How a Cell Crawls and the Role of Cortical Myosin II

ABSTRACT The movements of Dictyostelium discoideum amoebae translocating on a glass surface in the absence of chemoattractant have been reconstructed at 5-second intervals and motion analyzed by employing 3D-DIAS software. A morphometric analysis of pseudopods, the main cell body, and the uropod provides a comprehensive description of the basic motile behavior of a cell in four dimensions (4D), resulting in a list of 18 characteristics. A similar analysis of the myosin II phosphorylation mutant 3XASP reveals a role for the cortical localization of myosin II in the suppression of lateral pseudopods, formation of the uropod, cytoplasmic distribution of cytoplasm in the main cell body, and efficient motility. The results of the morphometric analysis suggest that pseudopods, the main cell body, and the uropod represent three motility compartments that are coordinated for efficient translocation. It provides a contextual framework for interpreting the effects of mutations, inhibitors, and chemoattractants on the basic motile behavior of D. discoideum. The generality of the characteristics of the basic motile behavior of D. discoideum must now be tested by similar 4D analyses of the motility of amoeboid cells of higher eukaryotic cells, in particular human polymorphonuclear leukocytes.

[1]  Dennis Bray,et al.  Cell Movements: From Molecules to Motility , 1992 .

[2]  D. Lauffenburger,et al.  A Mena invasion isoform potentiates EGF-induced carcinoma cell invasion and metastasis. , 2008, Developmental cell.

[3]  J. Spudich,et al.  Regulation of myosin self-assembly: phosphorylation of Dictyostelium heavy chain inhibits formation of thick filaments. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[4]  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.

[5]  Pascale G. Charest,et al.  The regulation of cell motility and chemotaxis by phospholipid signaling , 2008, Journal of Cell Science.

[6]  E. Voss,et al.  Amebae of Dictyostelium discoideum respond to an increasing temporal gradient of the chemoattractant cAMP with a reduced frequency of turning: evidence for a temporal mechanism in ameboid chemotaxis. , 1987, Cell motility and the cytoskeleton.

[7]  Juan Pablo Albar,et al.  Type I phosphatidylinositol 4-phosphate 5-kinase controls neutrophil polarity and directional movement , 2007, The Journal of cell biology.

[8]  M. Carlier,et al.  Regulation of actin assembly associated with protrusion and adhesion in cell migration. , 2008, Physiological reviews.

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

[10]  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.

[11]  J. Spudich,et al.  Molecular genetic truncation analysis of filament assembly and phosphorylation domains of Dictyostelium myosin heavy chain. , 1994, Journal of cell science.

[12]  J. Bonner,et al.  Acrasin, Acrasinase, and the sensitivity to acrasin in Dictyostelium discoideum. , 1969, Developmental biology.

[13]  George Oster,et al.  How nematode sperm crawl. , 2002, Journal of cell science.

[14]  J. McNally,et al.  In vivo observations of myosin II dynamics support a role in rear retraction. , 1999, Molecular biology of the cell.

[15]  T. Uyeda,et al.  Myosins and cell dynamics in cellular slime molds. , 2003, International review of cytology.

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

[17]  D R Soll,et al.  Frequency and orientation of pseudopod formation of Dictyostelium discoideum amebae chemotaxing in a spatial gradient: further evidence for a temporal mechanism. , 1987, Cell motility and the cytoskeleton.

[18]  P. Devreotes,et al.  Cyclic 3',5'-AMP relay in Dictyostelium discoideum III. The relationship of cAMP synthesis and secretion during the cAMP signaling response , 1980, The Journal of cell biology.

[19]  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.

[20]  Daniel F Lusche,et al.  The effects of extracellular calcium on motility, pseudopod and uropod formation, chemotaxis, and the cortical localization of myosin II in Dictyostelium discoideum. , 2009, Cell motility and the cytoskeleton.

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

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

[23]  T. Egelhoff,et al.  Myosin II dynamics in Dictyostelium: determinants for filament assembly and translocation to the cell cortex during chemoattractant responses. , 2002, Cell motility and the cytoskeleton.

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

[25]  J. McNally,et al.  MYOSIN II REDISTRIBUTION DURING REAR RETRACTION AND THE ROLE OF FILAMENT ASSEMBLY AND DISASSEMBLY , 2002, Cell biology international.

[26]  D. Soll,et al.  Ponticulin plays a role in the positional stabilization of pseudopods , 1995, The Journal of cell biology.

[27]  M. Sheetz,et al.  Cell migration as a five-step cycle. , 1999, Biochemical Society symposium.

[28]  M. Lokuta,et al.  Type Igamma PIP kinase is a novel uropod component that regulates rear retraction during neutrophil chemotaxis. , 2007, Molecular biology of the cell.

[29]  Edward Voss,et al.  3D-DIASemb: a computer-assisted system for reconstructing and motion analyzing in 4D every cell and nucleus in a developing embryo. , 2002, Developmental biology.

[30]  G. Shaulsky,et al.  The internal phosphodiesterase RegA is essential for the suppression of lateral pseudopods during Dictyostelium chemotaxis. , 2000, Molecular biology of the cell.

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

[32]  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.

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

[34]  A. Huttenlocher,et al.  The PCH family member proline-serine-threonine phosphatase-interacting protein 1 targets to the leukocyte uropod and regulates directed cell migration. , 2008, Molecular biology of the cell.

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

[36]  J. Spudich,et al.  Chemoattractant-elicited translocation of myosin in motile Dictyostelium. , 1989, Cell motility and the cytoskeleton.

[37]  Gary G. Borisy,et al.  Mechanism of filopodia initiation by reorganization of a dendritic network , 2003, The Journal of cell biology.

[38]  T. Naismith,et al.  Myosin-based cortical tension in Dictyostelium resolved into heavy and light chain-regulated components , 1996, Journal of Muscle Research and Cell Motility.

[39]  A. Scott.  Nematode sperm. , 1996, Parasitology today.

[40]  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.

[41]  E. Voss,et al.  The role of myosin heavy chain phosphorylation in Dictyostelium motility, chemotaxis and F-actin localization , 2004, Journal of Cell Science.

[42]  Janet L. Smith,et al.  Signaling pathways regulating Dictyostelium myosin II , 2004, Journal of Muscle Research & Cell Motility.

[43]  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.

[44]  Thomas E Schaus,et al.  Performance of a population of independent filaments in lamellipodial protrusion. , 2008, Biophysical journal.

[45]  C. Parent,et al.  Making all the right moves: chemotaxis in neutrophils and Dictyostelium. , 2004, Current opinion in cell biology.

[46]  R. Adelstein,et al.  Nonmuscle myosin II moves in new directions , 2008, Journal of Cell Science.

[47]  J. Theriot,et al.  Crawling toward a unified model of cell mobility: spatial and temporal regulation of actin dynamics. , 2004, Annual review of biochemistry.

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

[49]  Deborah Wessels,et al.  Computer-Assisted Systems for Dynamic 3D Reconstruction and Motion Analysis of Living Cells , 2007 .

[50]  E. Raz,et al.  Signaling pathways controlling primordial germ cell migration in zebrafish , 2004, Journal of Cell Science.

[51]  Revathi Ananthakrishnan,et al.  The Forces Behind Cell Movement , 2007, International journal of biological sciences.

[52]  Jay X. Tang,et al.  Nonmuscle myosin heavy chain IIA mediates integrin LFA-1 de-adhesion during T lymphocyte migration , 2008, The Journal of experimental medicine.

[53]  Y. Fukui,et al.  Myosin II-independent F-actin flow contributes to cell locomotion in dictyostelium. , 1999, Journal of cell science.

[54]  J W Sedat,et al.  Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. , 2000, Science.

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

[56]  D A Knecht,et al.  Three-dimensional localization of wild-type and myosin II mutant cells during morphogenesis of Dictyostelium. , 1995, Developmental biology.

[57]  Y. Fukui.  MECHANISTICS OF AMOEBOID LOCOMOTION: SIGNAL TO FORCES , 2002, Cell biology international.

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

[59]  D R Soll,et al.  A computer-assisted system for reconstructing and interpreting the dynamic three-dimensional relationships of the outer surface, nucleus and pseudopods of crawling cells. , 1998, Cell motility and the cytoskeleton.

[60]  Paul Herzmark,et al.  Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils , 2002, Nature Cell Biology.

[61]  Julie A. Theriot,et al.  Actin microfilament dynamics in locomoting cells , 1991, Nature.

[62]  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.

[63]  J. Spudich,et al.  In pursuit of myosin function. , 1989, Cell regulation.

[64]  T. Egelhoff,et al.  Dictyostelium myosin heavy chain kinase A regulates myosin localization during growth and development , 1996, The Journal of cell biology.

[65]  Andrzej GręObecki,et al.  Membrane and Cytoskeleton Flow in Motile Cells with Emphasis on the Contribution of Free-Living Amoebae , 1994 .

[66]  D. Soll,et al.  The chemotaxis defect of Shwachman-Diamond Syndrome leukocytes. , 2004, Cell motility and the cytoskeleton.

[67]  D. O’Day,et al.  Calmodulin-binding proteins in the model organism Dictyostelium: a complete & critical review. , 2008, Cellular signalling.

[68]  D. Soll,et al.  Cofilin determines the migration behavior and turning frequency of metastatic cancer cells , 2007, The Journal of cell biology.

[69]  Michael Loran Dustin.  Membrane domains and the immunological synapse: keeping T cells resting and ready. , 2002, The Journal of clinical investigation.

[70]  Shu Chien,et al.  Biochemistry and biomechanics of cell motility. , 2005, Annual review of biomedical engineering.

[71]  J. Murray,et al.  Three-dimensional motility cycle in leukocytes. , 1992, Cell motility and the cytoskeleton.

[72]  D. Soll,et al.  A contextual framework for characterizing motility and chemotaxis mutants in Dictyostelium discoideum , 2004, Journal of Muscle Research & Cell Motility.

[73]  J. Spudich,et al.  Dictyostelium myosin heavy chain phosphorylation sites regulate myosin filament assembly and localization in vivo , 1993, Cell.

[74]  E. Elson,et al.  Surface particle transport mechanism independent of myosin II in Dictyostelium , 1992, Nature.

[75]  P. Devreotes,et al.  Adenosine 3',5'-monophosphate waves in Dictyostelium discoideum: a demonstration by isotope dilution--fluorography. , 1981, Science.

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

[77]  J. Kolega.  The role of myosin II motor activity in distributing myosin asymmetrically and coupling protrusive activity to cell translocation. , 2006, Molecular biology of the cell.

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

[79]  F. Maxfield,et al.  Ca2+-dependent myosin II activation is required for uropod retraction during neutrophil migration. , 2000, Journal of cell science.

[80]  S. Brown,et al.  Spatial and temporal control of nonmuscle myosin localization: identification of a domain that is necessary for myosin filament disassembly in vivo , 1991, The Journal of cell biology.