Acetylcholine Increases Intracellular Ca2+ Via Nicotinic Receptors in Cultured PDF-Containing Clock Neurons of Drosophila

Journal of Neurophysiology

Volumn 91, Issue 2, 2004, Pages 912-923

  Wegener, Christian ^a,b   Hamasaka, Yasutaka ^a   Nässel, Dick R ^a,b  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b Animal Physiology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CALCIUM; CALCIUM CHANNEL; CHOLINERGIC RECEPTOR; FURA 2; GREEN FLUORESCENT PROTEIN; MUSCARINIC AGENT; MUSCARINIC RECEPTOR BLOCKING AGENT; NEUROPEPTIDE; NEUROTRANSMITTER; NICOTINIC AGENT; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; PIGMENT DISPERSING FACTOR; RECEPTOR ANTIBODY; RECEPTOR SUBUNIT; SODIUM ION; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; BIOLOGICAL RHYTHM; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EXTRACELLULAR CALCIUM; GENE EXPRESSION; NERVE ENDING; NONHUMAN; PACEMAKER NERVE CELL; PHOTORECEPTOR; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECOND MESSENGER; SIGNAL TRANSDUCTION;

ACETYLCHOLINE; ANIMALS; CALCIUM; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DROSOPHILA; DROSOPHILA PROTEINS; INTRACELLULAR FLUID; NEUROPEPTIDES; NICOTINE; RECEPTORS, NICOTINIC; TRANSCRIPTION FACTORS;

EID: 0842349513     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00678.2003     Document Type: Article

References (79)

1. Aizono Y, Endo Y, Sattelle DB, and Shirai Y. Prothoracicotropic hormone-producing neurosecretory cells in the silkworm, Bombyx mori, express a muscarinic acetylcholine receptor. Brain Res 763: 131-136, 1997.
2. Akiyama M, Minami Y, Nakajima T, Moriya T, and Shibata S. Calcium and pituitary adenylate cylase-activating polypeptide induced expression of circadian clock gene mPerl in the mouse cerebellar granule cell culture. J Neurochem 78: 499-508, 2001.
3. Albert JL and Lingle CJ. Activation of nicotinic acetylcholine receptors on cultured Drosophila and other neurones. J Physiol 463: 605-630, 1993.
4. Atluri P, Fleck MW, Shen Q, Mah SJ, Stadfelt D, Barnes W, Goderie SK, Temple S, and Schneider AS. Functional nicotinic acetylcholine receptor expression in stem and progenitor cells of the early embryonic mouse cerebral cortex. Dev Biol 240: 143-156, 2001.
5. Baines RA and Bacon JP. Pharmacological analysis of the cholinergic input to the locust VPLI neuron from an extraocular photoreceptor system. J Neurophysiol 72: 2864-2874, 1994.
6. Baird GS, Zacharias DA, and Tsien RY. Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc Nat Acad Sci USA 97: 11984-11989, 2000.
7. Berke B and Wu CF. Regional calcium regulation within cultured Drosophila neurons: effects of altered cAMP metabolism by the learning mutations dunce and rutabaga. J Neurosci 22: 4437-4447, 2002.
8. Bicker G and Kreissl S. Calcium imaging reveals nicotinic acetylcholine receptors on cultured mushroom body neurons. J Neurophysiol 71: 808-810, 1994.
9. Bloomquist BT, Shortridge RD, Schneuwly S, Perdew M, Montell C, Steller H, Rubin G, and Pak WL. Isolation of a putative phospholipase gene of Drosophila, norpA, and its role in phototransduction. Cell 54: 723-733, 1988.
10. Bolwig N. Senses and sense organs of the anterior end of the house fly larvae. Videnskab Medd Dansk Naturh Foren 109: 81-217, 1946.
11. Brand A. GFP as a cell and developmental marker in the Drosophila nervous system. Methods Cell Biol 58: 165-181, 1999.
12. Brett WJ. Persistent diurnal rhythmicity in Drosophila emergence. Ann Entomol Soc Am 48: 119-131, 1955.
13. Burrows M. The Neurobiology of an Insect Brain. Oxford, UK: Oxford, 1996.
14. Busto M, Iyengar B, and Campos AR. Genetic dissection of behavior: modulation of locomotion by light in the Drosophila melanogaster larva requires genetically distinct visual system functions. J Neurosci 19: 3337-3344, 1999.
15. Cayre M, Buckingham SD, Yagodin S, and Sattelle DB. Cultured insect mushroom body neurons express functional receptors for acetylcholine, GABA, glutamate, octopamine, and dopamine. J Neurophysiol 81: 1-14, 1999.
16. Chamaon K, Schulz R, Smalla KH, Seidel B, and Gundelfinger ED. Neuronal nicotinic acetylcholine receptors of Drosophila melanogaster: the α-subunit Dα 3 and the β-type subunit ARD co-assemble within the same receptor complex. FEBS Lett 482: 189-192, 2000.
17. Chamaon K, Smalla KH, Thomas U, and Gundelfinger ED. Nicotinic acetylcholine receptors of Drosophila: three subunits encoded by genomically linked genes can co-assemble into the same receptor complex. J Neurochem 80: 149-157, 2002.
18. Colwell CS, Whitmore D, Michel S, and Block GD. Calcium plays a central role in phase shifting the ocular circadian pacemaker of Aplysia. J Comp Physiol A 175: 415-423, 1994.
19. Diegelmann S, Fiala A, Leibold C, Spall T, and Buchner E. Transgenic flies expressing the fluorescence calcium sensor cameleon 2.1 under UAS control. Genesis 34: 95-98, 2002.
20. Dziema H and Obrietan K. PACAP potentiates L-type calcium channel conductance in suprachiasmatic nucleus neurons by activating the MAPK pathway. J Neurophysiol 88: 1374-1386, 2002.
21. Eckert M, Herbert Z, Pollak E, Molnar L, and Predel R. Identical cellular distribution of all abundant neuropeptides in the major abdominal neurohemal system of an insect (Periplaneta americana). J Comp Neurol 452: 264-275, 2002.
22. Emery P, So WV, Kaneko M, Hall JC, and Rosbash M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95: 669-679, 1998.
23. Emery P, Stanewsky R, Helfrich-Förster C, Emery-Le M, Hall JC, and Rosbash M. Drosophila CRY is a deep brain circadian photoreceptor. Neuron 20: 493-503, 2000.
24. Grimmelikhuijzen CJP. FMRFamide is generally occuring in the nervous system of coelenterates. Histochemistry 78: 361-381, 1983.
25. i and regulates electrical activity in insect neurosecretory cells (DUM neurons) via an acetylcholine receptor with "mixed" nicotinic-muscarinic pharmacology. Neurosci Lett 220: 142-146, 1996.
26. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
27. Halfon MS, Gisselbrecht S, Lu J, Estrada B, Keshishian H, and Michelson AM. New fluorescent protein reporters for use with the Drosophila GAL4 expression system and for vital detection of balancer chromosomes. Genesis 34: 135-138, 2002.
28. Harrison JB, Chen HH, Blake AD, Huskisson NS, Barker P, and Sattelle DB. Localization in the nervous system of Drosophila melanogaster of a C-terminus anti-peptide antibody to a cloned Drosophila muscarinic acetylcholine receptor. J Neuroendocrinol 7: 347-352, 1995.
29. Helfrich-Förster C. Development of pigment-dispersing hormone-immunoreactive neurons in the nervous system of Drosophila melanogaster. J Comp Neurol 380: 335-354, 1997.
30. Helfrich-Förster C. The circadian system of Drosophila melanogaster and its light input pathways. Zoology 105: 297-312, 2002.
31. Helfrich-Förster C, Edwards T, Yasuyama K, Wisotzki B, Schneuwly S, Stanewsky R, Meinertzhagen IA, and Hofbauer A. The extraretinal eyelet of Drosophila: development, ultrastructure and putative circadian function. J Neurosci 22: 9255-9266, 2002.
32. Helfrich-Förster C, Winter C, Hofbauer A, Hall JC, and Stanewsky R. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30: 249-261, 2001.
33. Hermsen B, Stetzer E, Thees R, Heiermann R, Schrattenholz A, Ebbinghaus U, Kretschmer A, Methfessel C, Reinhardt S, and Maelicke A. Neuronal nicotinic receptors in the locust Locusta migratoria. J Biol Chem 273: 18394-18404, 1998.
34. Hewes RS, Park D, Gauthier SA, Schaefer AM, and Taghert PM. The bHLH protein dimmed controls neuroendocrine cell differentiation in Drosophila. Development 130: 1771-1781, 2003.
35. Jan LY and Jan YN. Properties of the larval neuromuscular junction in Drosophila melanogoster. J Physiol 262: 189-214, 1976.
36. Jonas P, Phannavong B, Schuster R, Schröder C, and Gundelfinger ED. Expression of the ligand-binding nicotinic acetylcholine receptor subunit Dα 2 in the Drosophila central nervous system. J Neurobiol 25: 1494-1508, 1994.
37. Kaneko M and Hall JC. Neuroanatomy of cells expressing clock genes in Drosophila: transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J Comp Neurol 422: 66-94, 2000.
38. short mutation on phase shifts induced by light pulses delivered to Drosophila larvae. J Biol Rhythms 15: 13-30, 2000.
39. Kaneko M, Helfrich-Förster C, and Hall JC. Spatial and temporal expression of the period and timeless genes in the developing nervous system of Drosophila: newly identified pacemaker candidates and novel features of clock gene product cycling. J Neurosci 17: 6745-6760, 1997.
40. Kitamoto T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47: 81-92, 2001.
41. Kopp MDA, Schomerus C, Dehghani F, Korf HW, and Meissl H. Pituitary adenylate cyclase-activating polypeptide and melatonin in the suprachiasmatic nucleus: effects on the calcium signal transduction cascade. J Neurosci 19: 206-219, 1999.
42. Kraft R, Levine RB, and Restifo LL. The steroid hormone 20-hydroxyecdysone enhances neurite growth of Drosophila mushroom body neurons isolated during metamorphosis. J Neurosci 18: 8886-8899, 1998.
43. Lee D and O'Dowd DK. Fast excitatory synaptic transmission mediated by nicotinic acetylcholine receptors in Drosophila neurons. J Neurosci 19: 5311-5321, 1999.
44. Lee T and Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-461, 1999.
45. Lundquist CT, Baines RA, Thompson KSJ, and Bacon JP. Differential regulation of a homologous peptidergic neuron in grasshoppers: evolution of a neural circuit. J Comp Physiol A 182: 755-765, 1998.
46. Malpel S, Klarsfeld A, and Rouyer F. Larval optic nerve and adult extraretinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. Development 129: 1443-1453, 2002.
47. McMahon DG and Block GD. The Bulla ocular circadian pacemaker. I. Pacemaker neuron membrane potential controls phase through a calcium-dependent mechanism. J Comp Physiol A 161: 335-346, 1987.
48. Messutat S, Heine M, and Wicher D. Calcium-induced calcium release in neurosecretory insect neurons: fast and slow responses. Cell Calcium 30: 199-211, 2001.
49. Millar NS, Baylis HA, Reaper C, Bunting R, Mason WT, and Sattelle DB. Functional expression of a cloned Drosophila muscarinic acetylcholine receptor in a stable Drosophila cell line. J Exp Biol 198: 1843-1850, 1995.
50. Nässel DR. Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Progr Neurobiol 68: 1-84, 2002.
51. Nässel DR, Ohlsson L, and Sivasubramanian P. Postembryonic differentiation of serotonin-immunoreactive neurons in fleshfly optic lobes developing in situ or cultured in vivo without eye discs. J Comp Neurol 255: 327-340, 1987.
52. Nitabach MN, Blau J, and Holmes TC. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109: 485-495, 2002.
53. Park JH, Helfrich-Förster C, Lee G, Liu L, Rosbash M, and Hall JC. Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Nat Acad Sci USA 97: 3608-3613, 2000.
54. Persson MGS, Eklund MB, Dircksen H, Muren JE, and Nässel DR. Pigment-dispersing factor in the locust abdominal ganglia may have roles as circulating neurohormone and central neuromodulator. J Neurobiol 48: 19-41, 2001.
55. Petri B, Homberg U, Loesel R, and Stengl M. Evidence for a role of GABA and Mas-allatotropin in photic entrainment of the circadian clock of the cockroach Leucophaea maderae. J Exp Biol 205: 1459-1469, 2002.
56. Quick MW and Lester RAJ. Desensitization of neuronal nicotinic receptors. J Neurobiol 53: 457-478, 2002.
57. Reppert SM and Weaver DR. Coordination of circadian timing in mammals. Nature 418: 935-941, 2002.
58. Rohrbough J, O'Dowd DK, Baines RA, and Broadie K. Cellular bases of behavioral plasticity: establishing and modifiying synaptic circuits in the Drosophila genetic system. J Neurobiol 54: 254-271, 2003.
59. Sacchetti A, Subramaniam V, Jovin TM, and Alberti S. Oligomerization of DsRed is required for the generation of a functional red fluorescent chromophore. FEBS Lett 525: 13-19, 2002.
60. Sawin EP, Dowse HB, Hamblen-Coyle MJ, Hall JC, and Sokolowski MB. A lack of locomotor activity rhythms in Drosophila melanogaster larvae (Diptera: Drosophilidae). J Insect Behav 7: 249-262, 1994.
61. Schurov IL, McNulty S, Best JD, Sloper PJ, and Hastings MH. Glutamatergic induction of CREB phosphorylation and Fos expression in primary cultures of the suprachiasmatic hypothalamus in vitro is mediated by coordinate activity of NMDA and non-NMDA receptors. J Neuroendocrinol 11: 43-51, 1999.
62. Schuster R, Pannavong B, Schröder C, and Gundelfinger ED. Immunohistochemical localization of a ligand-binding and a structural subunit of nicotinic acetylcholine receptors in the central nervous system of Drosophila melanogaster. J Comp Neurol 335: 149-162, 1993.
63. Sehgal A, Price J, and Young MW. Ontogeny of a biological clock in Drosophila melanogaster. Proc Nat Acad Sci USA 89: 1423-1427, 1992.
64. Shirai Y, Jiang Y, Yoshioka S, and Aizono Y. The release of an insect neuropeptide hormone, bombyxin, is regulated by muscarinic transmission in the brain-corpus cardiacum-corpus allatum complex of the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Appl Entomol Zool 36: 431-438, 2001.
65. b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95: 681-692, 1998.
66. Suri V, Qian Z, Hall JC, and Rosbash M. Evidence that the TIM light response is relevant to light-induced phase shifts in Drosophila melanogaster. Neuron 21: 225-234, 1998.
67. 2+/calmodulin-dependent protein kinase II promoter. Cell Tissue Res 310: 237-252, 2002.
68. Wang JW, Wong AM, Flores J, Vosshall LB, and Axel R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112: 271-282, 2003.
69. Williams DA and Fay FS. Intracellular calibration of the fluorescent calcium indicator Fura-2. Cell Calcium 11: 75-83, 1990.
70. Wu CF, Suzuki N, and Poo MM. Dissociated neurons from normal and mutant Drosophila larval central nervous system in cell culture. J Neurosci 3: 1888-1899, 1983.
71. Yang Z, Emerson M, Su HS, and Sehgal A. Response of the timeless protein to light correlates with behavioral entrainment and suggests a nonvisual pathway for circadian photoreception. Neuron 21: 215-223, 1998.
72. Yasuyama K, Kitamoto T, and Salvaterra PM. Localization of choline acetyltransferase-expressing neurons in the larval visual system of Drosophila melanogaster. Cell Tissue Res 282: 193-202, 1995.
73. Yasuyama K and Meinertzhagen IA. Extraretinal photoreceptors at the compound eye's posterior margin in Drosophila melanogaster. J Comp Neurol 412: 193-202, 1999.
74. Yasuyama K and Salvaterra PM. Localization of choline acetyltransferase-expressing neurons in Drosophila nervous system. Microsc Res Technique 45: 65-79, 1999.
75. Yu D, Baird GS, Tsien RY, and Davis RL. Detection of calcium transients in Drosophila mushroom body neurons with camgaroo reporters. J Neurosci 23: 64-72, 2003.
76. Yuste R, Lanni F, and Konnerth A. Imaging Neurons - A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2000.
77. Zarei MM, Radcliffe KA, Chen D, Patrick JW, and Dani JA. Distributions of nicotinic acetylcholine receptor α 7 and β 2 subunits on cultured hippocampal neurons. Neuroscience 88: 755-764, 1999.
78. Zordan M, Osterwalder N, Rosato E, and Costa R. Extra-ocular photic entrainment in Drosophila melanogaster. J Neurogenetics 15: 97-116, 2001a.
79. Zordan M, Rosato E, Piccin A, and Foster R. Photic entrainment of the circadian clock: from Drosophila to mammals. Sem Cell Devel Biol 12: 317-328, 2001b.