Drosophila homologue of Eps15 is essential for synaptic vesicle recycling

Experimental Cell Research

Volumn 312, Issue 12, 2006, Pages 2288-2298

  Majumdar, Amitabha ^a   Ramagiri, Shobha ^a   Rikhy, Richa ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

Drosophila; Eps15; Shibire; Stoned; Synaptic vesicle recycling; Adaptin

Indexed keywords

ALPHA ADAPTIN; DROSOPHILA PROTEIN; DYNAMIN; EPIDERMAL GROWTH FACTOR RECEPTOR PATHWAY SUBSTRATE 15; MUTANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; COMPARATIVE STUDY; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; GENETICS; LARVA; NEUROMUSCULAR SYNAPSE; NEUROPHYSIOLOGY; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN INTERACTION; RECYCLING; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; SYNAPSE VESICLE; TEMPERATURE SENSITIVITY; TISSUE LEVEL;

MAMMALIA;

EID: 33745229330     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2006.03.030     Document Type: Article

References (51)

1. Estes P.S., Roos J., van der Bliek A., Kelly R.B., Krishnan K.S., and Ramaswami M. Traffic of dynamin within individual Drosophila synaptic boutons relative to compartment-specific markers. J. Neurosci. 16 (1996) 5443-5456
2. Roos J., and Kelly R.B. The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol. 9 (1999) 1411-1414
3. Gaidarov I., Santini F., Warren R.A., and Keen J.H. Spatial control of coated-pit dynamics in living cells. Nat. Cell Biol. 1 (1999) 1-7
4. Blanpied T.A., Scott D.B., and Ehlers M.D. Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36 (2002) 435-449
5. Fazioli F., Minichiello L., Matoskova B., Wong W.T., and Di Fiore P.P. eps15, a novel tyrosine kinase substrate, exhibits transforming activity. Mol. Cell. Biol. 13 (1993) 5814-5828
6. Torrisi M.R., Lotti L.V., Belleudi F., Gradini R., Salcini A.E., Confalonieri S., Pelicci P.G., and Di Fiore P.P. Eps15 is recruited to the plasma membrane upon epidermal growth factor receptor activation and localizes to components of the endocytic pathway during receptor internalization. Mol. Biol. Cell 10 (1999) 417-434
7. Benmerah A., Gagnon J., Begue B., Megarbane B., Dautry-Varsat A., and Cerf-Bensussan N. The tyrosine kinase substrate eps15 is constitutively associated with the plasma membrane adaptor AP-2. J. Cell Biol. 131 (1995) 1831-1838
8. Benmerah A., Begue B., Dautry-Varsat A., and Cerf-Bensussan N. The ear of alpha-adaptin interacts with the COOH-terminal domain of the Eps 15 protein. J. Biol. Chem. 271 (1996) 12111-12116
9. Benmerah A., Lamaze C., Begue B., Schmid S.L., Dautry-Varsat A., and Cerf-Bensussan N. AP-2/Eps15 interaction is required for receptor-mediated endocytosis. J. Cell Biol. 140 (1998) 1055-1062
10. Wendland B., and Emr S.D. Pan1p, yeast eps15, functions as a multivalent adaptor that coordinates protein-protein interactions essential for endocytosis. J. Cell Biol. 141 (1998) 71-84
11. Morgan J.R., Prasad K., Jin S., Augustine G.J., and Lafer E.M. Eps15 homology domain-NPF motif interactions regulate clathrin coat assembly during synaptic vesicle recycling. J. Biol. Chem. 278 (2003) 33583-33592
12. van Delft S., Schumacher C., Hage W., Verkleij A.J., and van Bergen en Henegouwen P.M. Association and colocalization of Eps15 with adaptor protein-2 and clathrin. J. Cell Biol. 136 (1997) 811-821
13. Chen H., Slepnev V.I., Di Fiore P.P., and De Camilli P. The interaction of epsin and Eps15 with the clathrin adaptor AP-2 is inhibited by mitotic phosphorylation and enhanced by stimulation-dependent dephosphorylation in nerve terminals. J. Biol. Chem. 274 (1999) 3257-3260
14. Martina J.A., Bonangelino C.J., Aguilar R.C., and Bonifacino J.S. Stonin 2: an adaptor-like protein that interacts with components of the endocytic machinery. J. Cell Biol. 153 (2001) 1111-1120
15. Cupers P., Jadhav A.P., and Kirchhausen T. Assembly of clathrin coats disrupts the association between Eps15 and AP-2 adaptors. J. Biol. Chem. 273 (1998) 1847-1850
16. Benmerah A., Bayrou M., Cerf-Bensussan N., and Dautry-Varsat A. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112 (1999) 1303-1311
17. Salcini A.E., Hilliard M.A., Croce A., Arbucci S., Luzzi P., Tacchetti C., Daniell L., De Camilli P., Pelicci P.G., Di Fiore P.P., and Bazzicalupo P. The Eps15 C. elegans homologue EHS-1 is implicated in synaptic vesicle recycling. Nat. Cell Biol. 3 (2001) 755-760
18. Ramaswami M., Rao S., van der Bliek A., Kelly R.B., and Krishnan K.S. Genetic studies on dynamin function in Drosophila. J. Neurogenet. 9 (1993) 73-87
19. Mathew D., Gramates L.S., Packard M., Thomas U., Bilder D., Perrimon N., Gorczyca M., and Budnik V. Recruitment of scribble to the synaptic scaffolding complex requires GUK-holder, a novel DLG binding protein. Curr. Biol. 12 (2002) 531-539
20. Guha A., Sriram V., Krishnan K.S., and Mayor S. Shibire mutations reveal distinct dynamin independent and dependent endocytic pathways in primary cultures of Drosophila hemocytes. J. Cell Sci. 116 (2003) 3373-3386
21. Macleod G.T., Marin L., Charlton M.P., and Atwood H.L. Synaptic vesicles: test for a role in presynaptic calcium regulation. J. Neurosci. 24 (2004) 2495-2505
22. Krishnan K.S., Rikhy R., Rao S., Shivalkar M., Mosko M., Narayanan R., Etter P., Estes P.S., and Ramaswami M. Nucleoside diphosphate kinase, a source of GTP, is required for dynamin-dependent synaptic vesicle recycling. Neuron 30 (2001) 197-210
23. Ramaswami M., Krishnan K.S., and Kelly R.B. Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron 13 (1994) 363-375
24. Lloyd T.E., Verstreken P., Ostrin E.J., Phillippi A., Lichtarge O., and Bellen H.J. A genome-wide search for synaptic vesicle cycle proteins in Drosophila. Neuron 26 (2000) 45-50
25. Sun B., Xu P., and Salvaterra P.M. Dynamic visualization of nervous system in live Drosophila. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10438-10443
26. Hotta Y., and Benzer S. Abnormal electroretinograms in visual mutants of Drosophila. Nature 222 (1969) 354-356
27. Heisenberg M. Separation of receptor and lamina potentials in the electroretinogram of normal and mutant Drosophila. J. Exp. Biol. 55 (1971) 85-100
28. Kelly L.E., and Suzuki D.T. The effects of increased temperature on electroretinograms of temperature-sensitive paralysis mutants of Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 71 (1974) 4906-4909
29. Pallanck L., Ordway R.W., and Ganetzky B. A Drosophila NSF mutant. Nature 376 (1995) 25
30. Estes P.S., Jackson T.C., Stimson D.T., Sanyal S., Kelly L.E., and Ramaswami M. Functional dissection of a eukaryotic dicistronic gene: transgenic stonedB, but not stonedA, restores normal synaptic properties to Drosophila stoned mutants. Genetics 165 (2003) 185-196
31. Stowers R.S., and Schwarz T.L. A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics 152 (1999) 1631-1639
32. Chen M.S., Obar R.A., Schroeder C.C., Austin T.W., Poodry C.A., Wadsworth S.C., and Vallee R.B. Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351 (1991) 583-586
33. van der Bliek A.M., and Meyerowitz E.M. Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351 (1991) 411-414
34. Poodry C.A., and Edgar L. Reversible alteration in the neuromuscular junctions of Drosophila melanogaster bearing a temperature-sensitive mutation, shibire. J. Cell Biol. 81 (1979) 520-527
35. Kosaka T., and Ikeda K. Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J. Neurobiol. 14 (1983) 207-225
36. Koenig J.H., and Ikeda K. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9 (1989) 3844-3860
37. Petrovich T.Z., Merakovsky J., and Kelly L.E. A genetic analysis of the stoned locus and its interaction with dunce, shibire and Suppressor of stoned variants of Drosophila melanogaster. Genetics 133 (1993) 955-965
38. Kawasaki F., Mattiuz A.M., and Ordway R.W. Synaptic physiology and ultrastructure in comatose mutants define an in vivo role for NSF in neurotransmitter release. J. Neurosci. 18 (1998) 10241-10249
39. Sone M., Suzuki E., Hoshino M., Hou D., Kuromi H., Fukata M., Kuroda S., Kaibuchi K., Nabeshima Y., and Hama C. Synaptic development is controlled in the periactive zones of Drosophila synapses. Development 127 (2000) 4157-4168
40. Koenig J.H., and Ikeda K. Synaptic vesicles have two distinct recycling pathways. J. Cell Biol. 135 (1996) 797-808
41. Ikeda K., Ozawa S., and Hagiwara S. Synaptic transmission reversibly conditioned by single-gene mutation in Drosophila melanogaster. Nature 259 (1976) 489-491
42. Fergestad T., and Broadie K. Interaction of stoned and synaptotagmin in synaptic vesicle endocytosis. J. Neurosci. 21 (2001) 1218-1227
43. Stimson D.T., Estes P.S., Rao S., Krishnan K.S., Kelly L.E., and Ramaswami M. Drosophila stoned proteins regulate the rate and fidelity of synaptic vesicle internalization. J. Neurosci. 21 (2001) 3034-3044
44. Walther K., Diril M.K., Jung N., and Haucke V. Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 964-969
45. Phillips A.M., Smith M., Ramaswami M., and Kelly L.E. The products of the Drosophila stoned locus interact with synaptic vesicles via synaptotagmin. J. Neurosci. 20 (2000) 8254-8261
46. Gonzalez-Gaitan M., and Jackle H. Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell 88 (1997) 767-776
47. Zhang B., Koh Y.H., Beckstead R.B., Budnik V., Ganetzky B., and Bellen H.J. Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21 (1998) 1465-1475
48. Roos J., and Kelly R.B. Dap160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin. J. Biol. Chem. 273 (1998) 19108-19119
49. Guichet A., Wucherpfennig T., Dudu V., Etter S., Wilsch-Brauniger M., Hellwig A., Gonzalez-Gaitan M., Huttner W.B., and Schmidt A.A. Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction. EMBO J. 21 (2002) 1661-1672
50. Verstreken P., Kjaerulff O., Lloyd T.E., Atkinson R., Zhou Y., Meinertzhagen I.A., and Bellen H.J. Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109 (2002) 101-112
51. Rikhy R., Kumar V., Mittal R., and Krishnan K.S. Endophilin is critically required for synapse formation and function in Drosophila melanogaster. J. Neurosci. 22 (2002) 7478-7484