Calcium mobilization stimulates Dictyostelium discoideum shear-flow-induced cell motility

Journal of Cell Science

Volumn 118, Issue 15, 2005, Pages 3445-3457

  Fache, Sébastien ^a   Dalous, Jérémie ^a   Engelund, Mads ^b   Hansen, Christian ^b   Chamaraux, François ^a   Fourcade, Bertrand ^a   Satre, Michel ^a   Devreotes, Peter ^c   Bruckert, Franz ^a,d  

^a CEA GRENOBLE   (France)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Grenoble INP Phelma   (France)

Author keywords

Calcium; Dictyostelium discoideum; Heterotrimeric G proteins; Hydrodynamic flow; Mechanosensitivity; Motility

Indexed keywords

ACTIN; CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHELATING AGENT; CALCIUM ION; EGTAZIC ACID; GADOLINIUM; GLASS; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR;

ARTICLE; BETA CHAIN; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CELL ADHESION; CELL MEMBRANE; CELL MOTILITY; CELL MOTION; CELL SURFACE; CHEMOSENSITIVITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSKELETON; DICTYOSTELIUM DISCOIDEUM; EXTRACELLULAR CALCIUM; HYDRODYNAMICS; MUTANT; NONHUMAN; NULL CELL; PRIORITY JOURNAL; SHEAR FLOW; SHEAR STRESS; VELOCITY; WILD TYPE;

ACTINS; ANIMALS; CALCIUM; CELL ADHESION; CELL LINE; CYTOSKELETON; DICTYOSTELIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; EGTAZIC ACID; GADOLINIUM; GLASS; MEMBRANE FLUIDITY; MODELS, CHEMICAL; MOVEMENT; SENSITIVITY AND SPECIFICITY; SHEAR STRENGTH; SURFACE PROPERTIES; TIME FACTORS;

DICTYOSTELIUM DISCOIDEUM;

EID: 24344449173     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02461     Document Type: Article

References (48)

1. Bailly, M. and Condeelis, J. (2002). Cell motility: insights from the backstage. Nat. Cell Biol. 4, 292-294.
2. Borisy, G. G. and Svitkina, T. M. (2000). Actin machinery: pushing the envelope. Curr. Opin. Cell. Biol. 12, 104-112.
3. Carlier, M. F. and Pantaloni, D. (1997). Control of actin dynamics in cell motility. J. Mol. Biol. 269, 459-467.
4. Chadwick, C. M., Ellison, J. E. and Garrod, D. R. (1984). Dual role for Dictyostelium contact site B in phagocytosis and developmental size regulation. Nature 307, 646-647.
5. Clow, P. A. and McNally, J. G. (1999). In vivo observations of myosin II dynamics support a role in rear retraction. Mol. Biol. Cell 10, 1309-1323.
6. Coates, J. C. and Harwood, A. J. (2001). Cell-cell adhesion and signal transduction during Dictyostelium development. J. Cell Sci. 114, 4349-4358.
7. Cubitt, A. B. and Firtel, R. A. (1992). Characterization of phospholipase activity in Dictyostelium discoideum. Identification of a Ca(2+)-dependent polyphosphoinositide-specific phospholipase C. Biochem. J. 283, 371-378.
8. Décavé, E., Garrivier, D., Brechet, Y., Fourcade, B. and Bruckert, F. (2002). Shear-flow-induced detachment kinetics of Dictyostelium discoideum cells from solid substrate. Biophys. J. 82, 2383-2395.
9. Décavé, E., Rieu, D., Dalous, J., Fache, S., Brechet, Y., Fourcade, B., Satre, M. and Bruckert, F. (2003). Shear-flow-induced motility of Dictyostelium discoideum cells on solid substrate. J. Cell Sci. 116, 4331-4343.
10. DesMarais, V., Ichetovkin, I., Condeelis, J. and Hitchcock-DeGregori, S. E. (2002). Spatial regulation of actin dynamics: a tropomyosin-free, actin rich compartment at the leading edge. J. Cell Sci. 115, 4649-4660.
11. Devreotes, P. and Janetopoulos, C. (2003). Eukaryotic chemotaxis: distinctions between directional sensing and polarization. J. Biol. Chem. 278, 8.
12. Ditsch, A. and Wegner, A. (1995). Two low-affinity Ca(2+)-binding sites of gelsolin that regulate association with actin. Eur. J. Biochem. 229, 512-516.
13. Drayer, A. L., Van der Kaay, J., Mayr, G. W. and Van Haastert, P. J. (1994). Role of phospholipase C in Dictyostelium: formation of inositol 1,4,5-trisphosphate and normal development in cells lacking phospholipase C activity. EMBO J. 13, 1601-1609.
14. Friedl, P., Borgmann, S. and Brucker, E. B. (2001). Amoeboid leukocyte crawling through extracellular matrix: lessons from the Dictyostelium paradigm of cell movement. J. Leukocyte Biol. 70, 491-509.
15. Fukui, Y., Lynch, T. J., Brzeska, H. and Kom, E. D. (1989). Myosin I is located at the leading edges of locomoting Dictyostelium amoebae. Nature 341, 328-331.
16. Gasteier, J. E., Madrid, R., Krautkramer, E., Schroder, S., Muranyi, W., Benichou, S. and Fackler, O. T. (2003). Activation of the Rac-binding partner FHOD1 induces actin stress fibers via a ROCK-dependent mechanism. J. Biol. Chem. 278, 38902-38912.
17. Gebbie, L., Benghezal, M., Cornillon, S., Froquet, R., Cherix, N., Malbouyres, M., Leffir, Y., Grangeasse, C., Fache, S., Dalous, J. et al. (2004). Phg2, a kinase involved in adhesion and focal site modeling in Dictyostelium. Mol. Biol. Cell 15, 3915-3925.
18. Grimson, M. J., Coates, J. C., Reynolds, J. P., Shipman, M., Blanton, R. L. and Harwood, A. J. (2000). Adherens junctions and beta-catenin-mediated cell signalling in a non-metazoan organism. Nature 408, 727-731.
19. Kindzelskii, A. L. and Petty, H. R. (2003). Intracellular calcium waves accompany neutrophil polarization, formylmethionylleucylphenylalanine stimulation, and phagocytosis: a high speed microscopy study. J. Immunol. 170, 64-72.
20. Kinosian, H. J., Newman, J., Lincoln, B., Selden, L. A., Gershman, L. C. and Estes, J. E. (1998). Ca2+ regulation of gelsolin activity: binding and severing of F-actin. Biophys. J. 76, 3101-3139.
21. Knecht, D. A., Fuller, D. L. and Loomis, W. F. (1987). Surface glycoprotein, gp24, involved in early adhesion of Dictyostelium discoideum. Dev. Biol. 121, 277-283.
22. Krause, M., Dent, E. W., Bear, J. E., Loureiro, J. J. and Gertler, F. B. (2003). Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu. Rev. Cell Dev. Biol. 19, 541-564.
23. Lee, J., Ishihara, A., Oxford, G., Johnson, B. and Jacobson, K. (1999). Regulation of cell movement is mediated by stretch-activated calcium channels. Nature 400, 382-386.
24. Lilly, P., Wu, L., Welker, D. L. and Devreotes, P. N. (1993). A G protein beta-subunit is essential for Dictyostelium development. Genes Dev. 7, 986-995.
25. Lin, K. M., Wenegieme, E., Lu, P. J., Chen, C. S. and Yin, H. L. (1997). Gelsolin binding to phosphatidylinositol 4,5-bisphosphate is modulated by calcium and pH. J. Biol. Chem. 272, 50.
26. Mandeville, J. T., Ghosh, R. N. and Maxfield, F. R. (1995). Intracellular calcium levels correlate with speed and persistent forward motion in migrating neutrophils. Biophys. J. 68, 1207-1217.
27. Meili, R. and Firtel, R. A. (2003). Two poles and a compass. Cell 114, 153-156.
28. Nebl, T. and Fisher, P. R. (1997). Intracellular Ca2+ signals in Dictyostelium chemotaxis are mediated exclusively by Ca2+ influx. J. Cell Sci. 110, 2845-2853.
29. Nebl, T., Kotsifas, M., Schaap, P. and Fisher, P. R. (2002). Multiple signalling pathways connect chemoattractant receptors and calcium-channels in Dictyostelium. J. Muscle Res. Cell Motil. 23, 853-865.
30. Niewohner, J., Weber, L, Maniak, M., Muller-Taubenberger, A. and 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.
31. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
32. Riveline, D., Zamir, E., Balaban, N. Q., Schwarz, U. S., Ishizaki, T., Narumiya, S., Kam, Z., Geiger, B. and Bershadsky, A. D. (2001). Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDial-dependent and ROCK-independent mechanism. J. Cell Biol. 153, 1175-1186.
33. Rooney, E. K., Gross, J. D. and Satre, M. (1994). Characterisation of an intracellular Ca2+ pump in Dictyostelium. Cell Calcium 16, 509-522.
34. Sakisaka, T., Ituh, T., Miura, K. and Takenawa, T. (1997). Phosphatidylinositol 4,5-bisphosphate phosphatase regulates the rearrangement of actin filaments. Mol. Cell Biol. 17, 3841-3849.
35. Schaloske, R., Schlatterer, C. and Malchow, D. (2000). A Xestospongin C-sensitive Ca(2+) store is required for cAMP-induced Ca(2+) influx and cAMP oscillations in Dictyostelium. J. Biol. Chem. 275, 8404-8408.
36. Schlatterer, C. and Malchow, D. (1993). Intracellular Gunaosine-5′-O-(3-thiotriphosphate) blocks chemotactic motility of Dictyostelium discoideum amoebae. Cell Motil. Cytoskeleton 26, 298-307.
37. Traynor, D., Milne, J. L., Insall, R. H. and Kay, R. R. (2000). Ca(2+) signalling is not required for chemotaxis in Dictyostelium. EMBO J. 19, 4846-4854.
38. Tsien, R. Y. (1980). New calcium indicators with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19, 2396-2404.
39. Unterweger, N. and Schlatterer, C. (1995). Introduction of calcium buffers into the cytosol of Dictyostelium discoideum amoebae alters cell morphology and inhibits chemotaxis. Cell Calcium 17, 97-110.
40. Van Duijn, B. and Van Haastert, P. J. (1992). Independent control of locomotion and orientation during Dictyostelium discoideum chemotaxis. J. Cell Sci. 102, 763-768.
41. Verkhovsky, A. B., Svitkina, T. M. and Borisy, G. G. (1999). Self-polarization and directional motility of cytoplasm. Curr. Biol. 9, 11-20.
42. Watts, D. J. and Ashworth, J. M. (1970). Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem. J. 119, 171-174.
43. Welch, M. D. and Mullins, R. D. (2002). Cellular control of actin nucleation. Annu. Rev. Cell Dev. Biol. 18, 247-288.
44. Wolven, A. K., Belmont, L. D., Mahoney, N. M., Almo, S. C. and Drubin, A G. (2000). In vivo importance of actin nucleotide exchange catalyzed by profilin. J. Cell Biol. 150, 895-904.
45. Wong, E. F., Brar, S. K., Sesaki, H., Yang, C. and Siu, C. H. (1996). Molecular cloning and characterization of DdCAD-1, a Ca2+-dependent cell-cell adhesion molecule, in Dictyostelium discoideum. J. Biol. Chem. 271, 16399-16408.
46. Wu, L., Valkema, R., Van Haastert, P. J. and Devreotes, P. N. (1995). The G protein beta subunit is essential for multiple responses to chemoattractants in Dictyostelium. J. Cell Biol. 129, 1667-1675.
47. Xu, J., Wang, F., Van Keymeulen, A., Herzmark, P., Straight, A., Kelly, K., Takuwa, Y., Sugimoto, N., Mitchison, T. and Bourne, H. R. (2003). Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114, 201-214.
48. Yumura, S., Furuya, K. and Takeuchi, I. (1996). Intracellular free calcium responses during chemotaxis of Dictyostelium cells. J. Cell Sci. 109, 2673-2678.