Reciprocal cholinergic and GABAergic modulation of the small ventrolateral pacemaker neurons of Drosophila's circadian clock neuron network

Journal of Neurophysiology

Volumn 107, Issue 8, 2012, Pages 2096-2108

  Lelito, Katherine R ^a   Shafer, Orie T ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Adenosine 3 ,5 cyclic monophosphate; Epac1 camps; GCaMP; Live imaging

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; CALCIUM ION; CARBACHOL; CYCLIC AMP; GREEN FLUORESCENT PROTEIN; MUSCARINIC RECEPTOR; NICOTINE; NICOTINIC RECEPTOR; PILOCARPINE; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL LEVEL; CHOLINERGIC STIMULATION; CHOLINERGIC TRANSMISSION; CIRCADIAN CLOCK NERVE CELL NETWORK; CIRCADIAN RHYTHM; CONCENTRATION RESPONSE; CONTROLLED STUDY; DROSOPHILA; FLUORESCENCE ANALYSIS; GABAERGIC TRANSMISSION; LARGE VENTROLATERAL PACEMAKER NERVE CELL; MALE; NERVE CELL NETWORK; NERVE CELL STIMULATION; NEUROMODULATION; NONHUMAN; PACEMAKER NERVE CELL; PRIORITY JOURNAL; SMALL VENTROLATERAL PACEMAKER NERVE CELL;

ANIMALS; CHOLINERGIC AGENTS; CHOLINERGIC NEURONS; CIRCADIAN CLOCKS; DROSOPHILA MELANOGASTER; GABA MODULATORS; GABAERGIC NEURONS; MALE; NERVE NET; NEURONS;

EID: 84859755880     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00931.2011     Document Type: Article

References (72)

1. Albus H, Vansteensel MJ, Michel S, Block GD, Meijer JH. A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol 15: 886-893, 2005.
2. Arble DM, Ramsey KM, Bass J, Turek FW. Circadian disruption and metabolic disease: findings from animal models. Best Pract Res Clin Endocrinol Metab 24: 785-800, 2010.
3. Aschoff J. Biological Rhythms. New York: Plenum, 1981.
4. B receptors. Physiol Rev 84: 835-867, 2004.
5. Börner S, Schwede F, Schlipp A, Berisha F, Calebiro D, Lohse MJ, Nikolaev VO. FRET measurements of intracellular cAMP concentrations and cAMP analog permeabilityinintact cells. NatProtoc 6: 427-438, 2011.
6. Brotz TM, Egelhaaf M, Borst A. A preparation of the blowfly (Calliphora erythrocephala) brain for in vitro electrophysiological and pharmacological studies. J Neurosci Methods 57: 37-46, 1995.
7. Buchner E, Buchner S, Crawford G, Mason WT, Salvaterra PM, Sattelle DB. Choline acetyltransferase-like immunoreactivity in the brain of Drosophila melanogaster. Cell Tissue Res 246: 57-62, 1986.
8. Cao G, Nitabach MN. Circadian control of membrane excitability in Drosophila melanogaster lateral ventral clock neurons. J Neurosci 28: 6493-6501, 2008.
9. Challet E. Minireview: entrainment of the suprachiasmatic clockwork in diurnal and nocturnal mammals. Endocrinology 148: 5648-5655, 2007.
10. A receptor RDL acts in peptidergic PDF neurons to promote sleep in Drosophila. Curr Biol 19: 386-390, 2009.
11. Dahdal D, Reeves DC, Ruben M, Akabas MH, Blau J. Drosophila pacemaker neurons require G protein signaling and GABAergic inputs to generate twenty-four hour behavioral rhythms. Neuron 68: 964-977, 2010.
12. o signaling is required for Drosophila associative learning. Nat Neurosci 9: 1036-1040, 2006.
13. Fogle KJ, Parson KG, Dahm NA, Holmes TC. CRYPTOCHROME is a blue-light sensor that regulates neuronal firing rate. Science 331: 1409-1413, 2011.
14. Foster FRG. A sense of time: body clocks, sleep and health. Dtsch Med Wochenschr 135: 2601-2608, 2010.
15. Golombek DA, Rosenstein RE. Physiology of circadian entrainment. Physiol Rev 90: 1063-1102, 2009.
16. Gorczyca M, Hall J. Immunohistochemical localization of choline acetyl- transferase during development and in Chats mutants of Drosophila mela- nogaster. J Neurosci 7: 1361-1369, 1987.
17. Grima B, Chelot E, Xia R, Rouyer F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431: 869-873, 2004.
18. Hamasaka Y, Rieger D, Parmentier ML, Grau Y, Helfrich-Förster C, Nässel DR. Glutamate and its metabotropic receptor in Drosophila clock neuron circuits. J Comp Neurol 505: 32-45, 2007.
19. Hamasaka Y, Wegener C, Nässel DR. GABA modulates Drosophila circadian clock neurons via GABAb receptors and decreases in calcium. J Neurobiol 65: 225-240, 2005.
20. Helfrich-Förster C. Development of pigment-dispersing hormone-immuno- reactive neurons in the nervous system of Drosophila melanogaster. J Comp Neurol 380: 335-354, 1997.
21. Helfrich-Förster C. The circadian clock in the brain: a structural and functional comparison between mammals and insects. J Comp Physiol A 190: 601-613, 2004.
22. Helfrich-Förster C. The circadian system of Drosophila melanogaster and its light input pathways. Zoology 105: 297-312, 2002.
23. Helfrich-Förster C, Edwards T, Yasuyama K, Wisotzki B, Schneuwly S, Stanewsky R, Meinertzhagen IA, Hofbauer A. The extraretinal eyelet of Drosophila: development, ultrastructure, and putative circadian function. J Neurosci 22: 9255-9266, 2002.
24. Helfrich-Förster C, Shafer OT, Wülbeck C, Grieshaber E, Rieger D, Taghert P. Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J Comp Neurol 500: 47-70, 2007.
25. Helfrich-Förster C, Winter C, Hofbauer A, Hall JC, Stanewsky R. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30: 249-261, 2001.
26. Herzog ED. Neurons and networks in daily rhythms. Nat Rev Neurosci 8: 790-802, 2007.
27. Ignell R, Root CM, Birse RT, Wang JW, Nässel DR, Winther ÂME. Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc Natl Acad Sci USA 106: 13070-13075, 2009.
28. 2+ responses in the suprachiasmatic nucleus network. Eur J Neurosci 30: 1462-1475, 2009.
29. Kaneko M, 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.
30. Kaneko M, Helfrich-Förster C, 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.
31. Klarsfeld A, Malpel S, Michard-Vanhée C, Picot M, Chélot E, Rouyer F. Novel features of cryptochrome-mediated photoreception in the brain circadian clock of Drosophila. J Neurosci 24: 1468-1477, 2004.
32. Küppers B, Sánchez-Soriano N, Letzkus J, Technau GM, Prokop A. In developing Drosophila neurones the production of γ-amino butyric acid is tightly regulated downstream of glutamate decarboxylase translation and can be influenced by calcium. J Neurochem 84: 939-951, 2003.
33. Levine JD, Casey CI, Kalderon DD, Jackson FR. Altered circadian pacemaker functions and cyclic AMP rhythms in the Drosophila learning mutant dunce. Neuron 13: 967-974, 1994.
34. Lin Y, Stormo GD, Taghert PH. The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J Neurosci 24: 7951-7957, 2004.
35. Liu C, Reppert SM. GABA synchronizes clock cells within the suprachias- matic circadian clock. Neuron 25: 123-128, 2000.
36. Malpel S, Klarsfeld A, Rouyer F. Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. Development 129: 1443-1453, 2002.
37. Markova O, Mukhtarov M, Real E, Jacob Y, Bregestovski P. Genetically encoded chloride indicator with improved sensitivity. J Neurosci Methods 170: 67-76, 2008.
38. McCarthy EV, Wu Y, deCarvalho T, Brandt C, Cao G, Nitabach MN. Synchronized bilateral synaptic inputs to Drosophila melanogaster neuro- peptidergic rest/arousal neurons. J Neurosci 31: 8181-8193, 2011.
39. B receptors from Drosophila. Eur J Neurosci 13: 477-486, 2001.
40. Nässel DR. Neurotransmitters and neuromodulators in the insect visual system. Prog Neurobiol 37: 179-254, 1991.
41. Nikolaev VO, Bünemann M, Hein L, Hannawacker A, Lohse MJ. Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 279: 37215-37218, 2004.
42. O'Neill JS, Maywood ES, Chesham JE, Takahashi JS, Hastings MH. cAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 320: 949-953, 2008.
43. Parisky KM, Agosto J, Pulver SR, Shang Y, Kuklin E, Hodge JJL, Kang K, Liu X, Garrity PA, Rosbash M, Griffith LC. PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60: 672-682, 2008.
44. Park D, Griffith LC. Electrophysiological and anatomical characterization of PDF-positive clock neurons in the intact adult Drosophila brain. J Neurophysiol 95: 3955-3960, 2006.
45. Peng Y, Stoleru D, Levine JD, Hall JC, Rosbash M. Drosophila free- running rhythms require intercellular communication. PLoS Biol 1: e13, 2003.
46. Petri B, Homberg U, Loesel R, 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.
47. Picot M, Cusumano P, Klarsfeld A, Ueda R, Rouyer F. Light activates output from evening neurons and inhibits output from morning neurons in the Drosophila circadian clock. PLoS Biol 5: e315, 2007.
48. Renn SCP, Park JH, Rosbash M, Hall JC, Taghert PH. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99: 791-802, 1999.
49. Rieger D, Shafer OT, Tomioka K, Helfrich-Forster C. Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. JNeurosci 26: 2531-2543, 2006.
50. Rieger D, Stanewsky R, Helfrich-Forster C. Cryptochrome, compound eyes, Hofbauer-Buchner eyelets, and ocelli play different roles in the entrainment and masking pathway of the locomotor activity rhythm in the fruit fly Drosophila melanogaster. J Biol Rhythms 18: 377-391, 2003.
51. Schwartz JRL, Roth T. Shift work sleep disorder: burden of illness and approaches to management. Drugs 66: 2357-2370, 2006.
52. Sehadova H, Glaser FT, Gentile C, Simoni A, Giesecke A, Albert JT, Stanewsky R. Temperature entrainment of Drosophila s circadian clock involves the gene nocte and signaling from peripheral sensory tissues to the brain. Neuron 64: 251-266, 2009.
53. Shafer OT, Helfrich-Forster C, Renn SCP, Taghert PH. Reevaluation of Drosophila melanogaster s neuronal circadian pacemakers reveals new neuronal classes. J Comp Neurol 498: 180-193, 2006.
54. Shafer OT, Kim DJ, Dunbar-Yaffe R, Nikolaev VO, Lohse MJ, Taghert PH. Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58: 223-237, 2008.
55. Shafer OT, Taghert PH. RNA-interference knockdown of Drosophila pigment dispersing factor in neuronal subsets: the anatomical basis of a neuropeptide s circadian functions. PLoS One 4: e8298, 2009.
56. Shakiryanova D, Levitan ES. Prolonged presynaptic posttetanic cyclic GMP signaling in Drosophila motoneurons. Proc Natl Acad Sci USA 105: 13610-13613, 2008.
57. Shang Y, Griffith L, Rosbash M. Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc Natl Acad Sci USA 105: 19587-19594, 2008.
58. Shang Y, Haynes P, Pirez N, Harrington KI, Guo F, Pollack J, Hong P, Griffith LC, Rosbash M. Imaging analysis of clock neurons reveals light buffers the wake-promoting effect of dopamine. Nat Neurosci 14: 889-895, 2011.
59. Sheeba V, Fogle KJ, Kaneko M, Rashid S, Chou YT, Sharma VK, Holmes TC. Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr Biol 18: 1537-1545, 2008a.
60. Sheeba V, Gu H, Sharma VK, O'Dowd DK, Holmes TC. Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. J Neurophysiol 99: 976-988, 2008b.
61. Soderlund DM. Sodium channels. In: Comprehensive Molecular Insect Science, edited by Gilbert LI, Latrou K, Gill SS. Amsterdam: Elsevier, 2005.
62. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol A 175: 179-191, 1994.
63. Stoleru D, Peng Y, Agosto J, Rosbash M. Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431: 862-868, 2004.
64. Stoleru D, Peng Y, Nawathean P, Rosbash M. A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 438: 238-242, 2005.
65. Sullivan W, Ashburner M, Hawley RS. Drosophila Protocols. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2000, p. xiv.
66. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayara-man V, Svoboda K, Looger LL. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6: 875-881, 2009.
67. Treherne JE, Smith DS. The metabolism of acetylcholine in the intact central nervous system of an insect (Periplaneta americana L.). J Exp Biol 43: 441-454, 1965a.
68. Treherne JE, Smith DS. The penetration of acetylcholine into the central nervous tissues of an insect (Periplaneta americana L.). J Exp Biol 43: 13-21, 1965b.
69. Waseem T, Mukhtarov M, Buldakova S, Medina I, Bregestovski P. Genetically encoded Cl-Sensor as a tool for monitoring of Cl-dependent processes in small neuronal compartments. J Neurosci Methods 193: 14-23, 2010.
70. 2+ via nicotinic receptors in cultured PDF-containing clock neurons of Drosophila. J Neurophysiol 91: 912-923, 2004.
71. Yasuyama K, Meinertzhagen IA. Extraretinal photoreceptors at the compound eye s posterior margin in Drosophila melanogaster. J Comp Neurol 412: 193-202, 1999.
72. Yoshii T, Wülbeck C, Sehadova H, Veleri S, Bichler D, Stanewsky R, Helfrich-Förster C. The neuropeptide pigment-dispersing factor adjusts period and phase of Drosophila s clock. J Neurosci 29: 2597-2610, 2009.