Myosin II is essential for the spatiotemporal organization of traction forces during cell motility

Molecular Biology of the Cell

Volumn 21, Issue 3, 2010, Pages 405-417

  Meili, Ruedi ^a   Alonso Latorre, Baldomero ^b   Del Álamo, Juan C ^b   Firtel, Richard A ^a   Lasheras, Juan C ^b,c  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN II;

ARTICLE; CELL MOTILITY; CELL STRESS; FORCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION;

ACTINS; ANIMALS; CELL MOVEMENT; CYTOSKELETON; DICTYOSTELIUM; MATHEMATICS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MYOSIN TYPE II; PERIODICITY; STRESS, MECHANICAL;

EID: 76049104121     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-08-0703     Document Type: Article

References (66)

1. Abercrombie, M., Heaysman, J., and Pegrum, S. (1970). The locomotion of fibroblasts in culture. I. Movements of the leading edge. Exp. Cell Res. 59, 393-398.
2. Bosgraaf, L., and van Haastert, P. (2006). The regulation of myosin II in Dictyostelium. Eur. J. Cell Biol. 85, 969-979.
3. Butler, J. P., Tolic-Norrelykke, I. M., Fabry, B., and Fredberg, J. J. (2002). Traction fields, moments, and strain energy that cells exert on their surroundings. Am J. Physiol. Cell Physiol. 282, C595-C605.
4. Charras, G. (2008). A short history of blebbing. J. Microsc. 231, 466-478.
5. 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, 1933-1944.
6. 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, 3207-3218.
7. Condeelis, J., Hall, A., Bresnick, A., Warren, V., Hock, R., Bennett, H., and Ogihara, S. (1988). Actin polymerization and pseudopod extension during amoeboid chemotaxis. Cell Motil. Cytoskeleton 10, 77-90.
8. de la Roche, M., and Cote, G. (2001). Regulation of Dictyostelium myosin I and II. Biochim. Biophys. Acta 1525, 245-261.
9. Del Alamo, J., Meili, R., Alonso-Latorre, B., Rodriguez-Rodriguez, J., Aliseda, A., Firtel, R., and Lasheras, J. (2007). Spatio-temporal analysis of eukaryotic cell motility by improved force cytometry. Proc. Natl. Acad. Sci. USA 104, 13343-13348.
10. Delozanne, A., and Spudich, J. A. (1987). Disruption of the Dictyostelium myosin heavy-chain gene by homologous recombination. Science 236, 1086-1091.
11. Devreotes, P., and Zigmond, S. (1988). Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu. Rev. Cell Biol. 4, 649-686.
12. Effler, J. C., Kee, Y. S., Berk, J. M., Tran, M. N., Iglesias, P. A., and Robinson, D. N. (2006). Mitosis-specific mechanosensing and contractile-protein redistribution control cell shape. Curr. Biol. 16, 1962-1967.
13. Faix, J., Steinmetz, M., Boves, H., Kammerer, R. A., Lottspeich, F., Mintert, U., Murphy, J., Stock, A., Aebi, U., and Gerisch, G. (1996). Cortexillins, major determinants of cell shape and size, are actin-bundling proteins with a parallel coiled-coil tail. Cell 86, 631-642.
14. Feneberg, W., Westphal, M., and Sackmann, E. (2001). Dictyostelium cells' cytoplasm as an active viscoplastic body. Eur. Biophys. J. 30, 284-294.
15. Fisher, P., Merkl, R., and Gerisch, G. (1989). 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. J. Cell Biol. 108, 973-984.
16. Fukui, Y., Murray, J., Riddelle, K., and Soll, D. (1991). Cell behavior and actomyosin organization in Dictyostelium during substrate exploration. Cell Struct. Funct. 16, 289-301.
17. Fukui, Y., Uyeda, T., Kitayama, C., and Inoue, S. (2000). How well can an amoeba climb? Proc. Natl. Acad. Sci. USA 97, 10020-10025.
18. Fukui, Y., and Yumura, S. (1986). Actomyosin dynamics in chemotactic amoeboid movement of Dictyostelium. Cell Motil. Cytoskeleton 6, 662-673.
19. Girard, K., Kuo, S., and Robinson, D. (2006). Dictyostelium myosin II mechanochemistry promotes active behavior of the cortex on long time scales. Proc. Natl. Acad. Sci. USA 103, 2103-2108.
20. Griffith, L. (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, 1309-1323.
21. Grinstead, C., and Snell, J. (1997). Introduction to Probability, Providence, RI: American Mathematical Society.
22. Heid, P. J., Geiger, J., Wessels, D., Voss, E., and Soll, D. R. (2005). Computerassisted analysis of filopod formation and the role of myosin II heavy chain phosphorylation in Dictyostelium. J. Cell Sci. 118, 2225-2237.
23. Huttenlocher, A., Sandborg, R., and Horwitz, A. (1995). Adhesion in cell migration. Curr. Opin. Cell Biol. 7, 697-706.
24. Iwadate, Y., and Yumura, S. (2008). Actin-based propulsive forces and myosin-II-based contractile forces in migrating Dictyostelium cells. J. Cell Sci. 121, 1314-1324.
25. Iwasa, J., and Mullins, R. (2007). Spatial and temporal relationships between actin-filament nucleation, capping, and disassembly. Curr. Biol. 17, 395-406.
26. Jacobelli, J., Bennett, F. C., Pandurangi, P., Tooley, A. J., and Krummel, M. F. (2009). Myosin-IIA and ICAM-1 regulate the interchange between two distinct modes of T cell migration. J. Immunol. 182, 2041-2050.
27. Jay, P., Pham, P., Wong, S., and Elson, E. (1995). A mechanical function of myosin II in cell motility. J. Cell Sci. 108, 387-393.
28. Keer, L. (1964). Stress distribution at the edge of an equilibrium crack. J. Mech. Phys. Sol. 12, 149-163.
29. Keren, K., Pincus, Z., Allen, G. M., Barnhart, E. L., Marriott, G., Mogilner, A., and Theriot, J. A. (2008). Mechanism of shape determination in motile cells. Nature 453, 475-480.
30. Ladam, G., Vonna, L., and Sackmann, E. (2005). Protrusion force transmission of amoeboid cells crawling on soft biological tissue. Acta Biomater. 1, 485-497.
31. Laevsky, G., and Knecht, D. (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, 3761-3770.
32. Langridge, P., and Kay, R. (2006). Blebbing of Dictyostelium cells in response to chemoattractant. Exp. Cell Res. 312, 2009-2017.
33. Lauffenburger, D., and Horwitz, A. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
34. Liu, X., Ito, K., Morimoto, S., Hikkoshi-Iwane, A., Yanagida, T., and Uyeda, T. (1998). Filament structure as an essential factor for regulation of Dictyostelium myosin by regulatory light chain phosphorylation. Proc. Natl. Acad. Sci. USA 95, 14124-14129.
35. Lombardi, M., Knecht, D., 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, 1624-1634.
36. Meili, R., Ellsworth, C., Lee, S., Reddy, T., Ma, H., and Firtel, R. (1999). Chemoattractant-mediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium. EMBO J. 18, 2092-2105.
37. Miller, M. J., Wei, S. H., Parker, I., and Cahalan, M. D. (2002). Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296, 1869-1873.
38. Pasternak, C., Spudich, J., and Elson, E. (1989). Capping of surface receptors and concomitant cortical tension are generated by conventional myosin. Nature 341, 549-551.
39. Pollard, T., and Borisy, G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
40. Pollenz, R. S., Chen, T.L.L., Trivinoslagos, L., and Chisholm, R. L. (1992). The Dictyostelium essential light chain is required for myosin function. Cell 69, 951-962.
41. Reichl, E. M., Ren, Y., Morphew, M. K., Delannoy, M., Effler, J. C., Girard, K. D., Divi, S., Iglesias, P. A., Kuo, S. C., and Robinson, D. N. (2008). Interactions between myosin and actin crosslinkers control cytokinesis contractility dynamics and mechanics. Curr. Biol. 18, 471-480.
42. Ren, Y., Effler, J. C., Norstrom, M., Luo, T., Firtel, R. A., Iglesias, P. A., Rock, R. S., and Robinson, D. N. (2009). Mechanosensing through cooperative interactions between myosin ii and the actin crosslinker cortexillin I. Curr. Biol. 19, 1421-1428.
43. Segall, J. (1987). Selection of chemotaxis mutants of Dictyostelium discoideum. J. Cell Biol. 104, 151-161.
44. Shelden, E., and Knecht, D. (1995). Mutants lacking myosin II cannot resist forces generated during multicellular morphogenesis. J. Cell Sci. 108 1105-1115.
45. Shelden, E., and Knecht, D. (1996). Dictyostelium cell shape generation requires myosin II. Cell Motil. Cytoskeleton 35, 59-67.
46. 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, L58-60.
47. Soll, D. R., Voss, E., Varnum-Finney, B., and Wessels, D. (1988). "Dynamic Morphology System": a method for quantitating changes in shape, pseudopod formation, and motion in normal and mutant amoebae of Dictyostelium discoideum. J. Cell. Biochem. 37, 177-192.
48. Stepanovic, V., Wessels, D., Daniels, K., Loomis, W. F., and Soll, D. R. (2005). Intracellular role of adenylyl cyclase in regulation of lateral pseudopod formation during Dictyostelium chemotaxis. Eukaryot. Cell 4, 775-786.
49. Stites, J., Wessels, D., Uhl, A., Egelhoff, T., Shutt, D., and Soll, D. (1998). Phosphorylation of the Dictyostelium myosin II heavy chain is necessary for maintaining cellular polarity and suppressing turning during chemotaxis. Cell Motil. Cytoskeleton 39, 31-51.
50. Uchida, K., Kitanishi-Yumura, T., and Yumura, S. (2003). Myosin II contributes to the posterior contraction and the anterior extension during the retraction phase in migrating Dictyostelium cells. J. Cell Sci. 116, 51-60.
51. Uchida, K., and Yumura, S. (2004). Dynamics of novel feet of Dictyostelium cells during migration. J. Cell Sci. 117, 1443-1455.
52. Varnum, B., and Soll, D. R. (1984). Effects of cAMP on single cell motility in Dictyostelium. J. Cell Biol. 99, 1151-1155.
53. Volk, A. P., Heise, C. K., Hougen, J. L., Artman, C. M., Volk, K. A., Wessels, D., Soll, D. R., Nauseef, W. M., Lamb, F. S., and Moreland, J. G. (2008). ClC-3 and IClswell are required for normal neutrophil chemotaxis and shape change. J. Biol. Chem. 283, 34315-34326.
54. Wear, M., Schafer, D., and Cooper, J. (2000). Actin dynamics: assembly and disassembly of actin networks. Curr. Biol. 10, R891-R895.
55. 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, 1519-1530.
56. Wessels, D., Lusche, D., Kuhl, S., Heid, P., and Soll, D. (2007). PTEN plays a role in the suppression of lateral pseudopod formation during Dictyostelium motility and chemotaxis. J. Cell Sci. 120, 2517-2531.
57. Wessels, D., and Soll, D. R. (1990). Myosin II heavy chain null mutant of Dictyostelium exhibits defective intracellular particle movement. J. Cell Biol. 111, 1137-1148.
58. Wessels, D., Soll, D. R., Knecht, D., Loomis, W. F., De Lozanne, A., and Spudich, J. (1988). Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. Dev. Biol. 128, 164-177.
59. Wessels, D., Vawter-Hugart, H., Murray, J., and Soll, D. (1994). Three-dimensional dynamics of pseudopod formation and the regulation of turning during the motility cycle of Dictyostelium. Cell Motil. Cytoskeleton 27, 1-12.
60. Witke, W., Schleicher, M., and Noegel, A. A. (1992). Redundancy in the microfilament system: abnormal development of Dictyostelium cells lacking two F-actin cross-linking proteins. Cell 68, 53-62.
61. Xu, X., Kuspa, A., Fuller, D., Loomis, W., and Knecht, D. (1996). Cell-cell adhesion prevents mutant cells lacking myosin II from penetrating aggregation streams of Dictyostelium. Dev. Biol. 175, 218-226.
62. 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. Dev. Biol. 232, 255-264.
63. Yoshida, K., and Soldati, T. (2006). Dissection of amoeboid movement into two mechanically distinct modes. J. Cell Sci. 119, 3833-3844.
64. 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, 894-899.
65. Zaidel-Bar, R., Cohen, M., Addadi, L., and Geiger, B. (2004). Hierarchical assembly of cell-matrix adhesion complexes. Biochem. Sci. Trans. 32, 416-420.
66. Zigmond, S., and Hirsch, J. (1973). Leukocyte locomotion and chemotaxis. New methods for evaluation, and demonstration of a cell-derived chemotactic factor. J. Exp. Med. 137, 387-410.