Pre- and post-synaptic mechanisms of synaptic strength homeostasis revealed by slowpoke and shaker K+ channel mutations in Drosophila

Neuroscience

Volumn 154, Issue 4, 2008, Pages 1283-1296

  Lee, J ^a   Ueda, A ^a   Wu, C F ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

cAMP; dorsal ventral differentials; membrane excitability; postsynaptic receptor composition; rutabaga adenylyl cyclase; synaptic strength

Indexed keywords

4 AMINOPYRIDINE; ADENYLATE CYCLASE; BYSLOWPOKE POTASSIUM CHANNEL; MUTANT PROTEIN; POTASSIUM CHANNEL; RECEPTOR SUBUNIT; SHAKER POTASSIUM CHANNEL;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; EXCITATORY JUNCTION POTENTIAL; HOMEOSTASIS; IMMUNOREACTIVITY; NAEGLERIA GRUBERI; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SYNAPTIC TRANSMISSION;

ADENYLATE CYCLASE; ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; ELECTROPHYSIOLOGY; HOMEOSTASIS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MICROSCOPY, CONFOCAL; NEUROMUSCULAR JUNCTION; NEURONAL PLASTICITY; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 45849105926     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.04.043     Document Type: Article

References (82)

1. Armstrong C.M. Voltage-gated K channels. Sci STKE 2003 (2003) re10
2. Atkinson N.S., Robertson G.A., and Ganetzky B. A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science 253 (1991) 551-555
3. Atwood H.L., Govind C.K., and Wu C.F. Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol 24 (1993) 1008-1024
4. Barnes-Davies M., Barker M.C., Osmani F., and Forsythe I.D. Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur J Neurosci 19 (2004) 325-333
5. Bastiani M.J., Harrelson A.L., Snow P.M., and Goodman C.S. Expression of fasciclin I and II glycoproteins on subsets of axon pathways during neuronal development in the grasshopper. Cell 48 (1987) 745-755
6. + channels: regulation of the soma-growth cone disparity and the quiescent state in Drosophila neurons. Neuroscience 142 (2006) 629-644
7. Bhattacharya A., Gu G.G., and Singh S. Modulation of dihydropyridine-sensitive calcium channels in Drosophila by a cAMP-mediated pathway. J Neurobiol 39 (1999) 491-500
8. Budnik V., Koh Y.H., Guan B., Hartmann B., Hough C., Woods D., and Gorczyca M. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 17 (1996) 627-640
9. Budnik V., Zhong Y., and Wu C.F. Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J Neurosci 10 (1990) 3754-3768
10. Byers D., Davis R.L., and Kiger Jr. J.A. Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature 289 (1981) 79-81
11. + current systems. Neuron 7 (1991) 763-773
12. Davis G.W., DiAntonio A., Petersen S.A., and Goodman C.S. Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron 20 (1998) 305-315
13. Davis G.W., Schuster C.M., and Goodman C.S. Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron 17 (1996) 669-679
14. DiAntonio A., Petersen S.A., Heckmann M., and Goodman C.S. Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. J Neurosci 19 (1999) 3023-3032
15. Dudai Y., Jan Y.N., Byers D., Quinn W.G., and Benzer S. Dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci U S A 73 (1976) 1684-1688
16. Dudai Y., Uzzan A., and Zvi S. Abnormal activity of adenylate cyclase in the Drosophila memory mutant rutabaga. Neurosci Lett 42 (1983) 207-212
17. 2+ sensitivity. Neurosci Lett 47 (1984) 119-124
18. + channel modulated by a functionally associated protein kinase. Nature 369 (1994) 563-565
19. V2.1 mutations. Brain Res 1140 (2007) 105-119
20. Featherstone D.E., Rushton E., Rohrbough J., Liebl F., Karr J., Sheng Q., Rodesch C.K., and Broadie K. An essential Drosophila glutamate receptor subunit that functions in both central neuropil and neuromuscular junction. J Neurosci 25 (2005) 3199-3208
21. Feng Y., Ueda A., and Wu C.F. A modified minimal hemolymph-like solution, HL3.1, for physiological recordings at the neuromuscular junctions of normal and mutant Drosophila larvae. J Neurogenet 18 (2004) 377-402
22. Ferguson G.D., and Storm D.R. Why calcium-stimulated adenylyl cyclases?. Physiology (Bethesda) 19 (2004) 271-276
23. Fettiplace R., and Fuchs P.A. Mechanisms of hair cell tuning. Annu Rev Physiol 61 (1999) 809-834
24. Fukui I., and Ohmori H. Tonotopic gradients of membrane and synaptic properties for neurons of the chicken nucleus magnocellularis. J Neurosci 24 (2004) 7514-7523
25. Ganetzky B., and Wu C.F. Neurogenetic analysis of potassium currents in Drosophila: synergistic effects on neuromuscular transmission in double mutants. J Neurogenet 1 (1983) 17-28
26. Gho M., and Ganetzky B. Analysis of repolarization of presynaptic motor terminals in Drosophila larvae using potassium-channel-blocking drugs and mutations. J Exp Biol 170 (1992) 93-111
27. Gielow M.L., Gu G.G., and Singh S. Resolution and pharmacological analysis of the voltage-dependent calcium channels of Drosophila larval muscles. J Neurosci 15 (1995) 6085-6093
28. Griffith L.C., Verselis L.M., Aitken K.M., Kyriacou C.P., Danho W., and Greenspan R.J. Inhibition of calcium/calmodulin-dependent protein kinase in Drosophila disrupts behavioral plasticity. Neuron 10 (1993) 501-509
29. Jan L.Y., and Jan Y.N. Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc Natl Acad Sci U S A 79 (1982) 2700-2704
30. Jan Y.N., Jan L.Y., and Dennis M.J. Two mutations of synaptic transmission in Drosophila. Proc R Soc Lond B Biol Sci 198 (1977) 87-108
31. Jin P., Griffith L.C., and Murphey R.K. Presynaptic calcium/calmodulin-dependent protein kinase II regulates habituation of a simple reflex in adult Drosophila. J Neurosci 18 (1998) 8955-8964
32. Johansen J., Halpern M.E., Johansen K.M., and Keshishian H. Stereotypic morphology of glutamatergic synapses on identified muscle cells of Drosophila larvae. J Neurosci 9 (1989) 710-725
33. Jonas E.A., and Kaczmarek L.K. Regulation of potassium channels by protein kinases. Curr Opin Neurobiol 6 (1996) 318-323
34. Kamb A., Iverson L.E., and Tanouye M.A. Molecular characterization of Shaker, a Drosophila gene that encodes a potassium channel. Cell 50 (1987) 405-413
35. Kawasaki F., Felling R., and Ordway R.W. A temperature-sensitive paralytic mutant defines a primary synaptic calcium channel in Drosophila. J Neurosci 20 (2000) 4885-4889
36. Keene A.C., and Waddell S. Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci 8 (2007) 341-354
37. Lahey T., Gorczyca M., Jia X.X., and Budnik V. The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13 (1994) 823-835
38. Landgraf M., Bossing T., Technau G.M., and Bate M. The origin, location, and projections of the embryonic abdominal motorneurons of Drosophila. J Neurosci 17 (1997) 9642-9655
39. Livingstone M.S., Sziber P.P., and Quinn W.G. Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell 37 (1984) 205-215
40. MacLean J.N., Zhang Y., Johnson B.R., and Harris-Warrick R.M. Activity-independent homeostasis in rhythmically active neurons. Neuron 37 (2003) 109-120
41. Marder E., and Goaillard J.M. Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci 7 (2006) 563-574
42. 2+ channels in hippocampal neurons. Nature 395 (1998) 900-905
43. Marrus S.B., Portman S.L., Allen M.J., Moffat K.G., and DiAntonio A. Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J Neurosci 24 (2004) 1406-1415
44. Martin A.R. A further study of the statistical composition on the end-plate potential. J Physiol 130 (1955) 114-122
45. Nguyen P.V., and Woo N.H. Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 71 (2003) 401-437
46. O'Brien R.J., Kamboj S., Ehlers M.D., Rosen K.R., Fischbach G.D., and Huganir R.L. Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 21 (1998) 1067-1078
47. Papazian D.M., Schwarz T.L., Tempel B.L., Jan Y.N., and Jan L.Y. Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science 237 (1987) 749-753
48. Paradis S., Sweeney S.T., and Davis G.W. Homeostatic control of presynaptic release is triggered by postsynaptic membrane depolarization. Neuron 30 (2001) 737-749
49. Park D., Coleman M.J., Hodge J.J., Budnik V., and Griffith L.C. Regulation of neuronal excitability in Drosophila by constitutively active CaMKII. J Neurobiol 52 (2002) 24-42
50. + channel homeostatic regulation. J Neurosci 27 (2007) 1072-1081
51. Petersen S.A., Fetter R.D., Noordermeer J.N., Goodman C.S., and DiAntonio A. Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 19 (1997) 1237-1248
52. Qin G., Schwarz T., Kittel R.J., Schmid A., Rasse T.M., Kappei D., Ponimaskin E., Heckmann M., and Sigrist S.J. Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila. J Neurosci 25 (2005) 3209-3218
53. Renger J.J., Ueda A., Atwood H.L., Govind C.K., and Wu C.F. Role of cAMP cascade in synaptic stability and plasticity: ultrastructural and physiological analyses of individual synaptic boutons in Drosophila memory mutants. J Neurosci 20 (2000) 3980-3992
54. Rieckhof G.E., Yoshihara M., Guan Z., and Littleton J.T. Presynaptic N-type calcium channels regulate synaptic growth. J Biol Chem 278 (2003) 41099-41108
55. Robitaille R., Garcia M.L., Kaczorowski G.J., and Charlton M.P. Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release. Neuron 11 (1993) 645-655
56. Salkoff L., Butler A., Ferreira G., Santi C., and Wei A. High-conductance potassium channels of the SLO family. Nat Rev Neurosci 7 (2006) 921-931
57. Schuster C.M., Davis G.W., Fetter R.D., and Goodman C.S. Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron 17 (1996) 641-654
58. Schuster C.M., Davis G.W., Fetter R.D., and Goodman C.S. Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17 (1996) 655-667
59. Schuster C.M., Ultsch A., Schloss P., Cox J.A., Schmitt B., and Betz H. Molecular cloning of an invertebrate glutamate receptor subunit expressed in Drosophila muscle. Science 254 (1991) 112-114
60. Sigrist S.J., Reiff D.F., Thiel P.R., Steinert J.R., and Schuster C.M. Experience-dependent strengthening of Drosophila neuromuscular junctions. J Neurosci 23 (2003) 6546-6556
61. Smith L.A., Wang X., Peixoto A.A., Neumann E.K., Hall L.M., and Hall J.C. A Drosophila calcium channel alpha1 subunit gene maps to a genetic locus associated with behavioral and visual defects. J Neurosci 16 (1996) 7868-7879
62. Stewart B.A., Atwood H.L., Renger J.J., Wang J., and Wu C.F. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol [A] 175 (1994) 179-191
63. Stewart B.A., Schuster C.M., Goodman C.S., and Atwood H.L. Homeostasis of synaptic transmission in Drosophila with genetically altered nerve terminal morphology. J Neurosci 16 (1996) 3877-3886
64. Tanouye M.A., and Ferrus A. Action potentials in normal and Shaker mutant Drosophila. J Neurogenet 2 (1985) 253-271
65. Tanouye M.A., Ferrus A., and Fujita S.C. Abnormal action potentials associated with the Shaker complex locus of Drosophila. Proc Natl Acad Sci U S A 78 (1981) 6548-6552
66. + channels in vivo. J Neurosci 17 (1997) 152-159
67. Thomas U., Kim E., Kuhlendahl S., Koh Y.H., Gundelfinger E.D., Sheng M., Garner C.C., and Budnik V. Synaptic clustering of the cell adhesion molecule fasciclin II by discs-large and its role in the regulation of presynaptic structure. Neuron 19 (1997) 787-799
68. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., and Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391 (1998) 892-896
69. Ueda A, Wu CF (2003) Reduced synaptic strength and increased variability of axonal terminal branches in Drosophila memory mutants: presynaptic ionic mechanisms. Program No 457.12 2003 Abstract Viewer/Itinerary Planner Washington, DC: Society for Neuroscience, 2003 Online.
70. K potassium channels revealed by Drosophila Shaker and Shab mutations. J Neurosci 26 (2006) 6238-6248
71. Wang J., Renger J.J., Griffith L.C., Greenspan R.J., and Wu C.F. Concomitant alterations of physiological and developmental plasticity in Drosophila CaM kinase II-inhibited synapses. Neuron 13 (1994) 1373-1384
72. + channel gene of Drosophila. Invert Neurosci 2 (1996) 51-60
73. Wu C.F., Ganetzky B., Haugland F.N., and Liu A.X. Potassium currents in Drosophila: different components affected by mutations of two genes. Science 220 (1983) 1076-1078
74. + currents in Drosophila neurons. J Neurophysiol 85 (2001) 1384-1394
75. Yazejian B., DiGregorio D.A., Vergara J.L., Poage R.E., Meriney S.D., and Grinnell A.D. Direct measurements of presynaptic calcium and calcium-activated potassium currents regulating neurotransmitter release at cultured Xenopus nerve-muscle synapses. J Neurosci 17 (1997) 2990-3001
76. Zhao M.L., and Wu C.F. Alterations in frequency coding and activity dependence of excitability in cultured neurons of Drosophila memory mutants. J Neurosci 17 (1997) 2187-2199
77. Zheng W., Feng G., Ren D., Eberl D.F., Hannan F., Dubald M., and Hall L.M. Cloning and characterization of a calcium channel alpha 1 subunit from Drosophila melanogaster with similarity to the rat brain type D isoform. J Neurosci 15 (1995) 1132-1143
78. Zhong Y., Budnik V., and Wu C.F. Synaptic plasticity in Drosophila memory and hyperexcitable mutants: role of cAMP cascade. J Neurosci 12 (1992) 644-651
79. Zhong Y., and Wu C.F. Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science 251 (1991) 198-201
80. Zhong Y., and Wu C.F. Differential modulation of potassium currents by cAMP and its long-term and short-term effects: dunce and rutabaga mutants of Drosophila. J Neurogenet 9 (1993) 15-27
81. Zhong Y., and Wu C.F. Neuronal activity and adenylyl cyclase in environment-dependent plasticity of axonal outgrowth in Drosophila. J Neurosci 24 (2004) 1439-1445
82. Zito K., Fetter R.D., Goodman C.S., and Isacoff E.Y. Synaptic clustering of Fascilin II and Shaker: essential targeting sequences and role of Dlg. Neuron 19 (1997) 1007-1016