Drainin required for membrane fusion of the contractile vacuole in Dictyostelium is the prototype of a protein family also represented in man

EMBO Journal

Volumn 18, Issue 12, 1999, Pages 3305-3316

  Becker, Michael ^a   Matzner, Monika ^a   Gerisch, Günther ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Functional genomics; Green fluorescent protein; Membrane fusion; Osmoregulation; Restriction enzyme mediated insertion

Indexed keywords

CELL MEMBRANE PROTEIN; DRAININ; GREEN FLUORESCENT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL SURVIVAL; CELL VACUOLE; CELL VOLUME; CHANNEL GATING; CONTROLLED STUDY; DICTYOSTELIUM; ENDOCYTOSIS; GENE DISRUPTION; HYDROPHOBICITY; MEMBRANE FUSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOREGULATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CELL SURVIVAL; CLONING, MOLECULAR; DICTYOSTELIUM; ENDOCYTOSIS; ENDOSOMES; GENE DELETION; GENETIC COMPLEMENTATION TEST; HUMANS; INTRACELLULAR MEMBRANES; MEMBRANE FUSION; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; OSMOTIC PRESSURE; PHENOTYPE; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; VACUOLES; WATER;

EID: 0033564209     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.12.3305     Document Type: Article

References (66)

1. Allen, C.A. and Green, D.P.L. (1997) The mammalian acrosome reaction: gateway to sperm fusion with the oocyte? BioEssays, 19, 241-247.
2. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
3. Bennett, M.K. (1995) SNAREs and the specificity of transport vesicle targeting. Curr. Opin. Cell Biol., 7, 581-586.
4. +-ATPases in reticular membranes of the contractile vacuole complex and in lysosomes. J. Cell Sci., 107, 2801-2812.
5. Bush, J., Temesvari, L., Rodriguez-Paris, J., Buczynski, G. and Cardelli, J. (1996) A role for a Rab4-like GTPase in endocytosis and in regulation of contractile vacuole structure and function in Dictyostelium discoideum. Mol. Biol. Cell, 7, 1623-1638.
6. 2+/GTP sensor in exocytotic secretion. Proc. Natl Acad. Sci. USA, 93, 10797-10802.
7. Cardelli, J.A., Richardson, J. and Miears, D. (1989) Role of acidic intracellular compartments in the biosynthesis of Dictyostelium lysosomal enzymes. The weak bases ammonium chloride and chloroquine differentially affect proteolytic processing and sorting. J. Biol. Chem., 264, 3454-3463.
8. Clarke, M. and Heuser, J. (1997) Water and ion transport. In Maeda, Y., Inouye, K. and Takeuchi, I. (eds), Dictyostelium. A Model System for Cell and Developmental Biology. Frontiers Science No. 21. Universal Academy Press, Inc., Tokyo, Japan, pp. 75-91.
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. Doberstein, S.K., Baines, I.C., Wiegand, G., Korn, E.D. and Pollard, T.D. (1993) Inhibition of contractile vacuole function in vivo by antibodies against myosin I. Nature, 365, 841-843.
11. Doflein, F., and Reichenow, E. (1953) Allgemeine Morphologie und Physiologie der Protozoen. In Doflein, F. and Reichenow, E. (eds), Lehrburch der Protozoenkunde. VEB Gustav Fischer Verlag, Jena, Germany, p. 13.
12. Emans, N., Gorvel, J.P., Walter, C., Gerke, V., Kellner, R., Griffiths, G. and Gruenberg, J. (1993) Annexin II is a major component of fusogenic endosomal vesicles. J. Cell Biol., 120, 1357-1369.
13. Franke, W.W., Krien, S. and Brown, R.M., Jr (1969) Simultaneous glutaraldehyde-osmium tetroxide fixation with postosmication, Histochemie, 19, 162-164.
14. Franke, W.W., Luder, M.R., Kartenbeck, J., Zerban, H. and Keenan, T.W. (1976) Involvement of vesicle coat material in casein secretion and surface regeneration. J. Cell Biol., 69, 173-195.
15. Franke, W.W., Grund, C., Schmid, E. and Mandelkow, E. (1978) Paracrystalline arrays of membrane-to-membrane cross bridges associated with the inner surface of plasma membrane. J. Cell Biol., 77, 323-328.
16. Furuichi, K., Ra, C. Isersky, C. and Rivera, J. (1986) Comparative evaluation of the effect of pharmacological agents on endocytosis and coendocytosis of IgE by rat basophilic leukaemia cells. Immunology, 58, 105-110.
17. Geppert, M. and Südhof, T.C. (1998) RAB3 and synaptotagmin: the yin and yang of synaptic membrane fusion. Annu. Rev. Neurosci., 21, 75-95.
18. Gerisch, G., Hagmann, J., Hirth, P., Rossier, C., Weinhart, U. and Westphal, M. (1985) Early Dictyostelium development: control mechanisms bypassed by sequential mutagenesis. Cold Spring Harbor Symp. Quant. Biol., 50, 813-822.
19. Giglione, C. and Gross, J.D. (1995) Anion effects on vesicle acidification in Dictyostelium. Biochem. Mol. Biol. Int., 36, 1057-1065.
20. Gingell, D., Todd, I. and Owens, N. (1982) Interaction between intracellular vacuoles and the cell surface analysed by finite aperture theory interference reflection microscopy. J. Cell Sci., 54, 287-298.
21. Griffiths, G. (ed.) (1993) Fine Structure Immunocytochemistry. Springer Verlag, Berlin, Germany.
22. Hacker, U., Albrecht, R. and Maniak, M. (1997) Fluid-phase uptake by macropinocytosis in Dictyostelium. J. Cell Sci., 110, 105-112.
23. Hammer, J., Lydan, M. and Jung, G. (1996) Dictyostelium MyoJ associates with membranes of the contractile vacuole complex. Mol. Biol. Cell, 7, 374a, abstract 2174.
24. Hanakam, F., Albrecht, R., Eckerskorn, C., Matzner, M. and Gerisch, G. (1996) Myristoylated and non-myristoylated forms of the pH sensor protein hisactophilin II: intracellular shuttling to plasma membrane and nucleus monitored in real time by a fusion with green fluorescent protein. EMBO J., 15, 2935-2943.
25. Hanson, P.I., Heuser, J.E. and Jahn, R. (1997) Neurotransmitter release - four years of SNARE complexes. Curr. Opin. Neurobiol., 7, 310-315.
26. Heuser, J., Zhu, Q. and Clarke, M. (1993) Proton pumps populate the contractile vacuoles of Dictyostelium amoebae. J. Cell Biol., 121, 1311-1327.
27. Howard, P.K., Ahern, K.G. and Firtel, R.A. (1988) Establishment of a transient expression system for Dictyostelium discoideum. Nucleic Acids Res., 16, 2613-2623.
28. Hughson, F.M. (1997) Enveloped viruses: a common mode of membrane fusion? Curr. Biol., 7, R565-R569.
29. Humbel, B.M. and Biegelmann, E. (1992) A preparation protocol for postembedding immunoelectron microscopy of Dictyostelium discoideum cells with monoclonal antibodies. Scanning Microsc., 6, 817-825.
30. 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.
31. Jung, G., Wu, X. and Hammer, J.A., III (1996) Dictyostelium mutants lacking multiple classic myosin I isoforms reveal combinations of shared and distinct functions. J. Cell Biol., 133, 305-323.
32. Klein, G. and Satre, M. (1986) Kinetics of fluid-phase pinocytosis in Dictyostelium discoideum amoebae. Biochem. Biophys. Res. Commun., 138, 1146-1152.
33. Kuspa, A. and Loomis, W.F. (1992) Tagging developmental genes in Dictyostelium discoideum by restriction enzyme-mediated integration of plasmid DNA. Proc. Natl Acad. Sci. USA, 89, 8803-8807.
34. Linder, J.C. and Staehelin, L.A. (1979) A novel model for fluid secretion by the trypanosomatid contractile vacuole apparatus. J. Cell Biol., 83, 371-382.
35. Liu, T. and Clarke, M. (1996) The vacuolar proton pump of Dictyostelium discoideum: molecular cloning and analysis of the 100 kDa subunit. J. Cell Sci., 109, 1041-1051.
36. 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.
37. Mehdy, M.C., Ratner, D. and Firtel, R.A. (1983) Induction and modulation of cell-type-specific gene expression in Dictyostelium. Cell, 32, 763-771.
38. 2+ ATPase PAT1 and the contractile vacuole in calcium regulation in Dictyostelium discoideum. J. Cell Sci., 112, 405-414.
39. Muallem, S., Kwiatkowska, K., Xu, X. and Yin, H.L. (1995) Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J. Cell Biol., 128, 589-598.
40. Nagase, T., Ishikawa, K., Miyajima, N., Tanaka, A., Kotani, H., Nomura, N. and Ohara, O. (1998) Prediction of the coding sequences of unidentified human genes. IX. The complete sequences of 100 new cDNA clones from brain which can code for large proteins in vitro. DNA Res., 5, 31-39.
41. Noegel, A., Welker, D.L., Metz, B.A. and Williams, K.L. (1985) Presence of nuclear associated plasmids in the lower eukaryote Dictyostelium discoideum. J. Mol. Biol., 185, 447-450.
42. Nolta, K.V. and Steck, T.L. (1994) Isolation and initial characterization of the bipartite contractile vacuole complex from Dictyostelium discoideum. J. Biol. Chem., 269, 2225-2233.
43. Nolta, K.V., Rodriguez-Paris, J.M. and Steck, T.L. (1994) Analysis of successive endocytic compartments isolated from Dictyostelium discoideum by magnetic fractionation. Biochim. Biophys. Acta, 1224, 237-246.
44. Novak, K.D., Peterson, M.D., Reedy, M.C. and Titus, M.A. (1995) Dictyostelium myosin I double mutants exhibit conditional defects in pinocytosis. J. Cell Biol., 131, 1205-1221.
45. Ochman, H., Gerber, A.S. and Hartl, D.L. (1988) Genetic application of an inverse polymerase chain reaction. Genetics, 120, 621-623.
46. O'Halloran, T.J. and Anderson, R.G.W. (1992) Clathrin heavy chain is required for pinocytosis, the presence of large vacuoles, and development in Dictyostelium. J. Cell Biol., 118, 1371-1377.
47. Prasher, D.C., Eckenrode, V.K., Ward, W.W., Prendergast, F.G. and Cormier, M.J. (1992) Primary structure of the Aequorea victoria green fluorescent protein. Gene, 111, 229-233.
48. Rauchenberger, R., Hacker, U., Murphy, J., Niewöhner, J. and Maniak, M. (1997) Coronin and vacuolin identify consecutive stages of a late, actin-coated endocytic compartment in Dictyostelium. Curr. Biol., 7, 215-218.
49. Rivero, F., Köppel, B., Peracino, B., Bozzaro, S., Siegert, F., Weijer, C.J., Schleicher, M., Albrecht, R. and Noegel, A.A. (1996) 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. J. Cell Sci., 109, 2679-2691
50. Rothman, J.E. (1994) Intracellular membrane fusion. Adv. Second Messenger Phosphoprotein Res., 29, 81-96.
51. Rybin, V., Ullrich, O., Rubino, M., Alexandrov, K., Simon, I., Seabra, M.C., Goody, R. and Zerial, M. (1996) GTPase activity of Rab5 acts as a timer for endocytic membrane fusion. Nature, 383, 266-269.
52. Sato, K. and Wickner, W. (1998) Functional reconstitution of ypt7p GTPase and a purified vacuole SNARE complex. Science, 281, 700-702.
53. Schiavo, G., Gmachl, M.J.S., Stenbeck, G., Söllner, T.H. and Rothman, J.E. (1995) A possible docking and fusion particle for synaptic transmission. Nature, 378, 733-736.
54. Schuster, S.C., Noegel, A.A., Oehme, F., Gerisch, G. and Simon, M.I. (1996) The hybrid histidine kinase DokA is part of the osmotic response system of Dictyostelium. EMBO J., 15, 3880-3889.
55. Skehel, J.J. and Wiley, D.C. (1998) Coiled coils in both intracellular vesicle and viral membrane fusion. Cell, 95, 871-874.
56. Sutoh, K. (1993) A transformation vector for Dictyostelium discoideum with a new selectable marker bsr. Plasmid, 30, 150-154.
57. Temesvari, L.A., Bush, J.M., Peterson, M.D., Novak, K.D., Titus, M.A. and Cardelli, J.A. (1996) Examination of the endosomal and lysosomal pathways in Dictyostelium discoideum myosin I mutants. J Cell Sci., 109, 663-673.
58. Tokuyasu, K.T. (1989) Use of poly(vinylpyrrolidone) and poly(vinylalcohol) for cryoultramicrotomy. Histochem. J., 21, 163-171.
59. Umbach, J.A., Mastrogiacomo, A. and Gundersen, C.B. (1995) Cystein string proteins and presynaptic function. J. Physiol., 89, 95-101.
60. Weber, T., Zemelman, B.V., McNew, J.A., Westermann, B., Gmachl, M., Parlati, F., Söllner, T.H. and Rothman, J.E. (1998) SNAREpins: minimal machinery for membrane fusion. Cell, 92, 759-772.
61. Westphal, M., Jungbluth, A., Heidecker, M., Mühlbauer, B., Heizer, C., Schwartz, J.-M., Marriott, G. and Gerisch, G. (1997) Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein. Curr. Biol., 7, 176-183.
62. Wilson, R. et al. (1994) 2.2 Mb of contiguous nucleotide sequence from chromosome III of C.elegans. Nature, 368, 32-38.
63. Xu, Z., Sato, K. and Wickner, W. (1998) LMA1 binds to vacuoles at Sec18p (NSF), transfers upon ATP hydrolysis to a t-SNARE (Vam3p) complex, and is released during fusion. Cell, 93, 1125-1134.
64. Yumura, S., Mori, H. and Fukui, Y. (1984) Localization of actin and myosin for the study of ameboid movement in Dictyostelium using improved immunofluorescence. J. Cell Biol., 99, 894-899.
65. Zhang, L., Marcu, M.G., Nau-Staudt, K. and Trifaro, J.-M. (1996) Recombinant scinderin enhances exocytosis, an effect blocked by two scinderin-derived actin-binding peptides and PIP2. Neuron, 17, 287-296.
66. Zhu, Q. and Clarke, M. (1992) Association of calmodulin and an unconventional myosin with the contractile vacuole complex of Dictyostelium discoideum. J. Cell Biol., 118, 347-358.