Cell migration in multicellular environments

Development Growth and Differentiation

Volumn 53, Issue 4, 2011, Pages 528-537

  Tsujioka, Masatsune ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b Science and Technology Agency   (Japan)

Author keywords

Cell adhesion; Cell migration; Cytoskeleton

Indexed keywords

ALPHA ACTININ; CYTOSKELETON PROTEIN; FILAMIN; MYOSIN HEAVY CHAIN; MYOSIN LIGHT CHAIN; PAXILLIN; TALIN;

BIOLOGICAL MODEL; CELL ADHESION; CELL AGGREGATION; CELL INTERACTION; CELL MIGRATION; CELL MOTION; CELL MUTANT; CELL POLARITY; DICTYOSTELIUM DISCOIDEUM; EXTRACELLULAR MATRIX; LIFE CYCLE; MORPHOGENESIS; NONHUMAN; REVIEW;

CELL MOVEMENT; DICTYOSTELIUM; MODELS, BIOLOGICAL;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM;

EID: 79956130413     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2011.01268.x     Document Type: Review

References (75)

1. Aman, A. & Piotrowski, T. 2010. Cell migration during morphogenesis. Dev. Biol. 341, 20-33.
2. Araki, T., Abe, T., Williams, J. G. & Maeda, Y. 1997. Symmetry breaking in Dictyostelium morphogenesis: evidence that a combination of cell cycle stage and positional information dictates cell fate. Dev. Biol. 192, 645-648.
3. Blaser, H., Reichman-Fried, M., Castanon, I., Dumstrei, K., Marlow, F. L., Kawakami, K., Solnica-Krezel, L., Heisenberg, C. P. & Raz, E. 2006. Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev. Cell 11, 613-627.
4. Bukahrova, T., Weijer, G., Bosgraaf, L., Dormann, D., Van Haastert, P. J. & Weijer, C. J. 2005. Paxillin is required for cell-substrate adhesion, cell sorting and slug migration during Dictyostelium development. J. Cell Sci. 118, 4295-4310.
5. Byrd, D. T. & Kimble, J. 2009. Scratching the niche that controls Caenorhabditis elegans germline stem cells. Semin. Cell Dev. Biol. 20, 1107-1113.
6. Chen, P., Ostrow, B. D., Tafuri, S. R. & Chisholm, R. L. 1994. Targeted disruption of the Dictyostelium RMLC gene produces cells defective in cytokinesis and development. J. Cell Biol. 127, 1933-1944.
7. Chen, T. L., Kowalczyk, P. A., Ho, G. & Chisholm, R. L. 1995. Targeted disruption of the Dictyostelium myosin essential light chain gene produces cells defective in cytokinesis and morphogenesis. J. Cell Sci. 108(Pt 10), 3207-3218.
8. Chuai, M., Dormann, D. & Weijer, C. J. 2009. Imaging cell signalling and movement in development. Semin. Cell Dev. Biol. 20, 947-955.
9. Conti, F. J., Felder, A., Monkley, S., Schwander, M., Wood, M. R., Lieber, R., Critchley, D. & Muller, U. 2008. Progressive myopathy and defects in the maintenance of myotendinous junctions in mice that lack talin 1 in skeletal muscle. Development 135, 2043-2053.
10. Conti, F. J., Monkley, S. J., Wood, M. R., Critchley, D. R. & Muller, U. 2009. Talin 1 and 2 are required for myoblast fusion, sarcomere assembly and the maintenance of myotendinous junctions. Development 136, 3597-3606.
11. Cornillon, S., Gebbie, L., Benghezal, M., Nair, P., Keller, S., Wehrle-Haller, B., Charette, S. J., Bruckert, F., Letourneur, F. & Cosson, P. 2006. An adhesion molecule in free-living Dictyostelium amoebae with integrin beta features. EMBO Rep. 7, 617-621.
12. Cox, D., Condeelis, J., Wessels, D., Soll, D., Kern, H. & Knecht, D. A. 1992. Targeted disruption of the ABP-120 gene leads to cells with altered motility. J. Cell Biol. 116, 943-955.
13. Cox, D., Ridsdale, J. A., Condeelis, J. & Hartwig, J. 1995. Genetic deletion of ABP-120 alters the three-dimensional organization of actin filaments in Dictyostelium pseudopods. J. Cell Biol. 128, 819-835.
14. Critchley, D. R. 2004. Cytoskeletal proteins talin and vinculin in integrin-mediated adhesion. Biochem. Soc. Trans. 32, 831-836.
15. Cukierman, E., Pankov, R., Stevens, D. R. & Yamada, K. M. 2001. Taking cell-matrix adhesions to the third dimension. Science 294, 1708-1712.
16. De Lozanne, A. & Spudich, J. A. 1987. Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236, 1086-1091.
17. Deakin, N. O. & Turner, C. E. 2008. Paxillin comes of age. J. Cell Sci. 121, 2435-2444.
18. Del Rio, A., Perez-Jimenez, R., Liu, R., Roca-Cusachs, P., Fernandez, J. M. & Sheetz, M. P. 2009. Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641.
19. Dormann, D. & Weijer, C. J. 2006. Imaging of cell migration. EMBO J. 25, 3480-3493.
20. Early, A., Abe, T. & Williams, J. 1995. Evidence for positional differentiation of prestalk cells and for a morphogenetic gradient in Dictyostelium. Cell 83, 91-99.
21. Eichinger, L., Pachebat, J. A., Glockner, G., Rajandream, M. A., Sucgang, R., Berriman, M., Song, J., Olsen, R., Szafranski, K., Xu, Q., Tunggal, B., Kummerfeld, S., Madera, M., Konfortov, B. A., Rivero, F., Bankier, A. T., Lehmann, R., Hamlin, N., Davies, R., Gaudet, P., Fey, P., Pilcher, K., Chen, G., Saunders, D., Sodergren, E., Davis, P., Kerhornou, A., Nie, X., Hall, N., Anjard, C., Hemphill, L., Bason, N., Farbrother, P., Desany, B., Just, E., Morio, T., Rost, R., Churcher, C., Cooper, J., Haydock, S., van Driessche, N., Cronin, A., Goodhead, I., Muzny, D., Mourier, T., Pain, A., Lu, M., Harper, D., Lindsay, R., Hauser, H., James, K., Quiles, M., Madan Babu, M., Saito, T., Buchrieser, C., Wardroper, A., Felder, M., Thangavelu, M., Johnson, D., Knights, A., Loulseged, H., Mungall, K., Oliver, K., Price, C., Quail, M. A., Urushihara, H., Hernandez, J., Rabbinowitsch, E., Steffen, D., Sanders, M., Ma, J., Kohara, Y., Sharp, S., Simmonds, M., Spiegler, S., Tivey, A., Sugano, S., White, B., Walker, D., Woodward, J., Winckler, T., Tanaka, Y., Shaulsky, G., Schleicher, M., Weinstock, G., Rosenthal, A., Cox, E. C., Chisholm, R. L., Gibbs, R., Loomis, W. F., Platzer, M., Kay, R. R., Williams, J., Dear, P. H., Noegel, A. A., Barrell, B. & Kuspa, A. 2005. The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43-57.
22. Fackler, O. T. & Grosse, R. 2008. Cell motility through plasma membrane blebbing. J. Cell Biol. 181, 879-884.
23. Faix, J., Steinmetz, M., Boves, H., Kammerer, R. A., Lottspeich, F., Mintert, U., Murphy, J., Stock, A., Aebi, U. & 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.
24. Fey, P., Stephens, S., Titus, M. A. & Chisholm, R. L. 2002. SadA, a novel adhesion receptor in Dictyostelium. J. Cell Biol., 159, 1109-1119.
25. Fraley, S. I., Feng, Y., Krishnamurthy, R., Kim, D. H., Celedon, A., Longmore, G. D. & Wirtz, D. 2010. A distinctive role for focal adhesion proteins in three-dimensional cell motility. Nat. Cell Biol. 12, 598-604.
26. Grant, W. N. & Williams, K. L. 1983. Monoclonal antibody characterisation of slime sheath: the extracellular matrix of Dictyostelium discoideum. EMBO J. 2, 935-940.
27. Harjanto, D. & Zaman, M. H. 2010. Matrix mechanics and receptor-ligand interactions in cell adhesion. Org. Biomol. Chem. 8, 299-304.
28. Hemmings, L., Rees, D. J., Ohanian, V., Bolton, S. J., Gilmore, A. P., Patel, B., Priddle, H., Trevithick, J. E., Hynes, R. O. & Critchley, D. R. 1996. Talin contains three actin-binding sites each of which is adjacent to a vinculin-binding site. J. Cell Sci. 109(Pt 11), 2715-2726.
29. Honigberg, L. & Kenyon, C. 2000. Establishment of left/right asymmetry in neuroblast migration by UNC-40/DCC, UNC-73/Trio and DPY-19 proteins in C. elegans. Development 127, 4655-4668.
30. Inouye, K. 2003. Pattern formation by cell movement in closely-packed tissues. In Morphogenesis and Pattern Formation in Biological Systems, Chapter 16 (eds T. Sekimura, N. Noji & P. K. Maini), pp. 191-202, Springer-Verlag, Tokyo.
31. Itoh, Y. & Seiki, M. 2006. MT1-MMP: a potent modifier of pericellular microenvironment. J. Cell. Physiol. 206, 1-8.
32. Iwadate, Y. & Yumura, S. 2008. Actin-based propulsive forces and myosin-II-based contractile forces in migrating Dictyostelium cells. J. Cell Sci. 121, 1314-1324.
33. Jang, A. C., Starz-Gaiano, M. & Montell, D. J. 2007. Modeling migration and metastasis in Drosophila. J. Mammary Gland Biol. Neoplasia 12, 103-114.
34. Jay, P. Y., Pham, P. A., Wong, S. A. & Elson, E. L. 1995. A mechanical function of myosin II in cell motility. J. Cell Sci. 108(Pt 1), 387-393.
35. Kardash, E., Reichman-Fried, M., Maitre, J. L., Boldajipour, B., Papusheva, E., Messerschmidt, E. M., Heisenberg, C. P. & Raz, E. 2010. A role for Rho GTPases and cell-cell adhesion in single-cell motility in vivo. Nat. Cell Biol. 12, 47-53. sup pp 1-11.
36. Kibler, K., Svetz, J., Nguyen, T. L., Shaw, C. & Shaulsky, G. 2003. A cell-adhesion pathway regulates intercellular communication during Dictyostelium development. Dev. Biol. 264, 506-521.
37. Knecht, D. A. & Loomis, W. F. 1987. Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science 236, 1081-1086.
38. Knobel, K. M., Jorgensen, E. M. & Bastiani, M. J. 1999. Growth cones stall and collapse during axon outgrowth in Caenorhabditis elegans. Development 126, 4489-4498.
39. Kolsch, V., Charest, P. G. & Firtel, R. A. 2008. The regulation of cell motility and chemotaxis by phospholipid signaling. J. Cell Sci. 121, 551-559.
40. Laevsky, G. & 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, 3761-3770.
41. Lammermann, T., Bader, B. L., Monkley, S. J., Worbs, T., Wedlich-Soldner, R., Hirsch, K., Keller, M., Forster, R., Critchley, D. R., Fassler, R. & Sixt, M. 2008. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453, 51-55.
42. Li, X. Y., Ota, I., Yana, I., Sabeh, F. & Weiss, S. J. 2008. Molecular dissection of the structural machinery underlying the tissue-invasive activity of membrane type-1 matrix metalloproteinase. Mol. Biol. Cell 19, 3221-3233.
43. Manstein, D. J., Titus, M. A., De Lozanne, A. & Spudich, J. A. 1989. Gene replacement in Dictyostelium: generation of myosin null mutants. EMBO J. 8, 923-932.
44. Marston, D. J. & Goldstein, B. 2006. Actin-based forces driving embryonic morphogenesis in Caenorhabditis elegans. Curr. Opin. Genet. Dev. 16, 392-398.
45. Marston, D. J., Roh, M., Mikels, A. J., Nusse, R. & Goldstein, B. 2008. Wnt signaling during Caenorhabditis elegans embryonic development. Methods Mol. Biol. 469, 103-111.
46. Medalia, O., Beck, M., Ecke, M., Weber, I., Neujahr, R., Baumeister, W. & Gerish, G. 2007. Organization of actin networks in intact filopodia. Curr. Biol. 17, 79-84.
47. Monkley, S. J., Pritchard, C. A. & Critchley, D. R. 2001. Analysis of the mammalian talin2 gene TLN2. Biochem. Biophys. Res. Commun. 286, 880-885.
48. Nagasaki, A., Kanada, M. & Uyeda, T. Q. 2009. Cell adhesion molecules regulate contractile ring-independent cytokinesis in Dictyostelium discoideum. Cell Res. 19, 236-246.
49. Nayal, A., Webb, D. J. & Horwitz, A. F. 2004. Talin: an emerging focal point of adhesion dynamics. Curr. Opin. Cell Biol. 16, 94-98.
50. Niewohner, J., Weber, I., Maniak, M., Muller-Taubenberger, A. & Gerisch, G. 1997. Talin-null cells of Dictyostelium are strongly defective in adhesion to particle and substrate surfaces and slightly impaired in cytokinesis. J. Cell Biol. 138, 349-361.
51. Pang, K. M., Lee, E. & Knecht, D. A. 1998. Use of a fusion protein between GFP and an actin-binding domain to visualize transient filamentous-actin structures. Curr. Biol. 8, 405-408.
52. Pasternak, C., Spudich, J. A. & Elson, E. L. 1989. Capping of surface receptors and concomitant cortical tension are generated by conventional myosin. Nature 341, 549-551.
53. Pollard, T. D. & Cooper, J. A. 2009. Actin, a central player in cell shape and movement. Science 326, 1208-1212.
54. Rivero, F., Furukawa, R., Fechheimer, M. & Noegel, A. A. 1999. Three actin cross-linking proteins, the 34kDa actin-bundling protein, alpha-actinin and gelation factor (ABP-120), have both unique and redundant roles in the growth and development of Dictyostelium. J. Cell Sci. 112(Pt 16), 2737-2751.
55. Sabeh, F., Ota, I., Holmbeck, K., Birkedal-Hansen, H., Soloway, P., Balbin, M., Lopez-Otin, C., Shapiro, S., Inada, M., Krane, S., Allen, E., Chung, D. & Weiss, S. J. 2004. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J. Cell Biol. 167, 769-781.
56. Saxe 3rd, C. L., Ginsburg, G. T., Louis, J. M., Johnson, R., Devreotes, P. N. & Kimmel, A. R. 1993. CAR2, a prestalk cAMP receptor required for normal tip formation and late development of Dictyostelium discoideum. Genes Dev. 7, 262-272.
57. Shelden, E. & Knecht, D. A. 1995. Mutants lacking myosin II cannot resist forces generated during multicellular morphogenesis. J. Cell Sci. 108(Pt 3), 1105-1115.
58. Silhankova, M. & Korswagen, H. C. 2007. Migration of neuronal cells along the anterior-posterior body axis of C. elegans: Wnts are in control. Curr. Opin. Genet. Dev. 17, 320-325.
59. Tsujioka, M., Machesky, L. M., Cole, S. L., Yahata, K. & Inouye, K. 1999. A unique talin homologue with a villin headpiece-like domain is required for multicellular morphogenesis in Dictyostelium. Curr. Biol. 9, 389-392.
60. Tsujioka, M., Yoshida, K. & Inouye, K. 2004. Talin B is required for force transmission in morphogenesis of Dictyostelium. EMBO J. 23, 2216-2225.
61. Tsujioka, M., Yoshida, K., Nagasaki, A., Yonemura, S., Muller-Taubenberger, A. & Uyeda, T. Q. 2008. Overlapping functions of the two talin homologues in Dictyostelium. Eukaryot. Cell 7, 906-916.
62. Uchida, K. S., Kitanishi-Yumura, T. & 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.
63. Urushihara, H. 2008. Developmental biology of the social amoeba: history, current knowledge and prospects. Dev. Growth Differ. 50(Suppl 1), S277-281.
64. Vicente-Manzanares, M., Ma, X., Adelstein, R. S. & Horwitz, A. R. 2009. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. 10, 778-790.
65. Weijer, C. J. 2004. Dictyostelium morphogenesis. Curr. Opin. Genet. Dev. 14, 392-398.
66. Wessels, D., Soll, D. R., Knecht, D., Loomis, W. F., De Lozanne, A. & Spudich, J. 1988. Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. Dev. Biol. 128, 164-177.
67. Williams, J. G. 2010. Dictyostelium finds new roles to model. Genetics 185, 717-726.
68. Witke, W., Schleicher, M. & 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.
69. Wolf, K., Mazo, I., Leung, H., Engelke, K., von Andrian, U. H., Deryugina, E. I., Strongin, A. Y., Brocker, E. B. & Friedl, P. 2003. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160, 267-277.
70. Xu, X. S., Lee, E., Chen, T., Kuczmarski, E., Chisholm, R. L. & Knecht, D. A. 2001. During multicellular migration, myosin ii serves a structural role independent of its motor function. Dev. Biol. 232, 255-264.
71. Yoshida, K. & Inouye, K. 2001. Myosin II-dependent cylindrical protrusions induced by quinine in Dictyostelium: antagonizing effects of actin polymerization at the leading edge. J. Cell Sci. 114, 2155-2165.
72. Yoshida, K. & Soldati, T. 2006. Dissection of amoeboid movement into two mechanically distinct modes. J. Cell Sci. 119, 3833-3844.
73. Yumura, S. & Fukui, Y. 1998. Spatiotemporal dynamics of actin concentration during cytokinesis and locomotion in Dictyostelium. J. Cell Sci. 111(Pt 15), 2097-2108.
74. Zhang, X., Jiang, G., Cai, Y., Monkley, S. J., Critchley, D. R. & Sheetz, M. P. 2008. Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat. Cell Biol. 10, 1062-1068.
75. Ziegler, W. H., Liddington, R. C. & Critchley, D. R. 2006. The structure and regulation of vinculin. Trends Cell Biol. 16, 453-460.