The role of the cortical cytoskeleton: F-actin crosslinking proteins protect against osmotic stress, ensure cell size, cell shape and motility, and contribute to phagocytosis and development

Journal of Cell Science

Volumn 109, Issue 11, 1996, Pages 2679-2691

  Rivero, Francisco ^a   Köppel, Bernd ^a,d   Peracino, Barbara ^b   Bozzaro, Salvatore ^b   Siegert, Florian ^c   Weijer, Cornelis J ^c,e   Schleicher, Michael ^c   Albrecht, Richard ^a   Noegel, Angelika A ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b SAN LUIGI GONZAGA HOSPITAL   (Italy)

^c UNIVERSITY OF MUNICH   (Germany)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^e UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

actinin; 120 kDa gelation factor; Development; Dictyostelium; Video microscopy

Indexed keywords

F ACTIN;

ARTICLE; CELL MOTILITY; CELL MUTANT; CELL SHAPE; CELL SIZE; CROSS LINKING; CYTOSKELETON; NONHUMAN; OSMOTIC STRESS; PHAGOCYTOSIS; PRIORITY JOURNAL; SARCODINA;

ACTININ; ACTINS; ANIMALS; CARRIER PROTEINS; CELL MOVEMENT; CELL SIZE; CHEMOTAXIS; CYTOSKELETON; DICTYOSTELIUM; GENE EXPRESSION; MICROFILAMENT PROTEINS; MUTAGENESIS; OSMOLAR CONCENTRATION; PHAGOCYTOSIS;

DICTYOSTELIUM; SARCODINA;

EID: 0029859177     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. André, E., Brink, M., Gerisch, G., Isenberg, G., Noegel, A. A., Schleicher, M., Segall, J. E. and Wallraff, E. (1989). A Dictyostelium mutant deficient in severin, an F-actin fragmenting protein shows normal motility and chemotaxis. J. Cell Biol. 108, 985-995.
2. Berthold, J., Stadler, J., Bozzaro, S., Fichtner, B. and Gerisch, G. (1985). Carbohydrate and other epitopes of the contact site A glycoprotein of Dictyostelium discoideum as characterized by monoclonal antibodies. Cell Differ. 16, 187-202.
3. Bichler, G. and Weijer, C. J. (1994). A Dictyostelium anterior-like cell mutant reveals sequential steps in the prespore prestalk differentiation pathway. Development 120, 2857-2868.
4. Bozzaro, S., Merkl, R. and Gerisch, G. (1987). Cell adhesion: its quantification, assay of the molecules involved and selection of defective mutants in Dictyostelium and Polysphondylium. Meth. Cell Biol. 28, 359-385
5. Brink, M., Gerisch, G., Isenberg, G., Noegel, A. A., Segall, J. E., Wallraff, E. and Schleicher, M. (1990). A Dictyostelium mutant lacking an F-actin cross-linking protein, the 120-kD gelation factor. J. Cell Biol. 111, 1477-1489.
6. Cantiello, H. F., Prat, A. G., Bonventre, J. V., Cunningham, C. C., Hartwig, J. H. and Ausiello, D. A. (1993). Actin-binding protein contributes to cell volume regulatory ion channel activation in melanoma cells. J. Biol. Chem. 268, 4596-4599.
7. Ceccarelli, A. and Bozzaro, S. (1992). Selection of mutants defective in binding to immobilized carbohydrates in Dictyostelium discoideum. Animal Biology 1, 50-68.
8. Chowdbury, S., Smith, K. W. and Gustin, M. C. (1992). Osmotic stress and the yeast cytoskeleton: phenotype specific suppression of an actin mutation. J. Cell Biol. 118, 561-571.
9. Claviez, M., Pagh, K., Maruta, H., Baltes, W., Fisher, P. and Gerisch, G. (1982). Electron microscopic mapping of monoclonal antibodies on the tail region of Dictyostelium myosin. EMBO J. 1, 1017-1022.
10. 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. Cytoskel. 10, 77-90.
11. Condeelis, J. (1993). Understanding the cortex of crawling cells: Insights from Dictyostelium. Trends Cell Biol. 3, 371-376.
12. Cox, D., Condeelis, J., Wessels, D., Soll, D., Kern, H. and Knecht D. A. (1992). Targeted disruption of the ABP-120 gene leads to cells with altered motility. J. Cell Biol. 116, 943-955.
13. - Dictyostelium mutants. Mol. Biol. Cell 7, 803-823.
14. Cunningham, C. C., Gorlin, J. D., Kwiatkowski, D. J., Hartwig, J. H., Janmey, P. A., Byers, H. R. and Stossel T. P. (1992). Actin-binding protein requirement for cortical stability and efficient locomotion. Science 255, 325-327.
15. Cunningham, C. C. (1995). Actin polymerization and intracellular solvent flow in cell surface blebbing. J. Cell Biol. 129, 1589-1599.
16. De Hostos, E. L., Bradtke, B., Lottspeich, F., Guggenheim, R. and Gerisch, G. (1991). Coronin, an actin-binding protein of Dictyostelium discoideum localized to cell surface projections, has sequence similarities to G protein β subunits. EMBO J. 10, 4097-4104.
17. De Hostos, E. L., Rehfueß, C., Bradtke, B., Waddell, D. R., Albrecht, R., Murphy, J. and Gerisch, G. (1993). Dictyostelium mutants lacking the cytoskeletal protein coronin are defective in cytokinesis and cell motility. J. Cell Biol. 120, 163-173.
18. De Lozanne, A. and Spudich, J. A. (1987). Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236, 1086-1091.
19. Dingermann, T., Reindl, N., Werner, H., Hildebrandt, M., Nellen, W., Harwood, A., Williams, J. and Nerke, K. (1989). Optimization and in situ detection of Escherichia coli beta-galactosidase gene expression in Dictyostelium discoideum. Gene 85, 353-362.
20. Doolittle, K. W., Reddy, I. and McNally, J. G. (1995). 3D analysis of cell movement during normal and myosin-II-null cell morphogenesis in Dictyostelium. Dev. Biol. 167, 118-129.
21. Early, A. E., Williams, J. G., Meyer, H. E., Por, S. B., Smith, E., Williams, K. L. and Gooley, A. A. (1988). Structural characterization of Dictyostelium discoideum prespore-specific gene D19 and of its product, cell surface glycoprotein PsA. Mol. Cell. Biol. 8, 3458-3466.
22. Egelhoff, T. T., Brown, S. S., Manstein, D. J. and Spudich, J. A. (1989). Hygromycin resistance as a selectable marker in Dictyostelium. Mol. Cell. Biol. 9, 1965-1972.
23. Eichinger, L., Köppel, B., Noegel, A. A., Schleicher, M., Schliwa, M., Weijer, C. J., Witke, W. and Janmey, P. A. (1996). Mechanical perturbation elicits a phenotypic difference between Dictyostelium wild-type cells and cytoskeletal mutants. Biophys. J. 70, 1054-1060.
24. Eliott, S., Joss, G. H., Spudich, A. and Williams, K. L. (1993). Patterns in Dictyostelium discoideum: the role of myosin II in the transition from the unicellular to the multicellular phase. J. Cell Sci. 104, 457-466.
25. Faix, J., Gerisch, G. and Noegel, A. A. (1992). Overexpression of the csA cell adhesion molecule under its own cAMP-regulated promoter impairs morphogenesis in Dictyostelium discoideum. J. Cell Sci. 102, 203-214.
26. Fisher, P. R., 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.
27. Fukui, Y., Lynch, T. J., Brzeska, H. and Korn, E. D. (1989). Myosin I is located at the leading edges of locomoting Dictyostelium amoebae. Nature 341, 328-331.
28. Furukawa, R. and Fechheimer, M. (1994). Differential localization of α-actinin and the 30 kD actin-bundling protein in the cleavage furrrow, phagocytic cup, and contractile vacuole of Dictyostelium discoideum. Cell Motil. Cytoskel. 29, 46-56.
29. Gerisch, G. and Keller, H. U. (1981). Chemotactic reorientation of granulocytes stimulated with micropipettes containing fMet-Leu-Phe. J. Cell Sci. 52, 1-10.
30. 2+ independent F-actin capping proteins: Cap32/34, a capping protein from Dictyostelium discoideum, does not share sequence homologies with known capping proteins. J. Biol. Chem. 264, 12639-12647.
31. Haugwitz, M., Noegel, A. A., Rieger, D., Lottspeich, F. and Schleicher, M. (1991). Dictyostelium discoideum contains two profilin isoforms that differ in structure and function. J. Cell Sci. 100, 481-489.
32. Haugwitz, M., Noegel, A. A., Karakesisoglou, J. and Schleicher, M. (1994). Dictyostelium amoebae that lack G-actin-sequestering profilins show defects in F-actin content, cytokinesis, and development. Cell 79, 303-314.
33. Janssen, K.-P., Eichinger, L., Janmey, P., Noegel, A. A., Schliwa, M., Witke, W. and Schleicher, M. (1996). Viscoelastic properties of F-actin solutions in the presence of normal and mutated actin-binding proteins. Arch. Biochem. Biophys. 325, 183-189.
34. Jermyn, K. A., Berks, M., Kay, R. R. and Williams, J. E. (1987). Two distinct classes of prestalk-enriched mRNA sequences in Dictyostelium discoideum. Development 100, 745-755.
35. Jung, G. and Hammer, J. A. (1990). Generation and characterization of Dictyostelium cells deficient in a myosin I heavy chain isoform. J. Cell Biol. 110, 1955-1964.
36. Klein, P. S., Sun, T. J., Saxe III, C. L., Kimmel, A. R., Johnson, R. L. and Devreotes, P. N. (1988). A chemoattractant receptor controls development in Dictvostelium discoideum. Science 241, 1467-1472.
37. Knecht, D. A., Cohen, S. M., Loomis, W. F. and Lodish, H. F. (1986). Developmental regulation of Dictyostelium discoideum actin gene fusions carried on low-copy and high-copy transformation vectors. Mol. Cell. Biol. 6, 3973-3983.
38. Kuwayama, H., Ecke, M., Gerisch, G. and Van Haastert, P. (1996). Protection against osmotic stress by cGMP mediated myosin phosphorylation. Science 271, 207-209.
39. Kwon, H. M. and Handler, J. S. (1995). Cell volume regulated transporters of compatible osmolytes. Curr. Opin. Cell Biol. 7, 465-471.
40. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
41. Luby-Phelps, K. (1994). Physical properties of cytoplasm. Curr. Opin. Cell Biol. 6, 3-9.
42. Maniak, M., Rauchenberger, R., Albrecht, R., Murphy, J. and Gerisch, G. (1995). Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein tag. Cell 83, 915-924.
43. Manstein, D. J., Titus, M. A., De Lozanne, A. and Spudich, J. A. (1989). Gene replacement in Dictyostelium: generation of myosin null mutants. EMBO J. 8, 923-932.
44. Matsudaira, P. (1991). Modular organization of actin crosslinking proteins. Trends Biochem. Sci. 16, 87-92.
45. Newell, P. C., Telser, A. and Sussman, M. (1969). Alternative developmental pathways determined by environmental conditions in the cellular slime mould Dictyostelium discoideum. J. Bacteriol. 100, 763-768.
46. Noegel, A. A., Harloff, C., Hirth, P., Merkl, R., Modersitzki, M., Stadler, J., Weinhart, U., Westphal, M. and Gerisch, G. (1985). Probing an adhesion mutant of Dictyostelium discoideum with cDNA clones and monoclonal antibodies indicates a specific defect in the contact site A glycoprotein. EMBO J. 4, 3805-3810.
47. Noegel, A. A., Gerisch, G., Stadler, J. and Westphal, M. (1986). Complete sequence and transcript regulation of a cell adhesion protein from aggregating Dictyostelium cells. EMBO J. 5, 1473-1476.
48. Noegel, A. A., Rapp, S., Lottspeich, F., Schleicher, M. and Stewart, M. (1989). The Dictyostelium gelation factor shares a putative actin binding site with α-actinins and dystrophin and also has a rod domain containing six 100-residue motifs that appear to have a cross-beta conformation. J. Cell Biol. 109, 607-618.
49. Pollenz, R. S., Chen, T.-L. L., Trivinos-Lagos, L. and Chisholm, R. L. (1992). The Dictyostelium essential light chain is required for myosin function. Cell 69, 951-962.
50. Rietdorf, J., Siegert, F. and Weijer, C. J. (1996). Analysis of optical density wave propagation and cell movement during mound formation in Dictyostelium discoideum. Dev. Biol. 177, 427-438.
51. Rivero, F., Furukawa, R., Noegel, A. A. and Fechheimer, M. (1996). Dictyostelium discoideum cells lacking the 34,000 Dalton actin binding protein can grow, locomote and develop, but exhibit defects in regulation of cell structure and movement: A case of partial redundancy. J. Cell Biol. (in press).
52. Schleicher, M., Noegel, A. A., Schwarz, T., Wallraff, E., Brink, M., Faix, J., Gerisch, G. and Isenberg, G. (1988). A Dictyostelium mutant with severe defects in α-actinin: Its characterization by cDNA probes and monoclonal antibodies. J. Cell Sci. 90, 59-71.
53. Schleicher, M., André, B., Andréoli, C., Eichinger, L., Haugwitz, M., Hofmann, A., Karakesisoglou, J., Stöckelhuber, M. and Noegel, A. A. (1995). Structure/function studies on cytoskeletal proteins in Dictyostelium amoebae as a paradigm. FEBS Lett. 369, 38-42.
54. Segall, J. E., Fisher, P. R. and Gerisch, G. (1987). Selection of chemotaxis mutants of Dictyostelium discoideum. J. Cell Biol. 10, 151-161.
55. Shelden, E. and Knecht, D. A. (1995). Mutants lacking myosin II cannot resist forces generated during multicellular morphogenesis. J. Cell Sci. 108, 1105-1115.
56. Siegert, F. and Weijer, C. (1989). Digital image processing of optical density wave propagation in Dictyostelium discoideum and analysis of the effects of caffeine and ammonia. J. Cell Sci. 93, 325-335.
57. Siegert, F. and Weijer, C. J. (1992). Three-dimensional scroll waves organize Dictyostelium slugs. Proc. Nat. Acad. Sci. USA 89, 6433-6437.
58. Siegert, F. and Weijer, C. (1995). Spiral and concentric waves organize multicellular Dictyostelium mounds. Curr. Biol. 5, 937-943.
59. Simpson, P. A., Spudich, J. A. and Parham, P. (1984). Monoclonal antibodies prepared against Dictyostelium actin: characterization and interaction with actin. J. Cell Biol. 99, 287-295.
60. Springer, M. L., Patterson, B. and Spudich, J. A. (1994). Stage specific requirement for myosin II during Dictyostelium development. Development 120, 2651-2660.
61. Stossel, T. P. (1993). On the crawling of animal cells. Science 260, 1086-1094.
62. Traynor, D., Tasaka, M., Takeuchi, I. and Williams, J. (1994). Aberrant pattern formation in myosin heavy chain mutants of Dictyostelium. Development 120, 591-601.
63. Vogel, G. (1987). Endocytosis and recognition mechanisms in Dictyostelium discoideum. Meth. Cell Biol. 28, 129-138.
64. Wachsstock, D. H., Schwarz, W. H. and Pollard, T. D. (1994). Cross-linker dynamics determine the mechanical properties of actin gels. Biophys. J. 66, 801-809.
65. Wallraff, E., Schleicher, M., Modersitzki, M., Rieger, D., Isenberg, G. and Gerisch, G. (1986). Selection of Dictyostelium mutants defective in cytoskeletal proteins: Use of an antibody that binds to the ends of α-actinin rods. EMBO J. 5, 61-67.
66. Weiner, O. H., Murphy, J., Griffiths, G., Schleicher, M. and Noegel, A. A. (1993). The actin-binding protein comitin (p24) is a component of the Golgi apparatus. J. Cell Biol. 123, 23-34.
67. Wessels, D., Soll, D. R., Knecht, D. A., Loomis, W. F., De Lozanne, A. and Spudich, J. A. (1988). Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. Der. Biol. 128, 164-177.
68. Williams, K. L. and Newell, P. C. (1976). A genetic study of aggregation in the cellular slime mould Dictyostelium discoideum using complementation analysis. Genetics 82, 287-307.
69. Witke, W., Nellen, W. and Noegel, A. A. (1987). Homologous recombination in the Dictyostelium α-actinin gene leads to an altered mRNA and lack of the protein. EMBO J. 6, 4143-4148.
70. Witke, W., Schleicher, M. and Noegel, A. A. (1992). Redundancy in the microfilament system: Abnormal development of Dictyostelium cells lacking two F-actin crosslinking proteins. Cell 68, 53-62.
71. Yumura, S., Mori, H. and Fukui, Y. (1984). Localization of actin and myosin for the study of amoeboid movement in Dictyostelium using improved immunofluorescence. J. Cell Biol. 99, 894-899.