Drosophila twinfilin is required for cell migration and synaptic endocytosis

Journal of Cell Science

Volumn 123, Issue 9, 2010, Pages 1546-1556

  Wang, Dan ^a   Zhang, Lijun ^b   Zhao, Guoli ^a   Wahlström, Gudrun ^c,d   Heino, Tapio I ^c   Chen, Jiong ^b   Zhang, Yong Q ^a  

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^b NANJING UNIVERSITY   (China)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

Actin turnover; Cell migration; Endocytosis; Synapse; Twinfilin

Indexed keywords

ACTIN; BINDING PROTEIN; F ACTIN; FLUORESCENT DYE; FM1 43; GLUTAMATE RECEPTOR 2; TWINFILIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DROSOPHILA; ELECTROPHYSIOLOGY; ENDOCYTOSIS; EPITHELIUM CELL; EXOCYTOSIS; IMMUNOCHEMISTRY; LARVA; MOLECULAR DYNAMICS; MUTANT; NERVE FIBER GROWTH; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; OVARY FOLLICLE CELL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SYNAPSE VESICLE;

ACTINS; ANIMALS; AXONS; CELL MOVEMENT; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOCYTOSIS; EXOCYTOSIS; FEMALE; MICROFILAMENT PROTEINS; MUTATION; NEUROTRANSMITTER AGENTS; ORGAN SPECIFICITY; OVARIAN FOLLICLE; PROFILINS; RECEPTORS, GLUTAMATE; SYNAPSES; SYNAPTIC TRANSMISSION;

METAZOA;

EID: 77951732228     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.060251     Document Type: Article

References (49)

1. Baum, B. and Perrimon, N. (2001). Spatial control of the actin cytoskeleton in Drosophila epithelial cells. Nat. Cell Biol. 3, 883-890. (Pubitemid 32952252)
2. Boquet, I., Boujemaa, R., Carlier, M. F. and Preat, T. (2000). Ciboulot regulates actin assembly during Drosophila brain metamorphosis. Cell 102, 797-808.
3. Chen, J., Godt, D., Gunsalus, K., Kiss, I., Goldberg, M. and Laski, F. A. (2001). Cofilin/ADF is required for cell motility during Drosophila ovary development and oogenesis. Nat. Cell Biol. 3, 204-209. (Pubitemid 32118375)
4. Chen, K., Merino, C., Sigrist, S. J. and Featherstone, D. E. (2005). The 4.1 protein coracle mediates subunit-selective anchoring of Drosophila glutamate receptors to the postsynaptic actin cytoskeleton. J. Neurosci. 25, 6667-6675. (Pubitemid 40995299)
5. Cingolani, L. A. and Goda, Y. (2008). Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci. 9, 344-356.
6. Coleman, S. K., Cai, C., Mottershead, D. G., Haapalahti, J. P. and Keinanen, K. (2003). Surface expression of GluR-D AMPA receptor is dependent on an interaction between its C-terminal domain and a 4.1 protein. J. Neurosci. 23, 798-806. (Pubitemid 36206170)
7. Coyle, I. P., Koh, Y. H., Lee, W. C., Slind, J., Fergestad, T., Littleton, J. T. and Ganetzky, B. (2004). Nervous wreck, an SH3 adaptor protein that interacts with Wsp, regulates synaptic growth in Drosophila. Neuron. 41, 521-534. (Pubitemid 38253065)
8. DiAntonio, A., Petersen, S. A., Heckmann, M. and Goodman, C. S. (1999). Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. J. Neurosci. 19, 3023-3032. (Pubitemid 29173998)
9. Dickman, D. K., Horne, J. A., Meinertzhagen, I. A. and Schwarz, T. L. (2005). A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking synaptojanin and endophilin. Cell 123, 521-533.
10. Dickman, D. K., Lu, Z., Meinertzhagen, I. A. and Schwarz, T. L. (2006). Altered synaptic development and active zone spacing in endocytosis mutants. Curr. Biol. 16, 591-598.
11. Falck, S., Paavilainen, V. O., Wear, M. A., Grossmann, J. G., Cooper, J. A. and Lappalainen, P. (2004). Biological role and structural mechanism of twinfilin-capping protein interaction. EMBO J. 23, 3010-3019. (Pubitemid 39093595)
12. Feng, Y., Ueda, A. and Wu, C. F. (2004). A modified minimal hemolymph-like solution, HL3.1, for physiological recordings at the neuromuscular junctions of normal and mutant Drosophila larvae. J. Neurogenet. 18, 377-402. (Pubitemid 40052750)
13. Gareus, R., Di Nardo, A., Rybin, V. and Witke, W. (2006). Mouse profilin 2 regulates endocytosis and competes with SH3 ligand binding to dynamin 1. J. Biol. Chem. 281, 2803-2811. (Pubitemid 43845744)
14. Goode, B. L., Drubin, D. G. and Lappalainen, P. (1998). Regulation of the cortical actin cytoskeleton in budding yeast by twinfilin, a ubiquitous actin monomer-sequestering protein. J. Cell Biol. 142, 723-733.
15. Helfer, E., Nevalainen, E. M., Naumanen, P., Romero, S., Didry, D., Pantaloni, D., Lappalainen, P. and Carlier, M. F. (2006). Mammalian twinfilin sequesters ADPG-actin and caps filament barbed ends: implications in motility. EMBO J. 25, 1184-1195.
16. Hopmann, R. and Miller, K. G. (2003). A balance of capping protein and profilin functions is required to regulate actin polymerization in Drosophila bristle. Mol. Biol. Cell 14, 118-228. (Pubitemid 36106024)
17. Idrissi, F. Z., Wolf, B. L. and Geli, M. I. (2002). Cofilin, but not profilin, is required for myosin-I-induced actin polymerization and the endocytic uptake in yeast. Mol. Biol. Cell 13, 4074-4087.
18. Iwasa, J. H. and Mullins, R. D. (2007). Spatial and temporal relationships between actinfilament nucleation, capping, and disassembly. Curr. Biol. 17, 395-406. (Pubitemid 46320990)
19. Jan, L. Y. and Jan, Y. N. (1976). Properties of the larval neuromuscular junction in Drosophila melanogaster. J. Physiol. 262, 189-214.
20. Jin, S., Pan, L., Liu, Z., Wang, Q., Xu, Z. and Zhang, Y. Q. (2009). Drosophila Tubulin-specific chaperone E functions at neuromuscular synapses and is required for microtubule network formation. Development 136, 1571-1581.
21. Kaksonen, M., Toret, C. P. and Drubin, D. G. (2006). Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7, 404-414. (Pubitemid 44050094)
22. Koh, T. W., Verstreken, P. and Bellen, H. J. (2004). Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43, 193-205. (Pubitemid 38942960)
23. Kuromi, H. and Kidokoro, Y. (1998). Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 20, 917-925. (Pubitemid 28247397)
24. Lappalainen, P. and Drubin, D. G. (1997). Cofilin promotes rapid actin filament turnover in vivo. Nature 388, 78-82. (Pubitemid 27283892)
25. Marrus, S. B., Portman, S. L., Allen, M. J., Moffat, K. G. and DiAntonio, A. (2004). Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J. Neurosci. 24, 1406-1415. (Pubitemid 38222992)
26. Martin, A. R. (1955). A further study of the statistical composition on the end-plate potential. J. Physiol. 130, 114-122.
27. Michel, C. I., Kraft, R. and Restifo, L. L. (2004). Defective neuronal development in the mushroom bodies of Drosophila fragile X mental retardation 1 mutants. J. Neurosci. 24, 5798-5809. (Pubitemid 38857234)
28. Moseley, J. B., Okada, K., Balcer, H. I., Kovar, D. R., Pollard, T. D. and Goode, B. L. (2006). Twinfilin is an actin-filament-severing protein and promotes rapid turnover of actin structures in vivo. J. Cell Sci. 119, 1547-1557. (Pubitemid 43732981)
29. Naora, H. and Montell, D. J. (2005). Ovarian cancer metastasis: integrating insights from disparate model organisms. Nat. Rev. Cancer 5, 355-366. (Pubitemid 40637827)
30. Ng, J. and Luo, L. (2004). Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 44, 779-793. (Pubitemid 39575632)
31. Ojala, P. J., Paavilainen, V. O., Vartiainen, M. K., Tuma, R., Weeds, A. G. and Lappalainen, P. (2002). The two ADF-H domains of twinfilin play functionally distinct roles in interactions with actin monomers. Mol. Biol. Cell 13, 3811-3821. (Pubitemid 35398550)
32. Okreglak, V. and Drubin, D. G. (2007). Cofilin recruitment and function during actin-mediated endocytosis dictated by actin nucleotide state. J. Cell Biol. 178, 1251-1264. (Pubitemid 47480230)
33. Paavilainen, V. O., Bertling, E., Falck, S. and Lappalainen, P. (2004). Regulation of cytoskeletal dynamics by actin-monomer-binding proteins. Trends Cell. Biol. 14, 386-394. (Pubitemid 38891708)
34. Paavilainen, V. O., Hellman, M., Helfer, E., Bovellan, M., Annila, A., Carlier, M. F., Permi, P. and Lappalainen, P. (2007). Structural basis and evolutionary origin of actin filament capping by twinfilin. Proc. Natl. Acad. Sci. USA 104, 3113-3118. (Pubitemid 46364122)
35. Palmgren, S., Ojala, P. J., Wear, M. A., Cooper, J. A. and Lappalainen, P. (2001). Interactions with PIP2, ADP-actin monomers, and capping protein regulate the activity and localization of yeast twinfilin. J. Cell Biol. 155, 251-260. (Pubitemid 34289300)
36. Palmgren, S., Vartiainen, M. and Lappalainen, P. (2002). Twinfilin, a molecular mailman for actin monomers. J. Cell Sci. 115, 881-886. (Pubitemid 34257373)
37. Pantaloni, D., Le Clainche, C. and Carlier, M. F. (2001). Mechanism of actin-based motility. Science 292, 1502-1506.
38. Pelkmans, L., Fava, E., Grabner, H., Hannus, M., Habermann, B., Krausz, E. and Zerial, M. (2005). Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436, 78-86. (Pubitemid 40966188)
39. Rosenmund, C. and Westbrook, G. L. (1993). Calcium-induced actin depolymerization reduces NMDA channel activity. Neuron 10, 805-814. (Pubitemid 23152037)
40. Schenck, A., Bardoni, B., Langmann, C., Harden, N., Mandel, J. L. and Giangrande, A. (2003). CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38, 887-898. (Pubitemid 36782381)
41. Shirao, T. and Sekino, Y. (2001). Clustering and anchoring mechanisms of molecular constituents of postsynaptic scaffolds in dendritic spines. Neurosci. Res. 40, 1-7. (Pubitemid 32328233)
42. Smythe, E. and Ayscough, K. R. (2006). Actin regulation in endocytosis. J. Cell Sci. 119, 4589-4598.
43. Vartiainen, M., Ojala, P. J., Auvinen, P., Peranen, J. and Lappalainen, P. (2000). Mouse A6/twinfilin is an actin monomer-binding protein that localizes to the regions of rapid actin dynamics. Mol. Cell. Biol. 20, 1772-1783. (Pubitemid 30100195)
44. Vartiainen, M. K., Sarkkinen, E. M., Matilainen, T., Salminen, M. and Lappalainen, P. (2003). Mammals have two twinfilin isoforms whose subcellular localizations and tissue distributions are differentially regulated. J. Biol. Chem. 278, 34347-34355. (Pubitemid 37553279)
45. Verstreken, P., Kjaerulff, O., Lloyd, T. E., Atkinson, R., Zhou, Y., Meinertzhagen, I. A. and Bellen, H. J. (2002). Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109, 101-112. (Pubitemid 34327520)
46. Wahlström, G., Vartiainen, M., Yamamoto, L., Mattila, P. K., Lappalainen, P. and Heino, T. I. (2001). Twinfilin is required for actin-dependent developmental processes in Drosophila. J. Cell Biol. 155, 787-796. (Pubitemid 34286231)
47. Winder, S. J. and Ayscough, K. R. (2005). Actin-binding proteins. J. Cell Sci. 118, 651-654.
48. Wolven, A. K., Belmont, L. D., Mahoney, N. M., Almo, S. C. and Drubin, D. G. (2000). In vivo importance of actin nucleotide exchange catalyzed by profilin. J. Cell Biol. 150, 895-904.
49. Zhang, Y. Q., Bailey, A. M., Matthies, H. J., Renden, R. B., Smith, M. A., Speese, S. D., Rubin, G. M. and Broadie, K. (2001). Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107, 591-603.