The exocytic gene secA is required for Dictyostelium cell motility and osmoregulation

Journal of Cell Science

Volumn 123, Issue 19, 2010, Pages 3226-3234

  Zanchi, Roberto ^a   Howard, Gillian ^a   Bretscher, Mark S ^a   Kay, Robert R ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

cAMP relay; Cell motility; Contractile vacuole; Dictyostelium; Exocytosis; SecA

Indexed keywords

CYCLIC AMP;

ACTIN POLYMERIZATION; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; ELECTRON MICROSCOPY; EXOCYTOSIS; GENE; NONHUMAN; OSMOREGULATION; PRIORITY JOURNAL; SECA GENE; SIGNAL TRANSDUCTION; TEMPERATURE SENSITIVE MUTANT;

ACTINS; CELL MEMBRANE; CELL MOVEMENT; CYCLIC AMP; DICTYOSTELIUM; EXOCYTOSIS; MICROSCOPY, ELECTRON; MUNC18 PROTEINS; MUTANT PROTEINS; OSMOSIS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; PSEUDOPODIA; TEMPERATURE;

DICTYOSTELIUM;

EID: 77956936926     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.072876     Document Type: Article

References (58)

1. Aguado-Velasco, C. and Bretscher, M. S. (1999). Circulation of the plasma membrane in Dictyostelium. Mol. Biol. Cell 10, 4419-4427.
2. Bagorda, A., Das, S., Rericha, E. C., Chen, D., Davidson, J. and Parent, C. A. (2009). Real-time measurements of cAMP production in live Dictyostelium cells. J. Cell Sci. 122, 3907-3914.
3. Betz, W. J., Mao, F. and Smith, C. B. (1996). Imaging exocytosis and endocytosis. Curr. Opin. Neurobiol. 6, 365-371.
4. Bloomfield, G., Tanaka, Y., Skelton, J., Ivens, A. and Kay, R. R. (2008). Widespread duplications in the genomes of laboratory stocks of Dictyostelium discoideum. Genome Biol. 9, R75.
5. Bretscher, M. S. (1984). Endocytosis: relation to capping and cell locomotion. Science 224, 681-686.
6. Bretscher, M. S. (1996). Getting membrane flow and the cytoskeleton to cooperate in moving cells. Cell 87, 601-606.
7. Bretscher, M. S. and Clotworthy, M. (2007). Using single loxP sites to enhance homologous recombination: ts mutants in Sec1 of Dictyostelium discoideum. PLoS ONE 2, e724.
8. Carr, C. M., Grote, E., Munson, M., Hughson, F. M. and Novick, P. J. (1999). Sec1p binds to SNARE complexes and concentrates at sites of secretion. J. Cell Biol. 146, 333-344. (Pubitemid 29369771)
9. Dormann, D., Libotte, T., Weijer, C. J. and Bretschneider, T. (2002). Simultaneous quantification of cell motility and protein-membrane-association using active contours. Cell Motil. Cytoskeleton 52, 221-230.
10. Du, F., Edwards, K., Shen, Z., Sun, B., De Lozanne, A., Briggs, S. and Firtel, R. A. (2008). Regulation of contractile vacuole formation and activity in Dictyostelium. EMBO J. 27, 2064-2076.
11. Gabriel, D., Hacker, U., Kohler, J., Muller-Taubenberger, A., Schwartz, J. M., Westphal, M. and Gerisch, G. (1999). The contractile vacuole network of Dictyostelium as a distinct organelle: its dynamics visualized by a GFP marker protein. J. Cell Sci. 112, 3995-4005.
12. Gauthier, N. C., Rossier, O. M., Mathur, A., Hone, J. C. and Sheetz, M. P. (2009). Plasma membrane area increases with spread area by exocytosis of a GPI-anchored protein compartment. Mol. Biol. Cell 20, 3261-3272.
13. Gerisch, G., Heuser, J. and Clarke, M. (2002). Tubular-vesicular transformation in the contractile vacuole system of Dictyostelium. Cell Biol. Int. 26, 845-852. (Pubitemid 35366116)
14. Gerisch, G., Benjak, A., Kohler, J., Weber, I. and Schneider, N. (2004). GFP-golvesin constructs to study Golgi tubulation and post-Golgi vesicle dynamics in phagocytosis. Eur. J. Cell Biol. 83, 297-303.
15. Grote, E., Carr, C. M. and Novick, P. J. (2000). Ordering the final events in yeast exocytosis. J. Cell Biol. 151, 439-452.
16. Hallett, M. B. and Dewitt, S. (2007). Ironing out the wrinkles of neutrophil phagocytosis: membrane reservoirs for surface area expansion. Trends Cell Biol. 17, 209-214.
17. Heuser, J. (2006). Evidence for recycling of contractile vacuole membrane during osmoregulation in Dictyostelium amoebae-a tribute to Gunther Gerisch. Eur. J. Cell Biol. 85, 859-871.
18. Hicke, L., Zanolari, B., Pypaert, M., Rohrer, J. and Riezman, H. (1997). Transport through the yeast endocytic pathway occurs through morphologically distinct compartments and requires an active secretory pathway and Sec18p/N-ethylmaleimide-sensitive fusion protein. Mol. Biol. Cell 8, 13-31. (Pubitemid 27294794)
19. Hoeller, O. and Kay, R. R. (2007). Chemotaxis in the absence of PIP3 gradients. Curr. Biol. 17, 813-817.
20. Jenne, N., Rauchenberger, R., Hacker, U., Kast, T. and Maniak, M. (1998). Targeted gene disruption reveals a role for vacuolin B in the late endocytic pathway and exocytosis. J. Cell Sci. 111, 61-70.
21. Jungbluth, A., Vonarnim, V., Biegelmann, E., Humbel, B., Schweiger, A. and Gerisch, G. (1994). Strong increase in the tyrosine phosphorylation of actin upon inhibition of oxidative phosphorylation-correlation with reversible rearrangements in the actin skeleton of Dictyostelium cells. J. Cell Sci. 107, 117-125. (Pubitemid 24039039)
22. Kay, R. R. (1987). Cell differentiation in monolayers and the investigation of slime mold morphogens. Methods Cell Biol. 28, 433-448.
23. Kay, R. R., Langridge, P., Traynor, D. and Hoeller, O. (2008). Changing directions in the study of chemotaxis. Nat. Rev. Mol. Cell Biol. 9, 455-463.
24. King, J. S. and Insall, R. H. (2009). Chemotaxis: finding the way forward with Dictyostelium. Trends Cell Biol. 19, 523-530.
25. Knecht, D. and Pang, K. M. (1995). Electroporation of Dictyostelium discoideum. Methods Mol. Biol. 47, 321-330.
26. Kriebel, P. W., Barr, V. A. and Parent, C. A. (2003). Adenylyl cyclase localization regulates streaming during chemotaxis. Cell 112, 549-560.
27. Laevsky, G. and Knecht, D. A. (2001). Under-agarose folate chemotaxis of Dictyostelium discoideum amoebae in permissive and mechanically inhibited conditions. Biotechniques 31, 1140-1149.
28. Lammermann, T., Bader, B. L., Monkley, S. J., Worbs, T., Wedlich-Soldner, R., Hirsch, K., Keller, M., Forster, R., Critchley, D. R., Fassler, R. et al. (2008). Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453, 51-55.
29. Langridge, P. D. and Kay, R. R. (2006). Blebbing of Dictyostelium cells in response to chemoattractant. Exp. Cell Res. 312, 2009-2017.
30. Langridge, P. D. and Kay, R. R. (2007). Mutants in the Dictyostelium Arp2/3 complex and chemoattractant-induced actin polymerization. Exp. Cell Res. 313, 2563-2574.
31. Lawson, M. A. and Maxfield, F. R. (1995). Ca(2+)- and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature 377, 75-79.
32. Maeda, Y. and Gerisch, G. (1977). Vesicle formation in Dictyostelium discoideum cells during oscillations of cAMP synthesis and release. Exp. Cell Res. 110, 119-126. (Pubitemid 8243341)
33. Malhotra, V., Orci, L., Glick, B. S., Block, M. R. and Rothman, J. E. (1988). Role of an N-ethylmaleimide-sensitive transport component in promoting fusion of transport vesicles with cisternae of the Golgi stack. Cell 54, 221-227.
34. Manstein, D. J., Schuster, H. P., Morandini, P. and Hunt, D. M. (1995). Cloning vectors for the production of proteins in Dictyostelium discoideum. Gene 162, 129-134.
35. Mohandas, N. and Evans, E. (1994). Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Annu. Rev. Biophys. Biomol. Struct. 23, 787-818.
36. Muller-Taubenberger, A., Lupas, A. N., Li, H. W., Ecke, M., Simmeth, E. and Gerisch, G. (2001). Calreticulin and calnexin in the endoplasmic reticulum are important for phagocytosis. EMBO J. 20, 6772-6782. (Pubitemid 33134207)
37. Noegel, A. A. and Schleicher, M. (2000). The actin cytoskeleton of Dictyostelium: a story told by mutants. J. Cell Sci. 113, 759-766.
38. Novick, P., Field, C. and Schekman, R. (1980). Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21, 205-215.
39. Pang, K. M., Lee, E. and 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.
40. Quiviger, B., de Chastellier, C. and Ryter, A. (1978). Cytochemical demonstration of alkaline phosphatase in the contractile vacuole of Dictyostelium discoideum. J. Ultrastruct. Res. 62, 228-236. (Pubitemid 8360149)
41. Raucher, D. and Sheetz, M. P. (2000). Cell spreading and lamellipodial extension rate is regulated by membrane tension. J. Cell Biol. 148, 127-136. (Pubitemid 30046787)
42. Ryter, A. and de Chastellier, C. (1977). Morphometric and cytochemical studies of Dictyostelium discoideum in vegetative phase. Digestive system and membrane turnover. J. Cell Biol. 75, 200-217.
43. Schneider, N., Schwartz, J. M., Kohler, J., Becker, M., Schwarz, H. and Gerisch, G. (2000). Golvesin-GFP fusions as distinct markers for Golgi and post-Golgi vesicles in Dictyostelium cells. Biol. Cell 92, 495-511.
44. Schoen, C. D., Arents, J. C., Bruin, T. and Van Driel, R. (1989). Intracellular localization of secretable cAMP in relaying Dictyostelium discoideum cells. Exp. Cell Res. 181, 51-62. (Pubitemid 19072790)
45. Shaffer, B. M. (1975). Secretion of cyclic AMP induced by cyclic AMP in the cellular slime mould Dictyostelium discoideum. Nature 255, 549-552.
46. Shen, J., Tareste, D. C., Paumet, F., Rothman, J. E. and Melia, T. J. (2007). Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 128, 183-195.
47. Sudhof, T. C. and Rothman, J. E. (2009). Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477.
48. Swaney, K. F., Huang, C. H. and Devreotes, P. N. (2010). Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu. Rev. Biophys. 39, 265-289.
49. Thompson, C. R. L. and Kay, R. R. (2000). Cell-fate choice in Dictyostelium: intrinsic biases modulate sensitivity to DIF signaling. Dev. Biol. 227, 56-64.
50. Thompson, C. R. L. and Bretscher, M. S. (2002). Cell polarity and locomotion, as well as endocytosis, depend on NSF. Development 129, 4185-4192.
51. Traynor, D. and Kay, R. R. (2007). Possible roles of the endocytic cycle in cell motility. J. Cell Sci. 120, 2318-2327.
52. 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.
53. Valdez-Taubas, J. and Pelham, H. R. (2003). Slow diffusion of proteins in the yeast plasma membrane allows polarity to be maintained by endocytic cycling. Curr. Biol. 13, 1636-1640.
54. Van Haastert, P. J. M. and Devreotes, P. N. (2004). Chemotaxis: signalling the way forward. Nat. Rev. Mol. Cell Biol. 5, 626-634.
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., Voss, E., Von, B. N., Burns, R., Stites, J. and Soll, D. R. (1998). A computer-assisted system for reconstructing and interpreting the dynamic three-dimensional relationships of the outer surface, nucleus and pseudopods of crawling cells. Cell. Motil. Cytoskeleton 41, 225-246.
57. Xiao, Z., Zhang, N., Murphy, D. B. and Devreotes, P. N. (1997). Dynamic distribution of chemoattractant receptors in living cells during chemotaxis and persistent stimulation. J. Cell Biol. 139, 365-374.
58. Yoshida, K. and 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.