Presynaptic calcium channel localization and calcium-dependent synaptic vesicle exocytosis regulated by the fuseless protein

Journal of Neuroscience

Volumn 28, Issue 14, 2008, Pages 3668-3682

  Long, A Ashleigh ^a   Kim, Eunju ^b   Leung, Hung Tat ^b   Woodruff III, Elvin ^a   An, Lingling ^b   Doerge, R W ^b   Pak, William L ^b   Broadie, Kendal ^a,c  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b PURDUE UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

Drosophila; Exocytosis; Neuromuscular junction; Photoreceptor; Synapse; Synaptic vesicle

Indexed keywords

CALCIUM; CALCIUM CHANNEL; FUSELESS PROTEIN; GENE PRODUCT; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; DROSOPHILA PROTEIN; GREEN FLUORESCENT PROTEIN; NERVE PROTEIN;

ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DROSOPHILA; EXOCYTOSIS; FUSELESS GENE; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; TRANSGENE; ULTRASTRUCTURE; WILD TYPE; ANIMAL; ANIMAL EMBRYO; CELL MEMBRANE; DRUG EFFECT; ELECTRORETINOGRAPHY; EVOKED VISUAL RESPONSE; GENETICS; HISTOLOGY; METABOLISM; METHODOLOGY; MICROARRAY ANALYSIS; MUTATION; NEUROMUSCULAR SYNAPSE; PATCH CLAMP; PHOTOSTIMULATION; PHOTOTRANSDUCTION; PHYSIOLOGY; RNA INTERFERENCE; SYNAPTOSOME; TRANSGENIC ANIMAL; VISUAL SYSTEM;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALCIUM; CALCIUM CHANNELS; CELL MEMBRANE; DROSOPHILA; DROSOPHILA PROTEINS; ELECTRORETINOGRAPHY; EMBRYO, NONMAMMALIAN; EVOKED POTENTIALS, VISUAL; EXOCYTOSIS; GREEN FLUORESCENT PROTEINS; MEMBRANE PROTEINS; MICROARRAY ANALYSIS; MUTATION; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; PHOTOTRANSDUCTION; PRESYNAPTIC TERMINALS; RNA INTERFERENCE; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; VISUAL PATHWAYS;

EID: 43649094011     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5553-07.2008     Document Type: Article

References (88)

1. Ambudkar IS (2007) TRPC1: a core component of store-operated calcium channels. Biochem Soc Trans 35:96-100.
2. Andrews HK, Zhang YQ, Trotta N, Broadie K (2002) Drosophila sec10 is required for hormone secretion but not general exocytosis or neurotransmission. Traffic 3:906-921.
3. Aravamudan B, Broadie K (2003) Synaptic Drosophila UNC-13 is regulated by antagonistic G-protein pathways via a proteasome-dependent degradation mechanism. J Neurobiol 54:417-438.
4. Aravamudan B, Fergestad T, Davis WS, Rodesch CK, Broadie K (1999) Drosophila UNC-13 is essential for synaptic transmission. Nat Neurosci 2:965-971.
5. Becherer U, Moser T, Stuhmer W, Oheim M (2003) Calcium regulates exocytosis at the level of single vesicles. Nat Neurosci 6:846-853.
6. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. JR Stat Soc Ser B 57:289-300.
7. Bourne Y, Dannenberg J, Pollmann V, Marchot P, Pongs O (2001) Immunocytochemical localization and crystal structure of human frequenin (neuronal calcium sensor 1). J Biol Chem 276:11949-11955.
8. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
9. Broadie K, Bellen HJ, DiAntonio A, Littleton JT, Schwarz TL (1994) Absence of synaptotagmin disrupts excitation-secretion coupling during synaptic transmission. Proc Natl Acad Sci USA 91:10727-10731.
10. Broadie K, Prokop A, Bellen HJ, O'Kane CJ, Schulze KL, Sweeney ST (1995) Syntaxin and synaptobrevin function downstream of vesicle docking in Drosophila. Neuron 15:663-673.
11. Buchner E (1991) Genes expressed in the adult brain of Drosophila and effects of their mutations on behavior: a survey of transmitter- and second messenger-related genes. J Neurogenet 7:153-192.
12. Burg MG, Sarthy PV, Koliantz G, Pak WL (1993) Genetic and molecular identification of a Drosophila histidine decarboxylase gene required in photoreceptor transmitter synthesis. EMBO J 12:911-919.
13. Chen YA, Scales SJ, Jagath JR, Scheller RH (2001) A discontinuous SNAP-25 C-terminal coil supports exocytosis. J Biol Chem 276:28503-28508.
14. Craig EA, Eisenman HC, Hundley HA (2003) Ribosome-tethered molecular chaperones: the first line of defense against protein misfolding. Curr Opin Microbiol 157:162.
15. Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, Krantz DE, DiAntonio A (2004) Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J Neurosci 24:10466-10474.
16. Deitcher DL, Ueda A, Stewart BA, Burgess RW, Kidokoro Y, Schwarz TL (1998) Distinct requirements for evoked and spontaneous release of neurotransmitter are revealed by mutations in the Drosophila gene neuronalsynaptobrevin. J Neurosci 18:2028-2039.
17. Del Castillo J, Katz B (1954) The failure of local-circuit transmission at the nerve-muscle junction. J Physiol (Lond) 123:7-8P.
18. Demuro A, Parker I (2006) Imaging single-channel calcium microdomains. Cell Calcium 40:413-422.
19. Dermaut B, Norga KK, Kania A, Verstreken P, Pan H, Zhou Y, Callaerts P, Bellen HJ (2005) Aberrant lysosomal carbohydrate storage accompanies endocytic defects and neurodegeneration in Drosophila benchwarmer. J Cell Biol 170:127-139.
20. DiAntonio A, Schwarz TL (1994) The effect on synaptic physiology of synaptotagmin mutations in Drosophila. Neuron 12:909-920.
21. DiAntonio A, Petersen SA, Heckmann M, Goodman CS (1999) Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. J Neurosci 19:3023-3032.
22. Dodge Jr FA, Rahamimoff R (1967) Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol (Lond) 193:419-432.
23. Farsad K, De Camilli P (2002) Neurotransmission and the synaptic vesicle cycle. Yale J Biol Med 75:261-284.
24. Featherstone DE, Davis WS, Dubreuil RR, Broadie K (2001) Drosophila α-and β-spectrin mutations disrupt presynaptic neurotransmitter release. J Neurosci 21:4215-4224.
25. Featherstone DE, Rushton E, Rohrbough J, Liebel F, Karr J, Sheng Q, Rodesch CK, Broadie K (2005) An essential Drosophila glutamate receptor subunit that functions in both neuropil and neuromuscular junction. J Neurosci 25:3199-3208.
26. Fergestad T, Broadie K (2001) Interaction of stoned and synaptotagmin in synaptic vesicle endocytosis. J Neurosci 21:1218-1227.
27. 2+ sensor for transmitter release at a central synapse. Cell 79:717-727.
28. Hille B (2001) Ion channels of excitable membranes. Sunderland, MA: Sinauer Associates.
29. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65-70.
30. Horrigan FT, Bookman RJ (1994) Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13:1119-1129.
31. Huang FD, Woodruff E, Mohrmann R, Broadie K (2006) Rolling blackout is required for synaptic vesicle exocytosis. J Neurosci 26:2369-2379.
32. Johnson EC, Pak WL (1986) Electrophysiological study of Drosophila rhodopsin mutants. J Gen Physiol 88:651-673.
33. Katz B, Miledi R (1965) The effect of calcium on acetylcholine release from motor nerve terminals. Proc R Soc Lond B Biol Sci 161:496-503.
34. Katz B, Miledi R (1968) The role of calcium in neuromuscular facilitation. J Physiol (Lond) 195:481-492.
35. Katz B, Miledi R (1970) Further study of the role of calcium in synaptic transmission. J Physiol (Lond) 207:789-801.
36. Kawasaki F, Mattiuz AM, Ordway RW (1998) Synaptic physiology and ultrastructure in comatose mutants define an in vivo role for NSF in neurotransmitter release. J Neurosci 18:10241-10249.
37. Kawasaki F, Felling R, Ordway RW (2000) A temperature-sensitive paralytic mutant defines a primary synaptic calcium channel in Drosophila. J Neurosci 20:4885-4889.
38. Kawasaki F, Collins SC, Ordway RW (2002) Synaptic calcium-channel function in Drosophila: analysis and transformation rescue of temperature-sensitive paralytic and lethal mutations of cacophony. J Neurosci 22:5856-5864.
39. Kawasaki F, Zou B, Xu X, Ordway RW (2004) Active zone localization of presynaptic calcium channels encoded by the cacophony locus of Drosophila. J Neurosci 24:282-285.
40. 2+-regulated versus constitutive exocytosis. J Neurosci 23:10531-10539.
41. Kidokoro Y (2003) Roles of SNARE proteins and synaptotagmin I in synaptic transmission: studies at the Drosophila neuromuscular synapse. Neurosignals 12:13-30.
42. Kiss JZ, Rougon G (1997) Cell biology of polysialic acid. Curr Opin Neurobiol 7:640-646.
43. 2+ channel clustering, and vesicle release. Science 312:1051-1054.
44. Kuromi H, Kidokoro Y (2000) Tetanic stimulation recruits vesicles from reserve pool via a cAMP-mediated process in Drosophila synapses. Neuron 27:133-143.
45. Lam G, Thummel CS (2000) Inducible expression of double-stranded RNA directs specific genetic interference in Drosophila. Curr Biol 10:957-963.
46. Larivee DC, Conrad SK, Stephenson RS, Pak WL (1981) Mutation that selectively affects rhodopsin concentration in the peripheral photoreceptors of Drosophila melanogaster. J Gen Physiol 78:521-545.
47. Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. New York: Academic.
48. Littleton JT, Ganetzky B (2000) Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26:35-43.
49. Littleton JT, Bellen HJ, Perin MS (1993) Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse. Development 118:1077-1088.
50. Littleton JT, Chapman ER, Kreber R, Garment MB, Carlson SD, Ganetzky B (1998) Temperature-sensitive paralytic mutations demonstrate that synaptic exocytosis requires SNARE complex assembly and disassembly. Neuron 21:401-413.
51. Llinas R, Steinberg IZ, Walton K (1976) Presynaptic calcium currents and their relation to synaptic transmission: voltage clamp study in squid giant synapse and theoretical model for the calcium gate. Proc Natl Acad Sci USA 73:2918-2922.
52. Llinas R, Sugimori M, Silver RB (1992) Microdomains of high calcium concentration in a presynaptic terminal. Science 256:677-679.
53. 2+ dynamics along identified synaptic terminals in Drosophila larvae. J Neurosci 26:12283-12293.
54. Markow TA, Merriam J (1977) Phototactic and geotactic behavior of countercurrent defective mutants of Drosophila melanogaster. Behav Genet 7:447-455.
55. Melzig J, Burg MG, Pak WL, Buchner E (1998) Selective histamine uptake rescues photo- and mechanoreceptor function of histidine decarboxylase-deficient Drosophila mutant. J Neurosci 18:7160-7166.
56. 2+ channels. Neuron 17:781-788.
57. Morin PM, Sagne C, Gasnier B (2004) Functional characterization of wildtype and mutant human sialin. EMBO J 23:4560-4570.
58. Nishimune H, Sanes JR, Carlson SS (2004) A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432:580-587.
59. Ohnishi O (1977) Spontaneous and ethyl methanesulfonate-induced mutations controlling viability in Drosophila melanogaster. III. Heterozygous effect of polygenic mutations. Genetics 87:547-556.
60. Pak WL (1975) Mutations affecting the vision of Drosophila melanogaster. In: Handbook of genetics, Vol 3 (King RC, ed), pp 703-733. New York: Plenum.
61. Pak WL (1995) Drosophila in vision research. The Friedenwald Lecture. Invest Ophthalmol Vis Sci 36:2340-2357.
62. Pak WL, Leung H-T (2003) Genetic approaches to visual transduction in Drosophila melanogaster. Receptors Channels 9:149-167.
63. 2+ sensor-1 in bovine chromaffin cells. J Neurosci 22:2427-2433.
64. Pongs O (1993) Structure-function studies on the pore of potassium channels. J Membr Biol 136:1-8.
65. Richmond JE, Broadie KS (2002) The synaptic vesicle cycle: exocytosis and endocytosis in Drosophila and C. elegans. Curr Opin Neurobiol 12:499-507.
66. Rizo J, Sudhof TC (2002) Snares and Munc18 in synaptic vesicle fusion. Nat Rev Neurosci 3:641-653.
67. Rohrbough J, Pinto S, Mihalek RM, Tully T, Broadie K (1999) latheo, a Drosophila gene involved in learning, regulates functional synaptic plasticity. Neuron 23:55-70.
68. Sheng ZH, Westenbroek RE, Catterall WA (1998) Physical link and functional coupling of presynaptic calcium channels and the synaptic vesicle docking/fusion machinery. J Bioenerg Biomembr 30:335-345.
69. Sippy T, Cruz-Martin A, Jeromin A, Schweizer FE (2003) Acute changes in short-term plasticity at synapses with elevated levels of neuronal calcium sensor-1. Nat Neurosci 6:1031-1038.
70. Speese SD, Trotta N, Rodesch CK, Aravamudan B, Broadie K (2003) The ubiquitin proteasome system acutely regulates presynaptic protein turnover and synaptic efficacy. Curr Biol 13:899 910.
71. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymphlike physiological solutions. J Comp Physiol 2:179-191.
72. Suzuki DT, Procunier D (1969) Temperature-sensitive mutations in Drosophila melanogaster. 3. Dominant lethals and semilethals on chromosome 2. Proc Natl Acad Sci USA 62:369-376.
73. Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, Urlaub H, Schenck S, Brügger B, Ringler P, Müller SA, Rammner B, Gräter F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmüller H, Heuser J, et al. (2006) Molecular anatomy of a trafficking organelle. Cell 127:831-846.
74. Trotta N, Rodesch CK, Fergestad T, Broadie K (2004) Cellular bases of activity-dependent paralysis in Drosophila stress-sensitive mutants. J Neurobiol 60:328-347.
75. Tsujimoto T, Jeromin A, Saitoh N, Roder JC, Takahashi T (2002) Neuronal calcium sensor 1 and activity-dependent facilitation of P/Q-type calcium currents at presynaptic nerve terminals. Science 295:2276-2279.
76. Verheijen FW, Verbeek E, Aula N, Beerens C, Havelaar A, Joosse M, Peltonen L, Aula P, Galjaard H, van der Spek P, Mancini G (1999) A new gene, encoding an anion transporter, is mutated in sialic acid storage diseases. Nat Genet 23:462-465.
77. Von Schilcher F (1976) The behavior of cacophony, a courtship song mutant in Drosophila melanogaster. Behav Biol 17:187-196.
78. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Durrbeck H, Buchner S, Dabauvalle MC, Schmidt M, Qin G, Wichmann C, Kittel R, Sigrist SJ, Buchner E (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49:833-844.
79. 2+ channels and transmitter release. Neuron 32:99-112.
80. Wreden CC, Wlizla M, Reimer RJ (2005) Varied mechanisms underlie the free sialic acid storage disorders. J Biol Chem 280:1408-1416.
81. Wu MN, Fergestad T, Lloyd TE, He Y, Broadie K, Bellen HJ (1999) Syntaxin 1A interacts with multiple exocytic proteins to regulate neurotransmitter release in vivo. Neuron 23:593-605.
82. Xing B, Ashleigh Long A, Harrison DA, Cooper RL (2005) Developmental consequences of neuromuscular junctions with reduced presynaptic calcium channel function. Synapse 57:132-147.
83. Yarovaya N, Schot R, Fodero L, McMahon M, Mahoney A, Williams R, Verbeek E, de Bondt A, Hampson M, van der Spek P, Stubbs A, Masters CL, Verheijen FW, Mancini GM, Venter DJ (2005) Sialin, an anion transporter defective in sialic acid storage diseases, shows highly variable expression in adult mouse brain, and is developmentally regulated. Neurobiol Dis 19:351-365.
84. Yoshihara M, Littleton JT (2002) Synaptotagmin I functions as a calcium sensor to synchronize neurotransmitter release. Neuron 36:897-908.
85. Yoshihara M, Suzuki K, Kidokoro Y (2000) Two independent pathways mediated by cAMP and protein kinase A enhance spontaneous transmitter release at Drosophila neuromuscular junctions. J Neurosci 20:8315- 8322.
86. Zhang YQ, Bailey AM, Matthies HJ, Renden RB, Smith MA, Speese SD, Rubin GM, Broadie K (2001) Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107:591-603.
87. Zucker RS (1993) Calcium and transmitter release at nerve terminals. Biochem Soc Trans 21:395-401.
88. Zucker RS (1996) Exocytosis: a molecular and physiological perspective. Neuron 17:1049-1055.