Organization of the Drosophila Circadian Control Circuit

Current Biology

Volumn 18, Issue 2, 2008, Pages

  Nitabach, Michael N ^a   Taghert, Paul H ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; GLUTAMIC ACID; NEUROPEPTIDE; NEUROPEPTIDE F; NPLP1 PROTEIN, DROSOPHILA; PDF PROTEIN, DROSOPHILA; UNCLASSIFIED DRUG;

ANIMAL; BIOLOGICAL RHYTHM; BRAIN; CIRCADIAN RHYTHM; CYTOLOGY; DROSOPHILA MELANOGASTER; ENVIRONMENT; LIGHT; LOCOMOTION; METABOLISM; PHYSIOLOGY; REVIEW; TEMPERATURE;

ANIMALS; BIOLOGICAL CLOCKS; BRAIN; CIRCADIAN RHYTHM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENVIRONMENT; GLUTAMIC ACID; LIGHT; LOCOMOTION; NEUROPEPTIDES; TEMPERATURE;

EID: 38149026267     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2007.11.061     Document Type: Review

References (101)

1. Hall J.C. Systems approaches to biological rhythms in Drosophila. Methods Enzymol. 393 (2005) 61-185
2. Taghert P.H., and Lin Y. Tick-talk: The cellular and molecular biology of Drosophila circadian rhythms. In: Gilbert L.I., Iatrou K., and Gill S.S. (Eds). Comprehensive Molecular Insect Science vol 4 (2005), Elsevier BV 357-395
3. Claridge-Chang A., Wijnen H., Naef F., Boothroyd C., Rajewsky N., and Young M.W. Circadian regulation of gene expression systems in the Drosophila head. Neuron 32 (2001) 657-671
4. McDonald M.J., and Rosbash M. Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107 (2001) 567-578
5. Ceriani M.F., Hogenesch J.B., Yanovsky M., Panda S., Straume M., and Kay S.A. Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. J. Neurosci. 22 (2002) 9305-9319
6. Lin Y., Han M., Shimada B., Wang L., Gibler T.M., Amarakone A., Awad T.A., Stormo G.D., Van Gelder R.N., and Taghert P.H. Influence of the period-dependent circadian clock on diurnal, circadian, and aperiodic gene expression in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 99 (2002) 9562-9567
7. Ueda H.R., Matsumoto A., Kawamura M., Iino M., Tanimura T., and Hashimoto S. Genome-wide transcriptional orchestration of circadian rhythms in Drosophila. J. Biol. Chem. 277 (2002) 14048-14052
8. Wijnen H., Naef F., Boothroyd C., Claridge-Chang A., and Young M.W. Control of daily transcript oscillations in Drosophila by light and the circadian clock. PLoS Genet. 2 (2006) e39
9. Boothroyd C.E., Wijnen H., Naef F., Saez L., and Young M.W. Integration of light and temperature in the regulation of circadian gene expression in Drosophila. PLoS Genet. 3 (2007) e54
10. Keegan K.P., Pradhan S., Wang J.P., and Allada R. Meta-Analysis of Drosophila circadian microarray studies identifies a novel set of rhythmically expressed genes. PLoS Comput. Biol. 3 (2007) e208
11. Shafer O.T., Rosbash M., and Truman J.W. Sequential nuclear accumulation of the clock proteins period and timeless in the pacemaker neurons of Drosophila melanogaster. J. Neurosci. 22 (2002) 5946-5954
12. Meyer P., Saez L., and Young M.W. PER-TIM interactions in living Drosophila cells: an interval timer for the circadian clock. Science 311 (2006) 226-229
13. Nitabach M.N., Blau J., and Holmes T.C. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109 (2002) 485-495
14. Harrisingh M.C., Wu Y., Lnenicka G.A., and Nitabach M.N. Intracellular Ca2+ regulates free-running circadian clock oscillation in vivo. J. Neurosci. 27 (2007) 12489-12499
15. Ashmore L.J., and Sehgal A. A fly's eye view of circadian entrainment. J. Biol. Rhythms 18 (2003) 206-216
16. Zerr D.M., Hall J.C., Rosbash M., and Siwicki K.K. Circadian rhythms of period protein immunoreactivity in the CNS and the visual system of Drosophila. J. Neurosci. 10 (1990) 2749-2762
17. Ewer J., Frisch B., Hamblen-Coyle M.J., Rosbash M., and Hall J.C. Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells' influence on circadian behavioral rhythms. J. Neurosci. 12 (1992) 3321-3349
18. Kaneko M., Helfrich-Förster C., and Hall J.C. 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 (1997) 6745-6760
19. Kaneko M., and Hall J.C. 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 (2000) 66-94
20. Taghert P.H., and Shafer O.T. Mechanisms of clock output in the Drosophila circadian pacemaker system. J. Biol. Rhythms 21 (2006) 445-457
21. Frisch B., Hardin P.E., Hamblen-Coyle M.J., Rosbash M., and Hall J.C. A promoter-less period gene mediates behavioral rhythmicity and cyclical per expression in a restricted subset of the Drosophila nervous system. Neuron 12 (1994) 555-570
22. Vosshall L.B., and Young M.W. Circadian rhythms in Drosophila can be driven by period expression in a restricted group of central brain cells. Neuron 15 (1995) 345-360
23. Dushay M.S., Rosbash M., and Hall J.C. The disconnected visual system mutations in Drosophila melanogaster drastically disrupt circadian rhythms. J. Biol. Rhythms 4 (1989) 1-27
24. Grima B., Chelot E., Xia R., and Rouyer F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431 (2004) 869-873
25. Park J.H., Helfrich-Förster C., Lee G., Liu L., Rosbash M., and Hall J.C. Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc. Natl. Acad. Sci. USA 97 (2000) 3608-3613
26. Yang Z., and Sehgal A. Role of molecular oscillations in generating behavioral rhythms in Drosophila. Neuron 29 (2001) 453-467
27. Lear B.C., Lin J.M., Keath J.R., McGill J.J., Raman I.M., and Allada R. The ion channel narrow abdomen is critical for neural output of the Drosophila circadian pacemaker. Neuron 48 (2005) 965-976
28. Lin Y., Stormo G.D., and Taghert P.H. The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J. Neurosci. 24 (2004) 7951-7957
29. Stanewsky R., Kaneko M., Emery P., Beretta B., Wager-Smith K., Kay S.A., Rosbash M., and Hall J.C. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95 (1998) 681-692
30. Renn S.C., Park J.H., Rosbash M., Hall J.C., and Taghert P.H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99 (1999) 791-802
31. Stoleru D., Peng Y., Nawathean P., and Rosbash M. A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 438 (2005) 238-242
32. Stoleru D., Peng Y., Agosto J., and Rosbash M. Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431 (2004) 862-868
33. Veleri S., Brandes C., Helfrich-Förster C., Hall J.C., and Stanewsky R. A self-sustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr. Biol. 13 (2003) 1758-1767
34. Collins B.H., Dissel S., Gaten E., Rosato E., and Kyriacou C.P. Disruption of Cryptochrome partially restores circadian rhythmicity to the arrhythmic period mutant of Drosophila. Proc. Natl. Acad. Sci. USA 102 (2005) 19021-19026
35. Helfrich-Förster C., Shafer O.T., Wülbeck C., Grieshaber E., Rieger D., and Taghert P.H. Development and morphology of the clock-gene-expressing Lateral Neurons of Drosophila melanogaster. J. Comp. Neurol. 500 (2007) 47-70
36. Pittendrigh C.S., and Daan S. A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: a clock for all seasons. J. Comp. Physiol. [A] 106 (1976) 333-355
37. Murad A., Emery-Le M., and Emery P. A subset of dorsal neurons modulates circadian behavior and light responses in Drosophila. Neuron 53 (2007) 689-701
38. Stoleru D., Nawathean P., Fernandez Mde L., Menet J.S., Ceriani M.F., and Rosbash M. The Drosophila circadian network is a seasonal timer. Cell 129 (2007) 207-219
39. Shafer O.T., Helfrich-Förster C., Renn S.C.P., and Taghert P.H. Re-evaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes and inter-class neurochemical interactions. J. Comp. Neurol. 498 (2006) 180-193
40. Yoshii T., Heshiki Y., Ibuki-Ishibashi T., Matsumoto A., Tanimura T., and Tomioka K. Temperature cycles drive Drosophila circadian oscillation in constant light that otherwise induces behavioural arrhythmicity. Eur. J. Neurosci. 22 (2005) 1176-1184
41. Miyasako Y., Umezaki Y., and Tomioka K. Separate sets of cerebral clock neurons are responsible for light and temperature entrainment of Drosophila circadian locomotor rhythms. J. Biol. Rhythms. 22 (2007) 115-126
42. Hamasaka Y., Rieger D., Parmentier M.L., Grau Y., Helfrich-Förster C., and Nässel D.R. Glutamate and its metabotropic receptor in Drosophila clock neuron circuits. J. Comp. Neurol. 505 (2007) 32-45
43. Helfrich-Förster C. The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 92 (1995) 612-616
44. Park J.H., and Hall J.C. Isolation and chronobiological analysis of a neuropeptide pigment-dispersing factor gene in Drosophila melanogaster. J. Biol. Rhythms 13 (1998) 219-228
45. Helfrich-Förster C. Robust circadian rhythmicity of Drosophila melanogaster requires the presence of lateral neurons, a brain-behavioral study of disconnected mutants. J. Comp. Physiol. [A] 182 (1998) 435-453
46. Kula E., Levitan E.S., Pyza E., and Rosbash M. PDF cycling in the dorsal protocerebrum of the Drosophila brain is not necessary for circadian clock function. J. Biol. Rhythms 21 (2006) 104-117
47. Blanchardon E., Grima B., Klarsfeld A., Chelot E., Hardin P.E., Preat T., and Rouyer F. Defining the role of Drosophila lateral neurons in the control of circadian rhythms in motor activity and eclosion by targeted genetic ablation and PERIOD protein overexpression. Eur. J. Neuro. 13 (2001) 871-888
48. Helfrich-Förster C., Tauber M., Park J.H., Muhlig-Versen M., Schneuwly S., and Hofbauer A. Ectopic expression of the neuropeptide pigment-dispersing factor alters behavioral rhythms in Drosophila melanogaster. J. Neurosci. 20 (2000) 3339-3353
49. Aton S.J., Colwell C.S., Harmar A.J., Waschek J., and Herzog E.D. Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat. Neurosci. 8 (2005) 476-483
50. Hyun S., Lee Y., Hong S.T., Bang S., Paik D., Kang J., Shin J., Lee J., Jeon K., Hwang S., et al. Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron 48 (2005) 267-278
51. Lear B.C., Merrill C.E., Lin J.M., Schroeder A., Zhang L., and Allada R. A G protein-coupled receptor, groom-of-PDF, is required for PDF neuron action in circadian behavior. Neuron 48 (2005) 221-227
52. Mertens I., Vandingenen A., Johnson E.C., Shafer O.T., Li W., Trigg J.S., De Loof A., Schoofs L., and Taghert P.H. PDF receptor signaling in Drosophila contributes to both circadian and geotactic behaviors. Neuron 48 (2005) 213-219
53. Scharrer B., and Scharrer E. Neurosecretion VI. A comparison between the intercerebralis-cadiacum-allatum system of insects and the hypothalamo-hypophysial system of vertebrates. Biol. Bull. 87 (1944) 242-251
54. Hartenstein V. The neuroendocrine system of invertebrates: a developmental and evolutionary perspective. J. Endocrinol. 190 (2006) 555-570
55. Rulifson E.J., Kim S.K., and Nusse R. Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296 (2002) 1118-1120
56. Terhzaz S., Rosay P., Goodwin S.F., and Veenstra J.A. The neuropeptide SIFamide modulates sexual behavior in Drosophila. Biochem. Biophys. Res. Commun. 352 (2007) 305-310
57. Foltenyi K., Greenspan R.J., and Newport J.W. Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat. Neurosci. 10 (2007) 1160-1167
58. Lee G., Bahn J.H., and Park J.H. Sex- and clock-controlled expression of the neuropeptide F gene in Drosophila. Proc. Natl. Acad. Sci. USA 103 (2006) 12580-12585
59. Garczynski S.F., Brown M.R., Shen P., Murray T.F., and Crim J.W. Characterization of a functional neuropeptide F receptor from Drosophila melanogaster. Peptides 23 (2002) 773-780
60. Baggerman G., Cerstiaens A., De Loof A., and Schoofs L. Peptidomics of the larval Drosophila melanogaster central nervous system. J. Biol. Chem. 277 (2002) 40368-40374
61. Verleyen P., Baggerman G., Wiehart U., Schoeters E., Van Lommel A., De Loof A., and Schoofs L. Expression of a novel neuropeptide, NVGTLARDFQLPIPNamide, in the larval and adult brain of Drosophila melanogaster. J. Neurochem. 88 (2004) 311-319
62. Baumgardt M., Miguel-Aliaga I., Karlsson D., Ekman H., and Thor S. Specification of neuronal identities by feedforward combinatorial coding. PLoS Biol. 5 (2007) e37
63. Klarsfeld A., Malpel S., Michard-Vanhee C., Picot M., Chelot E., and Rouyer F. Novel features of cryptochrome-mediated photoreception in the brain circadian clock of Drosophila. J. Neurosci. 24 (2004) 1468-1477
64. Wegener C., Hamasaka Y., and Nässel D.R. Acetylcholine increases intracellular Ca2+ via nicotinic receptors in cultured PDF-containing clock neurons of Drosophila. J. Neurophysiol. 91 (2004) 912-923
65. Hamasaka Y., and Nässel D.R. Mapping of serotonin, dopamine, and histamine in relation to different clock neurons in the brain of Drosophila. J. Comp. Neurol. 494 (2006) 314-330
66. Yuan Q., Lin F., Zheng X., and Sehgal A. Serotonin modulates circadian entrainment in Drosophila. Neuron 47 (2005) 115-127
67. Campbell S.S., and Murphy P.J. Extraocular circadian phototransduction in humans. Science 279 (1998) 396-399
68. Ruger M., Gordijn M.C., Beersma D.G., de Vries B., and Daan S. Acute and phase-shifting effects of ocular and extraocular light in human circadian physiology. J. Biol. Rhythms 18 (2003) 409-419
69. Wright Jr. K.P., and Czeisler C.A. Absence of circadian phase resetting in response to bright light behind the knees. Science 297 (2002) 571
70. Helfrich-Förster C., Winter C., Hofbauer A., Hall J.C., and Stanewsky R. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30 (2001) 249-261
71. Emery P., So W.V., Kaneko M., Hall J.C., and Rosbash M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95 (1998) 669-679
72. Hofbauer A., and Buchner E. Does Drosophila Have 7 Eyes?. Naturwissenschaften 76 (1989) 335-336
73. Fleissner G., and Frisch B. A new type of putative non-visual photoreceptors in the optic lobe of beetles. Cell Tissue Res. 273 (1993) 435-445
74. Yasuyama K., and Meinertzhagen I.A. Extraretinal photoreceptors at the compound eye's posterior margin in Drosophila melanogaster. J. Comp. Neurol. 412 (1999) 193-202
75. Helfrich-Förster C., Edwards T., Yasuyama K., Wisotzki B., Schneuwly S., Stanewsky R., Meinertzhagen I.A., and Hofbauer A. The extraretinal eyelet of Drosophila: development, ultrastructure, and putative circadian function. J. Neurosci. 22 (2002) 9255-9266
76. Malpel S., Klarsfeld A., and Rouyer F. Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. Development 129 (2002) 1443-1453
77. Yasuyama K., Okada Y., Hamanaka Y., and Shiga S. Synaptic connections between eyelet photoreceptors and pigment dispersing factor-immunoreactive neurons of the blowfly Protophormia terraenovae. J. Comp. Neurol. 494 (2006) 331-344
78. Mazzoni E.O., Desplan C., and Blau J. Circadian pacemaker neurons transmit and modulate visual information to control a rapid behavioral response. Neuron 45 (2005) 293-300
79. Emery P., Stanewsky R., Helfrich-Förster C., Emery-Le M., Hall J.C., and Rosbash M. Drosophila CRY is a deep brain circadian photoreceptor. Neuron 26 (2000) 493-504
80. Rieger D., Stanewsky R., and Helfrich-Förster 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 (2003) 377-391
81. Veleri S., Rieger D., Helfrich-Förster C., and Stanewsky R. Hofbauer-Buchner eyelet affects circadian photosensitivity and coordinates TIM and PER expression in Drosophila clock neurons. J. Biol. Rhythms 22 (2007) 29-42
82. Dolezelova E., Dolezel D., and Hall J.C. Rhythm defects caused by newly engineered null mutations in Drosophila's cryptochrome gene. Genetics 177 (2007) 329-345
83. Wheeler D.A., Hamblen-Coyle M.J., Dushay M.S., and Hall J.C. Behavior in light-dark cycles of Drosophila mutants that are arrhythmic, blind, or both. J. Biol. Rhythms 8 (1993) 67-94
84. Majercak J., Chen W.F., and Edery I. Splicing of the period gene 3'-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol. Cell Biol. 24 (2004) 3359-3372
85. Glaser F.T., and Stanewsky R. Temperature synchronization of the Drosophila circadian clock. Curr. Biol. 15 (2005) 1352-1363
86. Sayeed O., and Benzer S. Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc. Natl. Acad. Sci. USA 93 (1996) 6079-6084
87. Busza A., Murad A., and Emery P. Interactions between circadian neurons control temperature synchronization of Drosophila behavior. J. Neurosci. 27 (2007) 10722-10733
88. Nitabach M.N., Wu Y., Sheeba V., Lemon W.C., Strumbos J., Zelensky P.K., White B.H., and Holmes T.C. Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods. J. Neurosci. 26 (2006) 479-489
89. McGuire S.E., Mao Z., and Davis R.L. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci. STKE. 2004 (2004) pl6
90. b mutation reveals two circadian clocks that drive locomotor rhythm and have different responsiveness to light. J. Insect Physiol. 50 (2004) 479-488
91. Rieger D., Shafer O.T., Tomioka K., and Helfrich-Förster C. Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J. Neurosci. 26 (2006) 2531-2543
92. Zerr D.M., Hall J.C., Rosbash M., and Siwicki K.K. Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J. Neurosci. 10 (1990) 2749-2762
93. de la Iglesia H.O., Meyer J., Carpinou Jr. A., and Schwartz W.J. Antiphase oscillation of the left and right suprachiasmatic nuclei. Science 290 (2000) 799-801
94. Marder E., and Calabrese R.L. Principles of rhythmic motor pattern generation. Physiol. Rev. 76 (1996) 687-717
95. Park D., and Griffith L.C. Electrophysiological and anatomical characterization of PDF-positive clock neurons in the intact adult Drosophila brain. J. Neurophys. 95 (2006) 3955-3960
96. Kim Y.J., Zitnan D., Galizia C.G., Cho K.H., and Adams M.E. A command chemical triggers an innate behavior by sequential activation of multiple peptidergic ensembles. Curr. Biol. 16 (2006) 1395-1407
97. Harmar A.J., Marston H.M., Shen S., Spratt C., West K.M., Sheward W.J., Morrison C.F., Dorin J.R., Piggins H.D., Reubi J.C., et al. The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 109 (2002) 497-508
98. Maywood E.S., Reddy A.B., Wong G.K., O'Neill J.S., O'Brien J.A., McMahon D.G., Harmar A.J., Okamura H., and Hastings M.H. Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Curr. Biol. 16 (2006) 599-605
99. Yamaguchi S., Isejima H., Matsuo T., Okura R., Yagita K., Kobayashi M., and Okamura H. Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 302 (2003) 1408-1412
100. Peng Y., Stoleru D., Levine J.D., Hall J.C., and Rosbash M. Drosophila free-running rhythms require intercellular communication. PLoS Biol. 1 (2003) E13
101. Welsh D.K., Logothetis D.E., Meister M., and Reppert S.M. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14 (1995) 697-706