 95(1), pp. 12–21.
Cooper, G. M., and Hausman, R. E., 1997, The Cell: A Molecular Approach, Sinauer Associates, Sunderland, MA.
Lammermann, T., and Six, M., 2009, “Mechanical Modes of ‘Amoeboid’ Cell Migration,” Curr. Opin. Cell Biol., 21, pp. 636–644. [CrossRef] [PubMed]
Friedl, P., and Wolf, K., 2009, “Plasticity of Cell Migration: A Multiscale Tunning Model,” J. Cell Biol., 188(1), pp. 11–19. [CrossRef] [PubMed]
Huttenlocher, A., and Horwitz, A. R., 2011, “Integrins in Cell Migration,” Cold Spring Harbor Perspectives in Biology, 3(9), p. a005074. [CrossRef]
Mannherz, H. G., Mach, M., Nowak, D., Malicka-Blaszkiewicz, M., and Mazur, A., 2007, “Lamellipodial and Amoeboid Cell Locomotion: The Role of Actin-Cycling and Bleb Formation,” Biophys. Rev. Lett., 2(1), pp. 5–22. [CrossRef]
Meili, R., Alonso-Latorre, B., del Álamo, J. C., Firtel, R. A., and Lasheras, J. C., 2010, “Myosin II is Essential for the Spatiotemporal Organization of Traction Forces During Cell Motility,” Mol. Biol. Cell, 21, pp. 405–417. [CrossRef] [PubMed]
Smith, L. A., Aranda-Espinoza, H., Haun, J. B., Dembo, M., and Hammer, D. A., 2007, “Neutrophil Traction Stresses are Concentrated in the Uropod During Migration,” Biophys. J., 92(7), pp. 58–60. [CrossRef]
Shin, M. E., He, Y., Li, D., Na, S., Chowdhury, F., Poh, Y.-C., Collin, O., Su, P., de Lanerolle, P., Schwartz, M. A., Wang, N., and Wang, F., 2010, “Spatiotemporal Organization, Regulspatiotemporal Organization, Regulation, and Functions of Tractions During Neutrophil Chemotaxis,” Blood, 116, pp. 3297–3310. [CrossRef] [PubMed]
Beningo, K. A., Dembo, M., Kaverina, I., Small, J. V., and Wang, Y.-L., 2001, “Nascent Focal Adhesions are Responsible for the Generation of Strong Propulsive Forces in Migrating Fibroblasts,” J. Cell Biol., 153, pp. 881–888. [CrossRef] [PubMed]
Friedl, P., Borgmann, S., and Brocker, E.-B., 2001, “Amoeboid Leukocyte Crawling Through Extracellular Matrix: Lessons from the Dictyostelium Paradigm of Cell Movement,” J. Leukocyte Biol., 70(4), pp. 491–509.
Jannat, R. A., Dembo, M., and Hammer, D. A., 2011, “Traction Forces of Neutrophils Migrating on Compliant Substrates,” Biophys. J., 101, pp. 575–584. [CrossRef] [PubMed]
Ricart, B. G., Yang, M. T., Hunter, C. A., Chen, C. S., and Hammer, D. A., 2011, “Measuring Traction Forces of Motile Dendritic Cells on Micropost Arrays,” Biophys. J., 101, pp. 2620–2628. [CrossRef] [PubMed]
Lammermann, T., Bader, B. L., Monkley, S. J., Worbs, T., Wedlich-Soldner, R., Hirsch, K., Keller, M., Forster, R., Critchley, D. R., Fassler, R., and Six, M., 2008, “Rapid Leukocyte Migration by Integrin-Independent Flowing and Squeezing,” Nature, 453, pp. 51–55. [CrossRef] [PubMed]
del Álamo, J. C., Meili, R., Alonso-Latorre, B., Rodriguez-Rodriguez, J., Aliseda, A., Firtel, R. A., and Lasheras, J. C., 2007, “Spatiotemporal Analysis of Eukaryotic Cell Motility by Improved Force Cytometry,” Proc. Natl. Acad. Sci., 104(33), pp. 13343–13348. [CrossRef]
Stricker, J., Falzone, T., and Gardel, M. L., 2010, “Mechanics of the F-Actin Cytoskeleton,” J. Biomech., 43, pp. 9–14. [CrossRef] [PubMed]
Spiering, D., and Hodgson, L., 2011, “Dynamics of the Rho-Family Small Gtpases in Actin Regulation and Motility,” Cell Adhes. Migrat., 5(2), pp. 170–180. [CrossRef]
Sasaki, A. T., and Firtel, R. A., 2006, “Regulation of Chemotaxis by the Orchestrated Activation of RAS, PI3K, and TOR,” Eur. J. Cell Biol., 85, pp. 873–895. [CrossRef] [PubMed]
Fey, P., Stephens, S., Titus, M., and Chisholm, R., 2002, “Sada, A Novel Adhesion Receptor in Dictyostelium,” J. Cell Biol., 159, pp. 1109–1119. [CrossRef] [PubMed]
Uchida, K., and Yumura, S., 2004, “Dynamics of Novel Feet of Dictyostelium Cells During Migration,” J. Cell Sci., 117, pp. 1443–1455. [CrossRef] [PubMed]
Friedl, P., Entschladen, F., Conrad, C., Niggemann, B., and Zänker, K., 1998, “Cd4+ t Lymphocytes Migrating in Three-Dimensional Collagen Lattices Lack Focal Adhesions and Utilize Beta1 Integrin-Independent Strategies for Polarization, Interaction With Collagen Fibers and Locomotion,” Eur. J. Immunol., 28(8), pp. 2331–2343. [CrossRef] [PubMed]
Ananthakrishnan, R., and Ehrlicher, A., 2007, “The Forces Behind Cell Movement,” Int. J. Biol. Sci., 3(5), pp. 303–317. [CrossRef] [PubMed]
Li, B., and Wang, J. H.-C., 2010, “Application of Sensing Techniques to Cellular Force Measurement,” Sensors, 10, pp. 9948–9962. [CrossRef] [PubMed]
Li, B., Xie, L., Starr, Z. C., Yang, Z., Lin, J.-S., and Wang, J. H.-C., 2007, “Development of Micropost Force Sensor Array With Culture Experiments for Determination of Cell Traction Forces,” Cell Motil. Cytoskeleton, 64, pp. 509–518. [CrossRef] [PubMed]
Mathur, A., Roca-Cusachs, P., Rossier, O. M., Wind, S. J., Sheetz, M. P., and Hone, J., 2011, “New Approach for Measuring Protrusive Forces in Cells,” J. Vacuum Sci. Technol. B, 29(6), 06FA02. [CrossRef]
Han, S. J., Bielawski, K. S., Ting, L. H., Rodriguez, M. L., and Sniadecki, N. J., 2012, “Decoupling Substrate Stiffness, Spread Area, and Micropost Density: A Close Spatial Relationship Between Traction Forces and Focal Adhesions,” Biophys. J., 103, pp. 640–648. [CrossRef] [PubMed]
Yang, M. T., Fu, J., Wang, Y.-K., Desai, R. A., and Chen, C. S., 2011, “Assaying Stem Cell Mechanobiology on Microfabricated Elastomeric Substrates with Geometrically Modulated Rigidity,” Nat. Protoc., 6(2), pp. 187–213. [CrossRef] [PubMed]
Sniadecki, N. J., Lamb, C. M., Liu, Y., Chen, C. S., and Reich, D. H., 2008, “Magnetic Microposts for Mechanical Stimulation of Biological Cells: Fabrication, Characterization, and Analysis,” Rev. Sci. Instrum., 79, p. 044302. [CrossRef] [PubMed]
Lin, Y.-C., Kramer, C. M., Chen, C. S., and Reich, D. H., 2012, “Probing Cellular Traction Forces With Magnetic Nanowires and Microfabricated Force Sensor Arrays,” Nanotechnology, 23, p. 075101. [CrossRef] [PubMed]
McGarry, J. P., Fu, J., Yang, M. T., Chen, C. S., McMeeking, R. M., Evans, A. G., and Deshpande, V. S., 2009, “Simulation of the Contractile Response of Cells on an Array of Micro-Posts,” Philos. Trans. R. Soc. A, 367(1902), pp. 3477–3497. [CrossRef]
Wang, J. H.-C., and Lin, J.-S., 2007, “Cell Traction Force and Measurement Methods,” Biomech. Model. Mechanobiol., 6, pp. 361–371. [CrossRef] [PubMed]
Schwarz, U., Balaban, N., Riveline, D., Addadi, L., Bershadsky, A., Safran, S., and Geiger, B., 2003, “Measurement of Cellular Forces at Focal Adhesions Using Elastic Micro-Patterned Substrates,” Mater. Sci. Eng., 23(3), pp. 387–394. [CrossRef]
Reinhart-King, C. A., Dembo, M., and Hammer, D. A., 2003, “Endothelial Cell Traction Forces on RGD-Derivatized Polyacrylamide Substrata,” Langmuir, 19(5), pp. 1573–1579. [CrossRef]
Han, S. J., and Sniadecki, N. J., 2011, “Simulations of the Contractile Cycle in Cell Migration Using a Bio-Chemical-Mechanical Model,” Comput. Methods Biomech. Biomed. Eng., 14(5), pp. 459–468. [CrossRef]
Banerjee, S., and Marchetti, M. C., 2013, “Controlling Cell–Matrix Traction Forces by Extracellular Geometry,” New J. Phys., 15, p. 035015. [CrossRef]
Zielinski, R., Mihai, C., Kniss, D., and Ghadiali, S. N., 2013, “Finite Element Analysis of Traction Force Microscopy: Influence of Cell Mechanics, Adhesion, and Morphology,” ASME J. Biomech. Eng., 135(7), p. 071009. [CrossRef]
Holmes, W. R., and Edelstein-Keshet, L., 2012, “A Comparison of Computational Models for Eukaryotic Cell Shape and Motility,” PLOS Comput. Biol., 8(12), e1002793. [CrossRef] [PubMed]
Devreotes, P. N., and Zigmond, S. H., 1988, “Chemotaxis in Eukaryotic Cells: A Focus on Leukocytes and Dictyostelium,” Ann. Rev. Cell Biol., 4, pp. 649–686. [CrossRef]
Charest, P. G., and Firtel, R. A., 2007, “Big Roles for Small Gtpases in the Control of Directed Cell Movement,” Biochem. J., 401, pp. 377–390. [CrossRef] [PubMed]
Zigmond, S. H., 1993, “Recent Quantitative Studies of Actin Filament Turnover During Cell Locomotion,” Cell Motil. Cytoskeleton, 25, pp. 3309–3016. [CrossRef]
Borisy, G. G., and Svitkina, T. M., 2000, “Actin Machinery: Pushing the Envelope,” Curr. Opin. Cell Biol., 12, pp. 104–112. [CrossRef] [PubMed]
Mullins, R. D., Heuser, J. A., and Pollard, T. D., 1998, “The Interaction of arp2y3 Complex with Actin: Nucleation, High Affinity Pointed End Capping, and Formation of Branching Networks of Filaments,” Proc. Natl. Acad. Sci., 95, pp. 6181–6186. [CrossRef]
Pollard, T. D., 2007, “Regulation of Actin Filament Assembly by arp2/3 Complex and Formins,” Ann. Rev. Biophys. Biomol. Struct., 36, pp. 451–477. [CrossRef]
Weiner, O. D., Servant, G., Welch, M. D., Mitchison, T. J., Sedat, J. W., and Bourne, H. R., 1999, “Spatial Control of Actin Polymerization During Neutrophil Chemotaxis,” Nat. Cell Biol., 1, pp. 75–81. [CrossRef] [PubMed]
Spudich, J. A., 1989, “In Pursuit of Myosin Function,” Cell Regul., 1, pp. 1–11. [PubMed]
Stites, J., Wessels, D., Uhl, A., Egelhoff, T., Shutt, D., and Soll, D. R., 1998, “Phosphorylation of the Dictyostelium Myosin ii Heavy Chain is Necessary for Maintaining Cellular Polarity and Suppressing Turning During Chemotaxis,” Cell Motil. Cytoskeleton, 39, pp. 31–51. [CrossRef] [PubMed]
Yumura, S., Mori, H., and Fukui, Y., 1984, “Localization of Actin and Myosin for the Study of Ameboid Movement in Dictyostelium Using Improved Immunofluorescence,” J. Cell Biol., 99(3), pp. 894–899. [CrossRef] [PubMed]
Fukui, Y., and Yumura, S., 1986, “Actomyosin Dynamics in Chemotactic Amoeboid Movement of Dictyostelium,” Cell Motil. Cytoskeleton, 6, pp. 662–673. [CrossRef]
Moores, S. L., Sabry, J. H., and Spudich, J. A., 1996, “Myosin Dynamics in Live Dictyostelium Cells,” Proc. Natl. Acad. Sci., 93, pp. 443–446. [CrossRef]
Dembo, M., Oliver, T., Ishihara, A., and Jacobson, K., 1996, “Imaging the Traction Stresses Exerted by Locomoting Cells With Theelastic Substratum Method,” Biophys. J., 70, pp. 2008–2022. [CrossRef] [PubMed]
Dembo, M., and Wang, Y.-L., 1999, “Stresses at the Cell-to-Substrate Interface During Locomotion of Fibroblasts,” Biophys. J., 76, pp. 2307–2316. [CrossRef] [PubMed]
Butler, J. P., Tolić-Nørrelykke, I. M., Fabry, B., and Fredberg, J. J., 2002, “Traction Fields, Moments, and Strain Energy that Cells Exert on Their Surroundings,” Am. J. Cell Physiol., 282, pp. 595–605. [CrossRef]
Yang, Z., Lin, J.-S., Chen, J., and Wang, J. H.-C., 2006, “Determining Substrate Displacement and Cell Traction Fields-A New Approach,” J. Theor. Biol., 242, pp. 607–616. [CrossRef] [PubMed]
Wang, Y. L., and, Pelham, R. J., Jr., 1998, “Preparation of a Flexible, Porous Polyacrylamide Substrate for Mechanical Studies of Cultured Cells,” Methods Enzymol., 298, pp. 489–496. [PubMed]
Engler, A., Bacakova, L., Newman, C., Hategan, A., Griffin, M., and Discher, D., 2004, “Substrate Compliance Versus Ligand Density in Cell on Gel Responses,” Biophys. J., 86, pp. 617–628. [CrossRef] [PubMed]
Alonso-Latorre, B., 2010, “Force and Shape Coordination in Amoeboid Cell Motility,” Ph.D. thesis, University of California, San Diego, CA.
Keer, L. M., 1964, “Stress Distribution at the Edge of an Equilibrium Crack,” J. Mech. Phys. Solids, 12(3), pp. 149–163. [CrossRef]
Chippada, U., Yurke, B., and Langrana, N. A., 2011, “Simultaneous Determination of Young's Modulus, Shear Modulus, and Poisson's Ratio of Soft Hydrogels,” J. Mater. Res., 25(3), pp. 545–555. [CrossRef]
Takigawa, T., Morino, Y., Urayama, K., and Masudab, T., 1996, “Poisson's Ratio of Polyacrylamide (Paam) Gels,” Polym. Gels Networks, 4(1), pp. 1–5. [CrossRef]
Li, Y., Hu, Z., and Li, C., 1993, “New Method for Measuring Poisson's Ratio in Polymer Gels,” Appl. Polym. Sci., 50(6), pp. 1107–1111. [CrossRef]
Willert, C. E., and Gharib, M., 1991, “Digital Particle Image Velocimetry,” Exp. Fluids, 10(4), pp. 181–193. [CrossRef]
Gui, L., and Wereley, S. T., 2002, “A Correlation-Based Continuous Window-Shift Technique to Reduce the Peak-Locking Effect in Digital PIV Image Evaluation,” Exp. Fluids, 32, pp. 506–517. [CrossRef]
Hur, S. S., Zhao, Y., Li, Y.-S., Botvinick, E., and Chien, S., 2009, “Live Cells Exert 3-Dimensional Traction Forces on Their Substrata,” Cell. Mol. Bioeng., 2(3), pp. 425–436. [CrossRef] [PubMed]
Franck, C., Maskarinec, S. A., Tirrell, D. A., and Ravichandran, G., 2011, “Three-Dimensional Traction Force Microscopy: A New Tool for Quantifying Cell-Matrix Interactions,” PLOS ONE, 6(3), 317833. [CrossRef]
Delanoë-Ayari, H., and Rieu, J. P., 2010, “4D Traction Force Microscopy Reveals Asymmetric Cortical Forces in Migrating Dictyostelium Cells,” Phys. Rev. Lett., 105(24), p. 248103. [CrossRef] [PubMed]
del Álamo, J. C., Meili, R., Álvarez-González, B., Alonso-Latorre, B., Bastounis, E., Firtel, R., and Lasheras, J. C., 2013, “Three-Dimensional Quantification of Cellular Traction Forces and Mechanosensing of Thin Substrata by Fourier Traction Force Microscopy,” PLOS ONE, 8(9), e69850. [CrossRef] [PubMed]
Legant, W. R., Miller, J. S., Blakely, B. L., Cohen, D. M., Genin, G. M., and Chen, C. S., 2010, “Measurement of Mechanical Tractions Exerted by Cells in Three-Dimensional Matrices,” Nat. Methods, 7(2), pp. 969–971. [CrossRef] [PubMed]
Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T., and Horwitz, A. R., 2003, “Cell Migration: Integrating Signals from Front to Back,” Science, 302, pp. 1704–1709. [CrossRef] [PubMed]
Bailly, M., Condeelis, J. S., and Segall, J. E., 1998, “Chemoattractant-Induced Lamellipod Extension,” Microscop. Res. Tech., 43(5), pp. 433–443. [CrossRef]
Zhelev, D. V., Alteraifi, A. M., and Chodniewicz, D., 2004, “Controlled Pseudopod Extension of Human Neutrophils Stimulated With Different Chemoattractants,” Biophys. J., 87(1), pp. 688–695. [CrossRef] [PubMed]
Wessels, D., Vawter-Hugart, H., Murray, J., and Soll, D. R., 1994, “Three-Dimensional Dynamics of Pseudopod Formation and the Regulation of Turning During the Motility Cycle of Dictyostelium,” Cell Motil. Cytoskeleton, 27, pp. 1–12. [CrossRef] [PubMed]
Murray, J., Vawter-Hugart, H., Voss, E., and Soll, D. R., 1992, “Three-Dimensional Motility Cycle in Leukocytes,” Cell Motil. Cytoskeleton, 22, pp. 211–223. [CrossRef] [PubMed]
Ehrengruber, M. U., Deranleau, D. A., and Coates, T. D., 1996, “Shape Oscillations of Human Neutrophil Leukocytes: Characterization and Relationship to Cell Motility,” J. Exp. Biol., 199, pp. 741–747. [PubMed]
Lauffenburger, D. A., and Horwitz, A. F., 1996, “Cell Migration: A Physically Integrated Molecular Process,” Cell, 84, pp. 359–369. [CrossRef] [PubMed]
Bastounis, E., Meili, R., Alonso-Latorre, B., del Álamo, J. C., Lasheras, J. C., and Firtel, R. A., 2011, “The Scar/Wave Complex is Necessary for Proper Regulation of Traction Stresses During Amoeboid Motility,” Mol. Biol. Cell, 22, pp. 3995–4003. [CrossRef] [PubMed]
Chen, T., Kowalczyk, P., Ho, G., and Chisholm, R., 1995, “Targeted Disruption of the Dictyostelium Myosin Essential Light Chain Gene Produces Cells Defective in Cytokinesis and Morphogenesis,” J. Cell Sci., 108, pp. 3207–3218. [PubMed]
Xu, X. S., Lee, E., Chen.T., Kuczmarski, E., Chisholm, R. L., and Knecht, D. A., 2001, “During Multicellular Migration, Myosin II Serves a Structural Role Independent of its Motor Function,” Develop. Biol., 232, pp. 255–264. [CrossRef]
Lozanne, A. D., and Spudich, J. A., 1987, “Disruption of the Dictyostelium Myosin Heavy-Chain Gene by Homologous Recombination,” Science, 237(4805), pp. 1086–1091. [CrossRef]
Chen, P., Ostrow, B., Tafuri, S., and Chisholm, R., 1994, “Targeted Disruption of the Dictyostelium RMLC Gene Produces Cells Defective in Cytokinesis and Development,” J. Cell Biol., 127, pp. 1933–1944. [CrossRef] [PubMed]
Laevsky, G., and Knecht, D. A., 2003, “Cross-Linking of Actin Filaments by Myosin II is a Major Contributor to Cortical Integrity and Cell Motility in Restrictive Environments,” J. Cell Sci., 116, pp. 3761–3770. [CrossRef] [PubMed]
Griffith, L. M., Downs, S. M., and Spudich, J. A., 1987, “Myosin Light Chain Kinase and Myosin Light Chain Phosphatase from Dictyostelium: Effects of Reversible Phosphorylation on Myosin Structure and Function,” J. Cell Biol., 104(5), pp. 1309–1323. [CrossRef] [PubMed]
Alonso-Latorre, B., del Álamo, J., Meili, R., Firtel, R., and Lasheras., J., 2011, “Strain Energy Modes in Migrating Amoeboid Cells,” J. Cell. Mol. Biol., 4(4), pp. 603–615.
Weber, I., Wallraff, E., Albrecht, R., and Gerisch, G., 1995, “Motility and Substratum Adhesion of Dictyostelium Wild-Type and Cytoskeletal Mutant Cells: A Study by Ricm/Bright-Field Double-View Image Analysis,” J. Cell Sci., 108, pp. 1519–1530. [PubMed]
Lombardi, M. L., Knecht, D. A., Dembo, M., and Lee, J. , 2007. “Traction Force Microscopy in Dictyostelium Reveals Distinct Roles for Myosin Ii Motor and Actin Crosslinking Activity in Polarized Cell Movement,”J. Cell Sci., 120, pp. 1624–1634. [CrossRef] [PubMed]
Delanoe-Ayari, H., Iwaya, S., Maeda, Y. T., Inose, J., Riviere, C., Sano, M., and Rieu, J.-P., 2008, “Changes in the Magnitude and Distribution of Forces at Different Dictyostelium Developmental Stages,” Cell Motil. Cytoskeleton, 65, pp. 314–331. [CrossRef] [PubMed]
Steffen, A., Rottner, K., Ehinger, J., Innocenti, M., Scita, G., Wehland, J., and Stradal, T. E., 2004, “Sra-1 and Nap1 Link RAC to Actin Assembly Driving Lamellipodia Formation,” EMBO J., 23, pp. 749–759. [CrossRef] [PubMed]
Cory, G. O. C., and Ridley, A. J., 2002, “Cell Motility: Braking Waves,” Nature, 418, pp. 732–733. [CrossRef] [PubMed]
Basu, D., El-Assal, S. E.-D., Le, J., Mallery, E., and Szymanski, D. B., 2004, “Interchangeable Functions of Arabidopsis Pirogi and the Human Wave Complex Subunit Sra1 During Leaf Epidermal Development,” Developmental, 131, pp. 4345–4355. [CrossRef]
Davidson, A. J., and Insall, R. H., 2011, “Actin-Based Motility: Wave Regulatory Complex Structure Reopens Old Scars,” Curr. Biol., 21(2), pp. R66–R68. [CrossRef] [PubMed]

Figures

Grahic Jump Location
Fig. 1

(a) sketch of the configuration of the experiment. Substrate with an upper layer embedded with beads where the cells are moving. (b) DIC image taken with the microscope to identify the cell contours. (c) dilation and erosion application to determine the cell contour from the DIC image. (d) cell contour determination after a second dilation and erosion application. (e) image of the substrate embedded with beads used to calculate the deformation induced by the migrating cells. (f) displacement field for a wild-type cell at an instant of time. The arrows (color red online) represent the direction of the displacements and the contours underneath (color blue online) represent the magnitude of the tractions. This figure is taken from [16].

Grahic Jump Location
Fig. 2

Measurement of the Young's modulus with the calculation of the indentation produced by a tungsten carbide ball. This figure is taken from Ref. [57].

Grahic Jump Location
Fig. 3

Pole force calculation. The pole force at the front Ff is calculated by integrating the tractions stresses in the front half of the cell, ξ>0. The pole force at the back Fb is calculated by integrating the traction stresses in the back half of the cell, ξ<0.

Grahic Jump Location
Fig. 4

Sketch of the experimental configuration for the measurement of the three-dimensional deformation, where a z-stack of images, Δz, is acquired with the confocal microscope, and boundary conditions applied for the calculation of the traction forces in the three dimensions. This figure is taken from Ref. [67].

Grahic Jump Location
Fig. 5

The central image shows the periodic evolution of the cell length over time, the black color indicates the protrusion phase, the red color indicates the contraction phase, the green colors indicate the retraction phase, and the blue color the relaxation phase. The surrounding images show a sketch of each of the cycle phases and the average stress map for this cell at each of the four phases of the motility cycle. This figure is taken from Ref. [8].

Grahic Jump Location
Fig. 6

Average velocity versus motility cycle frequency (determined from the variations of the cell length) shows a linear relationship in WT, mlcE-, mhcA-, and scrA- cells. The blue, red, green, and black circles denote WT, scrA-, mlcE-, and mhcA- cells, respectively. The velocity-frequency slope, λ, for each of the cell lines is represented by the dotted lines, in blue and red for WT and scrA- cells, respectively, and magenta for both mhcA- and mlcE- cells. This figure is a combination of figures from Refs. [8,76].

Grahic Jump Location
Fig. 7

(a) conversion of the instantaneous stress map of a cell into a cell-based reference system. x and y are the coordinates in the laboratory reference frame, ξ and η are the coordinates in the cell based reference frame. φ is the angle between the longitudinal axis of the cell and the horizontal axis of the laboratory reference frame, L is the length of the cell, and xc and yc are the coordinates of the center of the cell in the laboratory reference frame. The arrow indicates the direction of the velocity, V, of the cell at this instant of time. (b) the first column indicates the calculation of the average traction forces in the cell-based reference frame for this cell at this instant of time. The origin is located at the center of the cell and the length of the cell is always between ξ=-1 and ξ=1. The second and third columns indicate the components of the average traction forces parallel (x-axis component) and perpendicular (y-axis component) to the cell major axis, respectively.

Grahic Jump Location
Fig. 8

The upper row shows the traction forces exerted in each of the phases of the motility cycle by WT cells, the second row shows the traction forces exerted in each of the phases of the motility cycle by mlcE- cells, and the third row shows the traction forces exerted in each of the phases of the motility cycle by mhcA- cells. This figure is taken from Ref. [8].

Grahic Jump Location
Fig. 9

The upper row shows the component of the traction forces exerted in the direction of the major axis of the cell by WT, mlcE-, and mhcA- cells. The second row shows the component of the traction forces exerted in the direction perpendicular to the major axis of the cell by WT, mlcE-, and mhcA- cells. This figure is taken from Ref. [8].

Grahic Jump Location
Fig. 10

The first row shows the traction forces exerted in each of the phases of the cycle by WT cells. The second row shows the traction forces exerted in each of the phases of the cycle by scrA- mutant cells. This figure is taken from Ref. [76].

Grahic Jump Location
Fig. 11

The upper row shows the component of the traction forces exerted in the direction of the major axis of the cell by WT, pirA-, and scrA- cells moving over polyacrilamide substrates. The second row shows the component of the traction forces exerted in the perpendicular direction to the major axis of the cell by WT, pirA-, and scrA- cells. This figure is taken from Ref. [76].

Grahic Jump Location
Fig. 12

(a) horizontal traction forces obtained by using the 3D method, (b) horizontal traction forces obtained by using the 2D method, and (c) difference between the horizontal traction forces calculated by using the 3D and 2D methods. The red color indicates that the traction forces calculated with the 3D method are bigger than the ones calculated with the 2D method, and the blue color indicates the opposite, that the traction forces calculated with the 3D method are lower than the ones calculated with the 2D method.

Grahic Jump Location
Fig. 13

Time evolution of the tangential strain energy obtained with the 3D method in blue and time evolution of the total strain energy obtained with the 2D method in red

Tables

Errata

Discussions

Related

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In