Shear flow-induced motility of Dictyostelium discoideum cells on solid substrate

Journal of Cell Science

Volumn 116, Issue 21, 2003, Pages 4331-4343

  Décavé, Emmanuel ^a   Rieu, Didier ^a   Dalous, Jérémie ^a   Fache, Sébastien ^a   Bréchet, Yves ^b   Fourcade, Bertrand ^a   Satre, Michel ^a   Bruckert, Franz ^a  

^a CEA GRENOBLE   (France)

^b UNIV GRENOBLE ALPES   (France)

Author keywords

Dictyostelium discoideum; Hydrodynamic flow; Mechanosensitivity; Motility

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ACTIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE;

ACTIN POLYMERIZATION; ARTICLE; CELL CONTACT; CELL MOTILITY; CELL POLARITY; CHEMOTAXIS; CONTROLLED STUDY; CYTOSKELETON; DICTYOSTELIUM DISCOIDEUM; ENZYME INHIBITION; HYDRODYNAMICS; KINEMATICS; NONHUMAN; PRIORITY JOURNAL; PSEUDOPODIUM; SHEAR FLOW; SHEAR STRESS; SIGNAL TRANSDUCTION; VELOCITY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTINS; ANIMALS; CELL ADHESION; CHEMOTAXIS; CHROMONES; CYTOSKELETON; DICTYOSTELIUM; ENZYME INHIBITORS; MORPHOLINES; PHOSPHATIDYLINOSITOLS; SHEAR STRENGTH; SIGNAL TRANSDUCTION;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; PROTOZOA;

EID: 0242635813     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00726     Document Type: Article

References (48)

1. Asthagiri, A. R. and Lauffenburger, D. A. (2000). Bioengineering models of cell signaling. Annu. Rev. Biomed. Eng. 2, 31-53.
2. Bereiter-Hahn, J. and Vesely, P. (1995). Reflection interference microscopy. In Cell Biology, A Laboratory Handbook, Vol. 3 (ed. J. Celis), pp. 54-63. Academic Press.
3. Buczynski, G., Grove, B., Nomura, A., Kleve, M., Bush, J., Firtel, R. A. and Cardelli, J. (1997). Inactivation of two Dictyostelium discoideum genes, DdPIK1 and DdPIK2, encoding proteins related to mammalian phosphatidylinositide 3-kinases, results in defects in endocytosis, lysosome to postlysosome transport, and actin cytoskeleton organization. J. Cell Biol. 136, 1271-1286.
4. Cantley, L. C. and Neel, B. G. (1999). New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc. Natl. Acad. Sci. USA 96, 4240-4245.
5. Chappell, D. C., Varner, S. E., Nerem, R. M., Medford, R. M. and Alexander, R. W. (1998). Oscillatory shear stress stimulates adhesion molecule expression in cultured human endothelium. Circ. Res. 82, 532-539.
6. Choquet, D., Felsenfeld, D. P. and Sheetz, M. P. (1997). Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88, 39-48.
7. Chung, C. Y. and Firtel, R. A. (1999). PAKa, a putative PAK family member, is required for cytokinesis and the regulation of the cytoskeleton in Dictyostelium discoideum cells during chemotaxis. J. Cell Biol. 147, 559-576.
8. Chung, C. Y., Lee, S., Briscoe, C., Ellsworth, C. and Firtel, R. A. (2000). Role of Rac in controlling the actin cytoskeleton and chemotaxis in motile cells. Proc. Natl. Acad. Sci. USA 97, 5225-5230.
9. Chung, C. Y., Funamoto, S. and Firtel, R. A. (2001). Signaling pathways controlling cell polarity and chemotaxis. Trends Biochem. Sci. 26, 557-566.
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. Cytoskeleton 10, 77-90.
11. Cornillon, S., Pech, E., Benghezal, M., Ravanel, K., Gaynor, E., Letourneur, F., Bruckert, F. and Cosson, P. (2000). Phg1p is a nine-transmembrane protein superfamily member involved in Dictyostelium adhesion and phagocytosis. J. Biol. Chem. 275, 34287-34292.
12. Decave, E., Garrivier, D., Brechet, Y., Bruckert, F. and Fourcade, B. (2002a). Peeling process in living cell movement under shear flow. Phys. Rev. Lett. 89, 108101.
13. Decave, E., Garrivier, D., Brechet, Y., Fourcade, B. and Bruckert, F. (2002b). Shear flow-induced detachment kinetics of Dictyostelium discoideum cells from solid substrate. Biophys. J. 82, 2383-2395.
14. Devreotes, P. N. and Zigmond, S. H. (1988). Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu. Rev. Cell. Biol. 4, 649-686.
15. Fukui, Y., Uyeda, T. Q., Kitayama, C. and Inoue, S. (2000). How well can an amoeba climb? Proc. Natl. Acad. Sci. USA 97, 10020-10025.
16. Funamoto, S., MeiIi, R., Lee, S., Parry, L. and Firtel, R. A. (2002). Spatial and temporal regulation of 3-phosphomositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 109, 611-623.
17. Garrivier, D., Decave, E., Brechet, Y., Bruckert, F. and Foureade, B. (2002). Peeling model for cell detachment. Eur. Phys. J. E 8, 79-97.
18. Hamasaki, T., Goto, S., Nishikawa, S. and Ushio, Y. (2001). A role of netrin-1 in the formation of the subcortical structure striatum: repulsive action on the migration of late-born striatal neurons. J. Neurosci. 21, 4272-4280.
19. Hamill, O. P. and Martinac, B. (2001). Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81, 685-740.
20. Hannigan, M., Zhan, L., Li, Z., Ai, Y., Wu, D. and Huang, C. K. (2002). Neutrophils lacking phosphoinositide 3-kinase γ show loss of directionality during N-formyl-Met-Leu-Phe-induced chemotaxis. Proc. Natl. Acad. Sci. USA 99, 3603-3608.
21. Iijima, M. and Devreotes, P. (2002). Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 109, 599-610.
22. Iijima, M., Huang, Y. E. and Devreotes, P. (2002). Temporal and spatial regulation of chemotaxis. Dev. Cell 3, 469-478.
23. Ingber, D. E. (1997). Tensegrity: the architectural basis of cellular mechanotransduction. Annu. Rev. Physiol. 59, 575-599.
24. Jay, P. Y., Pham, P. A., Wong, S. A. and Elson, E. L. (1995). A mechanical function of myosin II in cell motility. J. Cell Sci. 108, 393-397.
25. Kay, R. R. (2002). Chemotaxis and cell differentiation in Dictyostelium. Curr. Opin. Microbial. 5, 575-579.
26. Killirch, T., Path, P. J., Xiang, W., Bultmann, H., Rensing, L. and Vicker, M. G. (1993). The locomotion, shape and pseudopodial dynamics of unstimulated Dictyostelium cells are not random. J. Cell Sci. 106, 1005-1013.
27. Knecht, D. A. and Shelden, E. (1995). Three-dimensional localization of wild-type and myosin II mutant cells during morphogenesis of Dictyostelium. Dev. Biol. 170, 434-444.
28. Nerem, R. M., Alexander, R. W., Chappell, D. C., Medford, R. M., Varner, S. E. and Taylor, W. R. (1998). The study of the influence of flow on vascular endothelial biology. Am. J. Med. Sci. 316, 169-175.
29. Newell, P. C. (1995). Signal transduction and motility of Dictyostelium. Biosci. Rep. 15, 445-462.
30. Oliver, J. M., Krawiec, J. A. and Berlin, R. D. (1978). A carbamate herbicide causes microtubule and microfilament disruption and nuclear fragmentation in fibroblasts. Exp. Cell. Res. 116, 229-237.
31. Parent, C. A., Blacklock, B. J., Froehlich, W. M., Murphy, D. B. and Devreotes, P. N. (1998). G protein signaling events are activated at the leading edge of chemotactic cells. Cell 95, 81-91.
32. Rickert, P., Weiner, O. D., Wang, F., Bourne, H. R. and Servant, G. (2000). Leukocytes navigate by compass: roles of PI3Kγ and its lipid products. Trends Cell Biol. 10, 466-473.
33. 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 mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153, 1175-1186.
34. Rupper, A. C., Rodriguez-Paris, J. M., Grove, B. D. and Cardelli, J. A. (2001). p110-related PI 3-kinases regulate phagosome-phagosome fusion and phagosomal pH through a PKB/Akt dependent pathway in Dictyostelium. J. Cell Sci. 114, 1283-1295.
35. Sawada, Y. and Sheetz, M. P. (2002). Force transduction by Triton cytoskeletons. J. Cell Biol. 156, 609-615.
36. Shelden, E. and Knecht, D. A. (1995). Mutants lacking myosin II cannot resist forces generated during multicellular morphogenesis. J. Cell Sci. 108, 1105-1115.
37. Simson, R., Wallraff, E., Faix, J., Niewohner, J., Gerisch, G. and Sackmann, E. (1998). Membrane bending modulus and adhesion energy of wild-type and mutant cells of Dictyostelium lacking talin or cortexillins. Biophys. J. 74, 514-522.
38. Tessier-Lavigne, M. and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
39. Theriot, J. A. and Mitchison, T. J. (1991). Actin microfilament dynamics in locomoting cells. Nature 352, 126-131.
40. Verkhovsky, A. B., Svitkina, T. M. and Borisy, G. G. (1999). Self-polarization and directional motility of cytoplasm. Curr. Biol. 9, 11-20.
41. Vicker, M. G. (1994). The regulation of chemotaxis and chemokinesis in Dictyostelium amoebae by temporal signals and spatial gradients of cyclic AMP. J. Cell Sci. 107, 659-667.
42. Vlahos, C. J., Matter, W. F., Hui, K. Y. and Brown, R. F. (1994). A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248.
43. 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.
44. 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.
45. Weijer, C. J. (1999). Morphogenetic cell movement in Dictyostelium. Semin. Cell. Dev. Biol. 10, 609-619.
46. Weiner, O. D. (2002). Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr. Opin. Cell Biol. 14, 196-202.
47. Zamir, E. and Geiger, B. (2001). Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci. 114, 3583-3590.
48. Zhou, K., Takegawa, K., Emr, S. D. and Firtel, R. A. (1995). A phosphatidylinositol (PI) kinase gene family in Dictyostelium discoideum: biological roles of putative mammalian p110 and yeast Vps34p PI 3-kinase homologs during growth and development. Mol. Cell. Biol. 15, 5645-5656.