Myosin II Is Essential for the Spatiotemporal Organization of Traction Forces during Cell Motility

Amoeboid motility results from pseudopod protrusions and retractions driven by traction forces of cells. We propose that the motor and actin-crosslinking functions of MyoII differentially control the temporal and spatial distribution of the traction forces, and establish mechanistic relationships between these distributions, enabling cells to move.

[1]  E. Elson,et al.  A mechanical function of myosin II in cell motility. , 1995, Journal of cell science.

[2]  E. Sackmann,et al.  Protrusion force transmission of amoeboid cells crawling on soft biological tissue. , 2005, Acta biomaterialia.

[3]  Erich Sackmann,et al.  Dictyostelium cells' cytoplasm as an active viscoplastic body , 2001, European Biophysics Journal.

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

[5]  R. Chisholm,et al.  Targeted disruption of the Dictyostelium RMLC gene produces cells defective in cytokinesis and development , 1994, The Journal of cell biology.

[6]  T. Soldati,et al.  Dissection of amoeboid movement into two mechanically distinct modes , 2006, Journal of Cell Science.

[7]  M. Abercrombie,et al.  The locomotion of fibroblasts in culture. I. Movements of the leading edge. , 1970, Experimental cell research.

[8]  W. Loomis,et al.  Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. , 1988, Developmental biology.

[9]  R. Chisholm,et al.  The dictyostelium essential light chain is required for myosin function , 1992, Cell.

[10]  J. Spudich,et al.  Myosin light chain kinase and myosin light chain phosphatase from Dictyostelium: effects of reversible phosphorylation on myosin structure and function , 1987, The Journal of cell biology.

[11]  M. Abercrombie,et al.  The locomotion of fibroblasts in culture. II. "RRuffling". , 1970, Experimental cell research.

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

[13]  R. Kay,et al.  Blebbing of Dictyostelium cells in response to chemoattractant. , 2006, Experimental cell research.

[14]  D. Soll,et al.  Myosin II heavy chain null mutant of Dictyostelium exhibits defective intracellular particle movement , 1990, The Journal of cell biology.

[15]  M. Steinmetz,et al.  Cortexillins, Major Determinants of Cell Shape and Size, Are Actin-Bundling Proteins with a Parallel Coiled-Coil Tail , 1996, Cell.

[16]  J. Segall,et al.  Selection of chemotaxis mutants of Dictyostelium discoideum , 1987, The Journal of cell biology.

[17]  W. Loomis,et al.  Intracellular Role of Adenylyl Cyclase in Regulation of Lateral Pseudopod Formation during Dictyostelium Chemotaxis , 2005, Eukaryotic Cell.

[18]  Hui Ma,et al.  Chemoattractant‐mediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium , 1999, The EMBO journal.

[19]  D A Knecht,et al.  Dictyostelium cell shape generation requires myosin II. , 1996, Cell motility and the cytoskeleton.

[20]  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.

[21]  J. Iwasa,et al.  Spatial and Temporal Relationships between Actin-Filament Nucleation, Capping, and Disassembly , 2007, Current Biology.

[22]  D. Lauffenburger,et al.  Cell Migration: A Physically Integrated Molecular Process , 1996, Cell.

[23]  Sally H. Zigmond,et al.  Leukocyte locomotion and chemotaxis. New methods for evaluation, and demonstration of a cell-derived chemotactic factor. , 1973 .

[24]  Thomas D Pollard,et al.  Cellular Motility Driven by Assembly and Disassembly of Actin Filaments , 2003, Cell.

[25]  S. Kuo,et al.  Dictyostelium myosin II mechanochemistry promotes active behavior of the cortex on long time scales , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[26]  R. Chisholm,et al.  During multicellular migration, myosin ii serves a structural role independent of its motor function. , 2001, Developmental biology.

[27]  Mark J. Miller,et al.  Two-Photon Imaging of Lymphocyte Motility and Antigen Response in Intact Lymph Node , 2002, Science.

[28]  Charles M. Grinstead,et al.  Introduction to probability , 1999, Statistics for the Behavioural Sciences.

[29]  T. Pollard,et al.  Cellular Motility Driven by Assembly and Disassembly of Actin Filaments , 2003, Cell.

[30]  Guillaume Charras,et al.  A short history of blebbing , 2008, Journal of microscopy.

[31]  Pablo A. Iglesias,et al.  Interactions between Myosin and Actin Crosslinkers Control Cytokinesis Contractility Dynamics and Mechanics , 2008, Current Biology.

[32]  P. V. van Haastert,et al.  The regulation of myosin II in Dictyostelium. , 2006, European journal of cell biology.

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

[34]  J. Murray,et al.  Cell behavior and actomyosin organization in Dictyostelium during substrate exploration. , 1991, Cell structure and function.

[35]  J. Davies,et al.  Molecular Biology of the Cell , 1983, Bristol Medico-Chirurgical Journal.

[36]  A. Noegel,et al.  Redundancy in the microfilament system: Abnormal development of dictyostelium cells lacking two F-actin cross-linking proteins , 1992, Cell.

[37]  L. Keer Stress distribution at the edge of an equilibrium crack , 1964 .

[38]  M. Dembo,et al.  Neutrophil traction stresses are concentrated in the uropod during migration. , 2007, Biophysical journal.

[39]  P. Fisher,et al.  Quantitative analysis of cell motility and chemotaxis in Dictyostelium discoideum by using an image processing system and a novel chemotaxis chamber providing stationary chemical gradients , 1989, The Journal of cell biology.

[40]  J. Spudich,et al.  Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. , 1987, Science.

[41]  G. Laevsky,et al.  Cross-linking of actin filaments by myosin II is a major contributor to cortical integrity and cell motility in restrictive environments , 2003, Journal of Cell Science.

[42]  E. Voss,et al.  Computer-assisted analysis of filopod formation and the role of myosin II heavy chain phosphorylation in Dictyostelium , 2005, Journal of Cell Science.

[43]  James A. Spudich,et al.  Capping of surface receptors and concomitant cortical tension are generated by conventional myosin , 1989, Nature.

[44]  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.

[45]  Y. Fukui,et al.  Actomyosin dynamics in chemotactic amoeboid movement of Dictyostelium , 1986 .

[46]  D. Knecht,et al.  Mutants lacking myosin II cannot resist forces generated during multicellular morphogenesis. , 1995, Journal of cell science.

[47]  Micah Dembo,et al.  Traction force microscopy in Dictyostelium reveals distinct roles for myosin II motor and actin-crosslinking activity in polarized cell movement , 2007, Journal of Cell Science.

[48]  S. Yumura,et al.  Dynamics of novel feet of Dictyostelium cells during migration , 2004, Journal of Cell Science.

[49]  D. Soll,et al.  ClC-3 and IClswell are Required for Normal Neutrophil Chemotaxis and Shape Change* , 2008, Journal of Biological Chemistry.

[50]  G. Côté,et al.  Regulation of Dictyostelium myosin I and II. , 2001, Biochimica et biophysica acta.

[51]  A. Kuspa,et al.  Cell-cell adhesion prevents mutant cells lacking myosin II from penetrating aggregation streams of Dictyostelium. , 1996, Developmental biology.

[52]  P. Devreotes,et al.  Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. , 1988, Annual review of cell biology.

[53]  T. Yanagida,et al.  Filament structure as an essential factor for regulation of Dictyostelium myosin by regulatory light chain phosphorylation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Y. Fukui,et al.  How well can an amoeba climb? , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Y. Fukui,et al.  Localization of actin and myosin for the study of ameboid movement in Dictyostelium using improved immunofluorescence , 1984, The Journal of cell biology.

[56]  L. Addadi,et al.  Hierarchical assembly of cell-matrix adhesion complexes. , 2004, Biochemical Society transactions.

[57]  S. Yumura,et al.  Myosin II contributes to the posterior contraction and the anterior extension during the retraction phase in migrating Dictyostelium cells , 2003, Journal of Cell Science.

[58]  J. Cooper,et al.  Actin dynamics: Assembly and disassembly of actin networks , 2000, Current Biology.

[59]  J. Murray,et al.  Three-dimensional dynamics of pseudopod formation and the regulation of turning during the motility cycle of Dictyostelium. , 1994, Cell motility and the cytoskeleton.

[60]  S. Zigmond,et al.  L E U K O C Y T E LOCOMOTION AND C H E M O T A X I S NEW METHODS FOR EVALUATION, AND DEMONSTRATION OF A CELL-DERIVED CHEMOTACTIC FACTOR* , 2003 .

[61]  F. C. Bennett,et al.  Myosin-IIA and ICAM-1 Regulate the Interchange between Two Distinct Modes of T Cell Migration1 , 2009, The Journal of Immunology.

[62]  John N. Tsitsiklis,et al.  Introduction to Probability , 2002 .

[63]  A. Bresnick,et al.  Actin polymerization and pseudopod extension during amoeboid chemotaxis. , 1988, Cell motility and the cytoskeleton.

[64]  G. Gerisch,et al.  Motility and substratum adhesion of Dictyostelium wild-type and cytoskeletal mutant cells: a study by RICM/bright-field double-view image analysis. , 1995, Journal of cell science.

[65]  P. Iglesias,et al.  Mechanosensing through Cooperative Interactions between Myosin II and the Actin Crosslinker Cortexillin I , 2009, Current Biology.

[66]  Pablo A. Iglesias,et al.  Mitosis-Specific Mechanosensing and Contractile-Protein Redistribution Control Cell Shape , 2006, Current Biology.

[67]  Ben Fabry,et al.  Traction fields, moments, and strain energy that cells exert on their surroundings. , 2002, American journal of physiology. Cell physiology.

[68]  A. Huttenlocher,et al.  Adhesion in cell migration. , 1995, Current opinion in cell biology.

[69]  Deborah Wessels,et al.  PTEN plays a role in the suppression of lateral pseudopod formation during Dictyostelium motility and chemotaxis , 2007, Journal of Cell Science.

[70]  R. Chisholm,et al.  Targeted disruption of the Dictyostelium myosin essential light chain gene produces cells defective in cytokinesis and morphogenesis. , 1995, Journal of cell science.