Drosophila Swiprosin-1/EFHD2 accumulates at the prefusion complex stage during Drosophila myoblast fusion

Journal of Cell Science

Volumn 124, Issue 19, 2011, Pages 3266-3278

  Hornbruch Freitag, Christina ^a   Griemert, Barbara ^a,b   Buttgereit, Detlev ^a   Renkawitz Pohl, Renate ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Actin foci; Calcium,myogenesis; Cg10641; Drosophila swip 1; Furmas; Immunological synapse; Singles bar; SL2 cells; Sticks and stones

Indexed keywords

CALCIUM BINDING PROTEIN; SWIPROSIN 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL MEMBRANE; DROSOPHILA; IMMUNE SYSTEM; MAMMAL; MUSCLE DEVELOPMENT; MUSCLE PERFUSION; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; ANIMALS; CELL ADHESION; CELL FUSION; CELL MEMBRANE; CONSERVED SEQUENCE; CYTOPLASMIC VESICLES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EXOCYTOSIS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; IMMUNE SYSTEM; IMMUNOGLOBULINS; INCLUSION BODIES; LARVA; MESODERM; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; MYOBLASTS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RNA INTERFERENCE; SEQUENCE DELETION; SIGNAL TRANSDUCTION;

MUS;

EID: 80053090362     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.083907     Document Type: Article

References (78)

1. Abmayr, S., Zhuang, S. and Geisbrecht, E. (2008). Myoblast fusion in Drosophila. Methods Mol. Biol. 475, 75-97.
2. Ackermann, F., Zitranski, N., Borth, H., Buech, T., Gudermann, T. and Boekhoff, I. (2009). CaMKIIalpha interacts with multi-PDZ domain protein MUPP1 in spermatozoa and prevents spontaneous acrosomal exocytosis. J. Cell Sci. 122, 4547-4557.
3. Armknecht, S., Boutros, M., Kiger, A., Nybakken, K., Mathey-Prevot, B. and Perrimon, N. (2005). High-throughput RNA interference screens in Drosophila tissue culture cells. Methods Enzymol. 392, 55-73.
4. Avramidou, A., Kroczek, C., Lang, C., Schuh, W., Jäck, H. and Mielenz, D. (2007). The novel adaptor protein Swiprosin-1 enhances BCR signals and contributes to BCR-induced apoptosis. Cell Death Differ. 14, 1936-1947.
5. Barclay, J., Morgan, A. and Burgoyne, R. (2005). Calcium-dependent regulation of exocytosis. Cell Calcium 38, 343-353.
6. Beckett, K. and Baylies, M. K. (2007). 3D analysis of founder cell and fusion competent myoblast arrangements outlines a new model of myoblast fusion. Dev. Biol. 309, 113-125.
7. Benado, A., Nasagi-Atiya, Y. and Sagi-Eisenberg, R. (2009). Protein trafficking in immune cells. Immunobiology 214, 507-525.
8. Berger, S., Schäfer, G., Kesper, D., Holz, A., Eriksson, T., Palmer, R., Beck, L., Klämbt, C., Renkawitz-Pohl, R. and Önel, S. (2008). WASP and SCAR have distinct roles in activating the Arp2/3 complex during myoblast fusion. J. Cell Sci. 121, 1303-1313.
9. Bischof, J., Maeda, R., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
10. Bour, B. A., Chakravarti, M., West, J. M. and Abmayr, S. M. (2000). Drosophila Sns, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev. 14, 1498-1511.
11. Brand, A. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
12. Brown, N. H. (1993). Integrins hold Drosophila together. BioEssays 15, 383-390.
13. Burgoyne, R. and Morgan, A. (2003). Secretory granule exocytosis. Physiol. Rev. 83, 581-632.
14. Carrasco-Rando, M. and Ruiz-Gómez, M. (2008). Mind bomb 2, a founder myoblastspecific protein, regulates myoblast fusion and muscle stability. Development 135, 849-857.
15. Chen, E. and Olson, E. (2004). Towards a molecular pathway for myoblast fusion in Drosophila. Trends Cell Biol. 14, 452-460.
16. Chintapalli, V., Wang, J. and Dow, J. (2007). Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39, 715-720.
17. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S. et al. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
18. Doberstein, S., Fetter, R., Mehta, A. and Goodman, C. (1997). Genetic analysis of myoblast fusion: blown fuse is required for progression beyond the prefusion complex. J. Cell Biol. 136, 1249-1261.
19. Dütting, S., Brachs, S. and Mielenz, D. (2011). Fraternal twins: Swiprosin-1/EFhd2 and Swiprosin-2/EFhd1, two homologous EF-hand containing calcium binding adaptor proteins with distinct functions. Cell Commun. Signal. 9, 2.
20. Estrada, B., Choe, S., Gisselbrecht, S., Michaud, S., Raj, L., Busser, B., Halfon, M., Church, G. and Michelson, A. (2006). An integrated strategy for analyzing the unique developmental programs of different myoblast subtypes. PLoS Genet. 2, e16.
21. Estrada, B., Maeland, A., Gisselbrecht, S., Bloor, J., Brown, N. and Michelson, A. (2007). The MARVEL domain protein, Singles Bar, is required for progression past the pre-fusion complex stage of myoblast fusion. Dev. Biol. 307, 328-339.
22. Furlong, E., Andersen, E., Null, B., White, K. and Scott, M. (2001). Patterns of gene expression during Drosophila mesoderm development. Science 293, 1629-1633.
23. Fyrberg, C., Parker, H., Hutchison, B. and Fyrberg, E. (1994). Drosophila melanogaster genes encoding three troponin-C isoforms and a calmodulin-related protein. Biochem. Genet. 32, 119-135.
24. Galletta, B. J., Chakravarti, M., Banerjee, R. and Abmayr, S M. (2004). SNS: Adhesive properties, localization requirements and ectodomain dependence in S2 cells and embryonic myoblasts. Mech. Dev. 121, 1455-1468.
25. Gifford, J., Walsh, M. and Vogel, H. (2007). Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem. J. 405, 199-221.
26. Gildor, B., Massarwa, R., Shilo, B. and Schejter, E. (2009). The SCAR and WASp nucleation-promoting factors act sequentially to mediate Drosophila myoblast fusion. EMBO Rep. 10, 1043-1050.
27. Hakeda-Suzuki, S., Ng, J., Tzu, J., Dietzl, G., Sun, Y., Harms, M., Nardine, T., Luo, L. and Dickson, B. (2002). Rac function and regulation during Drosophila development. Nature 416, 438-442.
28. Haralalka, S. and Abmayr, S. (2010). Myoblast fusion in Drosophila. Exp. Cell Res. 316, 3007-3013.
29. Henikoff, S., Henikoff, J., Sakai, A., Loeb, G. and Ahmad, K. (2009). Genome-wide profiling of salt fractions maps physical properties of chromatin. Genome Res. 19, 460-469.
30. Herranz, R., Díaz-Castillo, C., Nguyen, T. P., Lovato, T. L., Cripps, R. M. and Marco, R. (2004). Expression patterns of the whole troponin C gene repertoire during Drosophila development. Gene Expr. Patterns 4, 183-190.
31. Horsley, V. and Pavlath, G. (2004). Forming a multinucleated cell: molecules that regulate myoblast fusion. Cells Tissues Organs 176, 67-78.
32. Hübner, K., Windoffer, R., Hutter, H. and Leube, R. (2002). Tetraspan vesicle membrane proteins: synthesis, subcellular localization, and functional properties. Int. Rev. Cytol. 214, 103-159.
33. Hummel, T., Leifker, K. and Klämbt, C. (2000). The Drosophila HEM-2/NAP1 homolog KETTE controls axonal pathfinding and cytoskeletal organization. Genes Dev. 14, 863-873.
34. Kesper, D., Stute, C., Buttgereit, D., Kreisköther, N., Vishnu, S., Fischbach, K. and Renkawitz-Pohl, R. (2007). Myoblast fusion in Drosophila melanogaster is mediated through a fusion-restricted myogenic-adhesive structure (FuRMAS). Dev. Dyn. 236, 404-415.
35. Kim, S., Shilagardi, K., Zhang, S., Hong, S., Sens, K., Bo, J., Gonzalez, G. and Chen, E. (2007). A critical function for the actin cytoskeleton in targeted exocytosis of prefusion vesicles during myoblast fusion. Dev. Cell 12, 571-586.
36. Kroczek, C., Lang, C., Brachs, S., Grohmann, M., Dütting, S., Schweizer, A., Nitschke, L., Feller, S., Jäck, H. and Mielenz, D. (2010). Swiprosin-1/EFhd2 controls B cell receptor signaling through the assembly of the B cell receptor, Syk, and phospholipase C gamma2 in membrane rafts. J. Immunol. 184, 3665-3676.
37. Kummerow, C., Junker, C., Kruse, K., Rieger, H., Quintana, A. and Hoth, M. (2009). The immunological synapse controls local and global calcium signals in T lymphocytes. Immunol. Rev. 231, 132-147.
38. Laemmli, U. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
39. Leiss, D., Hinz, U., Gasch, A., Mertz, R. and Renkawitz-Pohl, R. (1988). Beta 3 tubulin expression characterizes the differentiating mesodermal germ layer during Drosophila embryogenesis. Development 104, 525-531.
40. Lupas, A. (1996). Coiled coils: new structures and new functions. Trends Biochem. Sci. 21, 375-382.
41. Maqbool, T. and Jagla, K. (2007). Genetic control of muscle development: learning from Drosophila. J. Muscle Res. Cell Motil. 28, 397-407.
42. Martens, S. and McMahon, H. (2008). Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9, 543-556.
43. Massarwa, R., Carmon, S., Shilo, B. and Schejter, E. (2007). WIP/WASp-based actinpolymerization machinery is essential for myoblast fusion in Drosophila. Dev. Cell 12, 557-569.
44. McMahon, H., Bolshakov, V., Janz, R., Hammer, R., Siegelbaum, S. and Südhof, T. (1996). Synaptophysin, a major synaptic vesicle protein, is not essential for neurotransmitter release. Proc. Natl. Acad. Sci. USA 93, 4760-4764.
45. McMahon, S. and Monroe, J. (1996). The role of early growth response gene 1 (egr-1) in regulation of the immune response. J. Leukoc. Biol. 60, 159-166.
46. Mielenz, D., Vettermann, C., Hampel, M., Lang, C., Avramidou, A., Karas, M. and Jäck, H. (2005). Lipid rafts associate with intracellular B cell receptors and exhibit a B cell stage-specific protein composition. J. Immunol. 174, 3508-3517.
47. Ng, J., Nardine, T., Harms, M., Tzu, J., Goldstein, A., Sun, Y., Dietzl, G., Dickson, B. and Luo, L. (2002). Rac GTPases control axon growth, guidance and branching. Nature 416, 442-447.
48. Nguyen, H. T., Voza, F., Ezzeddine, N. and Frasch, M. (2004). Drosophila mind bomb2 is required for maintaining muscle integrity and survival. J. Cell Biol. 22, 219-227.
49. Nose, A., Mahajan, V. B. and Goodman, C. S. (1992). Connectin: a homophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them in Drosophila. Cell 70, 553-567.
50. Önel, S. (2009). Actin regulators take the reins in Drosophila myoblast fusion. Cent. Eur. J. Biol. 4, 11-18.
51. Önel, S.-F. and Renkawitz-Pohl, R. (2009). FuRMAS: triggering myoblast fusion in Drosophila. Dev. Dyn. 238, 1513-1525.
52. Önel, S.-F., Dottermusch, C., Sickmann, A., Buttgereit, D. and Renkawitz-Pohl, R. (2011). Role of the actin cytoskeleton within FuRMAS during Drosophila myoblast fusion and first functionally conserved factors in vertebrates. In Cell Fusions: Regulation and Control (ed. I. Larsson), pp. 137-170. Heidelberg, Berlin: Springer.
53. Paululat, A., Burchard, S. and Renkawitz-Pohl, R. (1995). Fusion from myoblasts to myotubes is dependent on the rolling stone gene (rost) of Drosophila. Development 121, 2611-2620.
54. Ramesh, T., Kim, Y., Kwon, M., Jun, C. and Kim, S. (2009). Swiprosin-1 regulates cytokine expression of human mast cell line HMC-1 through actin remodeling. Immune Netw. 9, 274-284.
55. Richardson, B., Beckett, K., Nowak, S. and Baylies, M. (2007). SCAR/WAVE and Arp2/3 are crucial for cytoskeletal remodeling at the site of myoblast fusion. Development 134, 4357-4367.
56. Richardson, B., Beckett, K. and Baylies, M. (2008a). Live imaging of Drosophila myoblast fusion. Methods Mol. Biol. 475, 263-274.
57. Richardson, B., Nowak, S. and Baylies, M. (2008b). Myoblast fusion in fly and vertebrates: new genes, new processes and new perspectives. Traffic 9, 1050-1059.
58. Rochlin, K., Yu, S., Roy, S. and Baylies, M. (2010). Myoblast fusion: when it takes more to make one. Dev. Biol. 341, 66-83.
59. Ruiz-Gómez, M., Coutts, N., Price, A., Taylor, M. and Bate, M. (2000). Drosophila dumbfounded: a myoblast attractant essential for fusion. Cell 102, 189-198.
60. Sánchez-Pulido, L., Martín-Belmonte, F., Valencia, A. and Alonso, M. (2002). MARVEL: a conserved domain involved in membrane apposition events. Trends Biochem. Sci. 27, 599-601.
61. Sapir, A., Avinoam, O., Podbilewicz, B. and Chernomordik, L. (2008). Viral and developmental cell fusion mechanisms: conservation and divergence. Dev. Cell 14, 11-21.
62. Schäfer, G., Weber, S., Holz, A., Bogdan, S., Schumacher, S., Müller, A., Renkawitz-Pohl, R. and Önel, S. (2007). The Wiskott-Aldrich syndrome protein (WASP) is essential for myoblast fusion in Drosophila. Dev. Biol. 304, 664-674.
63. Schneider, I. (1972). Cell lines derived from late embryonic stages of Drosophila melanogaster. J. Embryol. Exp. Morphol. 27, 353-365.
64. Schröter, R., Lier, S., Holz, A., Bogdan, S., Klämbt, C., Beck, L. and Renkawitz-Pohl, R. (2004). kette and blown fuse interact genetically during the second fusion step of myogenesis in Drosophila. Development 131, 4501-4509.
65. Schröter, R., Buttgereit, D., Beck, L., Holz, A. and Renkawitz-Pohl, R. (2006). Blown fuse regulates stretching and outgrowth but not myoblast fusion of the circular visceral muscles in Drosophila. Differentiation 74, 608-621.
66. Schweizer, F. and Ryan, T. (2006). The synaptic vesicle: cycle of exocytosis and endocytosis. Curr. Opin. Neurobiol. 16, 298-304.
67. Sens, K. L., Zhang, S., Jin, P., Duan, R., Zhang, G., Luo, F., Parachini, L. and Chen, E. H. (2010). An invasive podosome-like structure promotes fusion pore formation during myoblast fusion. J. Cell Biol. 191, 1013-1027.
68. Shelton, C., Kocherlakota, K., Zhuang, S. and Abmayr, S. (2009). The immunoglobulin superfamily member Hbs functions redundantly with Sns in interactions between founder and fusion-competent myoblasts. Development 136, 1159-1168.
69. Strünkelnberg, M., Bonengel, B., Moda, L., Hertenstein, A., de Couet, H., Ramos, R. and Fischbach, K. (2001). rst and its paralogue kirre act redundantly during embryonic muscle development in Drosophila. Development 128, 4229-4239.
70. Stute, C., Kesper, D., Holz, A., Buttgereit, D. and Renkawitz-Pohl, R. (2006). Establishment of cell type specific Gal4-driver lines for the mesoderm of Drosophila. Dros Inf Serf 89, 111-115.
71. Tautz, D. and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81-85.
72. Thylur, R., Kim, Y., Kwon, M., Oh, H., Kwon, H., Kim, S., Im, S., Chun, J., Park, Z. and Jun, C. (2009). Swiprosin-1 is expressed in mast cells and up-regulated through the protein kinase C beta I/eta pathway. J. Cell. Biochem. 108, 705-715.
73. Tweedie, S., Ashburner, M., Falls, K., Leyland, P., McQuilton, P., Marygold, S., Millburn, G., Osumi-Sutherland, D., Schroeder, A., Seal, R. et al. (2009). FlyBase: enhancing Drosophila gene ontology annotations. Nucleic Acids Res. 37, D555-D559.
74. Valtorta, F., Pennuto, M., Bonanomi, D. and Benfenati, F. (2004). Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis? BioEssays 26, 445-453.
75. Vega, I. E., Traverso, E. E., Ferrer-Acosta, Y., Matos, E., Colon, M., Gonzales, J., Dickson, D., Hutton, M., Lewis, J. and Yen, S. H. (2008). A novel calcium-binding protein is associated with tau proteins in tauopathy. J. Neurochem. 106, 96-106.
76. Vuadens, F., Rufer, N., Kress, A., Corthésy, P., Schneider, P. and Tissot, J. (2004). Identification of swiprosin 1 in human lymphocytes. Proteomics 4, 2216-2220.
77. Wojcik, S. and Brose, N. (2007). Regulation of membrane fusion in synaptic excitationsecretion coupling: speed and accuracy matter. Neuron 55, 11-24.
78. Yamanaka, M. K., Saugstad, J. A., Hanson-Painton, O., McCarthy, B. J. and Tobin, S. L. (1987). Structure and expression of the Drosophila calmodulin gene. Nucleic Acids Res. 15, 3335-3348.