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Research Article

The Drosophila Circadian Pacemaker Circuit: Pas de Deux or Tarantella?

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Pages 37-61 | Published online: 11 Oct 2008

REFERENCES

  • Allada R., Emery P., Takahashi J. S., Rosbash M. Stopping time: the genetics of fly and mouse circadian clocks. Annu Rev Neurosci 2001; 24: 1091–1119
  • Aschoff J., Wever R. Circadian period and phase-angle difference in chaffinches (Fringilla coelebs L.). Comp Biochem Physiol 1966; 18: 397–404
  • Aschoff J. Circadian rhythms: influences of internal and external factors on the period measured in constant conditions. Z Tierpsychol 1979; 49: 225–249
  • Bachleitner W., Kempinger L., Wulbeck C., Rieger D., Helfrich-Forster C. Moonlight shifts the endogenous clock of Drosophila melanogaster. Proc Natl Acad Sci U S A. 2007; 104: 3538–3543
  • Bae K., Edery I. Regulating a circadian clock's period, phase and amplitude by phosphorylation: insights from Drosophila. J Biochem (Tokyo) 2006; 140: 609–617
  • Bao S., Rihel J., Bjes E., Fan J. Y., Price J. L. The Drosophila double-timeS mutation delays the nuclear accumulation of period protein and affects the feedback regulation of period mRNA. J Neurosci 2001; 21: 7117–7126
  • Benito J., Zheng H., Hardin P. E. PDP1epsilon functions downstream of the circadian oscillator to mediate behavioral rhythms. J Neurosci 2007; 27: 2539–2547
  • Blanchardon E., Grima B., Klarsfeld A., Chelot E., Hardin P. E., Preat T., 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 Neurosci 2001; 13: 871–888
  • Bradshaw W., Holzapfel C. Evolution. Tantalizing timeless. Science 2007; 316: 1851–1852
  • Bunning E. Common features of photoperiodism in plants and animals. Photochem Photobiol 1969; 9: 219–228
  • Busza A., Emery-Le M., Rosbash M., Emery P. Roles of the two Drosophila CRYPTOCHROME structural domains in circadian photoreception. Science 2004; 304: 1503–1506
  • Busza A., Murad A., Emery P. Interactions between circadian neurons control temperature synchronization of Drosophila behavior. J Neurosci 2007; 27: 10722–10733
  • Cheng Y., Hardin P. E. Drosophila photoreceptors contain an autonomous circadian oscillator that can function without period mRNA cycling. J Neurosci 1998; 18: 741–750
  • Claridge-Chang A., Wijnen H., Naef F., Boothroyd C., Rajewsky N., Young M. W. Circadian regulation of gene expression systems in the Drosophila head. Neuron 2001; 32: 657–671
  • Collins B., Mazzoni E. O., Stanewsky R., Blau J. Drosophila CRYPTOCHROME is a circadian transcriptional repressor. Curr Biol 2006; 16: 441–449
  • Collins B. H., Rosato E., Kyriacou C. P. Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C. Proc Natl Acad Sci U S A 2004; 101: 1945–1950
  • Colwell C. S. Circadian modulation of calcium levels in cells in the suprachiasmatic nucleus. Eur J Neurosci 2000; 12: 571–576
  • Cyran S. A., Buchsbaum A. M., Reddy K. L., Lin M. C., Glossop N. R., Hardin P. E., Young M. W., Storti R. V., Blau J. vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 2003; 112: 329–341
  • Cyran S. A., Yiannoulos G., Buchsbaum A. M., Saez L., Young M. W., Blau J. The double-time protein kinase regulates the subcellular localization of the Drosophila clock protein period. J Neurosci 2005; 25: 5430–5437
  • Daan S., Albrecht U., van der Horst G. T., Illnerova H., Roenneberg T., Wehr T. A., Schwartz W. J. Assembling a clock for all seasons: are there M and E oscillators in the genes?. J Biol Rhythms 2001; 16: 105–116
  • Davis F. C., Gorski R. A. Unilateral lesions of the hamster suprachiasmatic nuclei: Evidence for redundant control of circadian rhythms. J Comp Physiol [A] 1984; 154: 221–232
  • de la Iglesia H. O., Cambras T., Schwartz W. J., Diez-Noguera A. Forced desynchronization of dual circadian oscillators within the rat suprachiasmatic nucleus. Curr Biol 2004; 14: 796–800
  • de la Paz Fernandez M., Chu J., Villella A., Atkinson N., Kay S. A., Ceriani M. F. Impaired clock output by altered connectivity in the circadian network. Proc Natl Acad Sci U S A 2007; 104: 5650–5655
  • Dissel S., Codd V., Fedic R., Garner K. J., Costa R., Kyriacou C. P., Rosato E. A constitutively active cryptochrome in Drosophila melanogaster. Nat Neurosci 2004; 7: 834–840
  • Edery I., Zwiebel L. J., Dembinska M. E., Rosbash M. Temporal phosphorylation of the Drosophila period protein. Proc Natl Acad Sci U S A 1994; 91: 2260–2264
  • Emery P., Stanewsky R., Helfrich-Forster C., Emery-Le M., Hall J. C., Rosbash M. Drosophila CRY is a deep brain circadian photoreceptor. Neuron 2000; 26: 493–504
  • Etter P. D., Ramaswami M. The ups and downs of daily life: profiling circadian gene expression in Drosophila. Bioessays 2002; 24: 494–498
  • Ewer J., Frisch B., Hamblen-Coyle M. J., Rosbash M., 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 1992; 12: 3321–3349
  • Fan Y., Hida A., Anderson D. A., Izumo M., Johnson C. H. Cycling of CRYPTOCHROME proteins is not necessary for circadian-clock function in mammalian fibroblasts. Curr Biol 2007; 17: 1091–1100
  • Fang Y., Sathyanarayanan S., Sehgal A. Post-translational regulation of the Drosophila circadian clock requires protein phosphatase 1 (PP1). Genes Dev 2007; 21: 1506–1518
  • Frisch B., Hardin P. E., Hamblen-Coyle M. J., Rosbash M., Hall J. C. A promoterless period gene mediates behavioral rhythmicity and cyclical per expression in a restricted subset of the Drosophila nervous system. Neuron 1994; 12: 555–570
  • Glaser F. T., Stanewsky R. Temperature synchronization of the Drosophila circadian clock. Curr Biol 2005; 15: 1352–1363
  • Glossop N. R., Lyons L. C., Hardin P. E. Interlocked feedback loops within the Drosophila circadian oscillator. Science 1999; 286: 766–768
  • Glossop N. R., Houl J. H., Zheng H., Ng F. S., Dudek S. M., Hardin P. E. VRILLE feeds back to control circadian transcription of Clock in the Drosophila circadian oscillator. Neuron 2003; 37: 249–261
  • Gorska-Andrzejak J., Keller A., Raabe T., Kilianek L., Pyza E. Structural daily rhythms in GFP-labelled neurons in the visual system of Drosophila melanogaster. Photochem Photobiol Sci 2005; 4: 721–726
  • Green D. J., Gillette R. Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res 1982; 245: 198–200
  • Grima B., Lamouroux A., Chelot E., Papin C., Limbourg-Bouchon B., Rouyer F. The F-box protein slimb controls the levels of clock proteins period and timeless. Nature 2002; 420: 178–182
  • Grima B., Chelot E., Xia R., Rouyer F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 2004; 431: 869–873
  • Hardin P. E., Hall J. C., Rosbash M. Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 1990; 343: 536–540
  • Hardin P. E. Essential and expendable features of the circadian timekeeping mechanism. Curr Opin Neurobiol 2006; 16: 686–692
  • Harms E., Kivimae S., Young M. W., Saez L. Posttranscriptional and posttranslational regulation of clock genes. J Biol Rhythms 2004; 19: 361–373
  • Harrington M., Molyneux P., Soscia S., Prabakar C., McKinley-Brewer J., Lall G. Behavioral and neurochemical sources of variability of circadian period and phase: studies of circadian rhythms of npy-/- mice. Am J Physiol Regul Integr Comp Physiol 2007; 292: R1306–1314
  • Helfrich-Forster C., Homberg U. Pigment-dispersing hormone-immunoreactive neurons in the nervous system of wild-type Drosophila melanogaster and of several mutants with altered circadian rhythmicity. J Comp Neurol 1993; 337: 177–190
  • Helfrich-Forster 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 U S A 1995; 92: 612–616
  • Helfrich-Forster C. Development of pigment-dispersing hormone-immunoreactive neurons in the nervous system of Drosophila melanogaster. J Comp Neurol 1997; 380: 335–354
  • Helfrich-Forster C., Stengl M., Homberg U. Organization of the circadian system in insects. Chronobiol Int 1998; 15: 567–594
  • Helfrich-Forster C. Differential control of morning and evening components in the activity rhythm of Drosophila melanogaster—sex-specific differences suggest a different quality of activity. J Biol Rhythms 2000; 15: 135–154
  • Helfrich-Forster C., Winter C., Hofbauer A., Hall J. C., Stanewsky R. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 2001; 30: 249–261
  • Helfrich-Forster C. The circadian system of Drosophila melanogaster and its light input pathways. Zoology (Jena) 2002; 105: 297–312
  • Helfrich-Forster C., Edwards T., Yasuyama K., Wisotzki B., Schneuwly S., Stanewsky R., Meinertzhagen I. A., Hofbauer A. The extraretinal eyelet of Drosophila: development, ultrastructure, and putative circadian function. J Neurosci 2002a; 22: 9255–9266
  • Helfrich-Forster C., Wulf J., de Belle J. S. Mushroom body influence on locomotor activity and circadian rhythms in Drosophila melanogaster. J Neurogenet 2002b; 16: 73–109
  • Helfrich-Forster C. The neuroarchitecture of the circadian clock in the brain of Drosophila melanogaster. Microsc Res Tech 2003; 62: 94–102
  • Helfrich-Forster C. Neurobiology of the fruit fly's circadian clock. Genes Brain Behav 2005; 4: 65–76
  • Helfrich-Forster C., Shafer O. T., Wulbeck C., Grieshaber E., Rieger D., Taghert P. Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J Comp Neurol 2007; 500: 47–70
  • Helfrich C. Role of the optic lobes in the regulation of the locomotor activity rhythm of Drosophila melanogaster: behavioral analysis of neural mutants. J Neurogenet 1986; 3: 321–343
  • Hendricks J. C., Finn S. M., Panckeri K. A., Chavkin J., Williams J. A., Sehgal A., Pack A. I. Rest in Drosophila is a sleep-like state. Neuron 2000; 25: 129–138
  • Herzog E. D., Takahashi J. S., Block G. D. Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nat Neurosci 1998; 1: 708–713
  • Hong S.-F., Saunders D. S. Internal desynchronization in blow fly (Calliphora vicina) locomotor activity rhythms: Evidence for a complex circadian pacemaker. Biol Rhythm Res 1998; 29: 387–396
  • Howlader G., Paranjpe D. A., Sharma V. K. Non-ventral lateral neuron-based, non-PDF-mediated clocks control circadian egg-laying rhythm in Drosophila melanogaster. J Biol Rhythms 2006; 21: 13–20
  • Howlader G., Sharma V. K. Circadian regulation of egg-laying behavior in fruit flies Drosophila melanogaster. J Insect Physiol 2006; 52: 779–785
  • Hunter-Ensor M., Ousley A., Sehgal A. Regulation of the Drosophila protein timeless suggests a mechanism for resetting the circadian clock by light. Cell 1996; 84: 677–685
  • Hyun S., Lee Y., Hong S. T., et al. Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron 2005; 48: 267–278
  • Ikeda M., Sugiyama T., Wallace C. S., Gompf H. S., Yoshioka T., Miyawaki A., Allen C. N. Circadian dynamics of cytosolic and nuclear Ca2+ in single suprachiasmatic nucleus neurons. Neuron 2003; 38: 253–263
  • Inouye S. T., Kawamura H. Persistence of circadian rhythmicity in a mammalian hypothalamic “island” containing the suprachiasmatic nucleus. Proc Natl Acad Sci U S A 1979; 76: 5962–5966
  • Itri J. N., Michel S., Vansteensel M. J., Meijer J. H., Colwell C. S. Fast delayed rectifier potassium current is required for circadian neural activity. Nat Neurosci 2005; 8: 650–656
  • Joiner W. J., Crocker A., White B. H., Sehgal A. Sleep in Drosophila is regulated by adult mushroom bodies. Nature 2006; 441: 757–760
  • Kadener S., Stoleru D., McDonald M., Nawathean P., Rosbash M. Clockwork Orange is a transcriptional repressor and a new Drosophila circadian pacemaker component. Genes Dev 2007; 21: 1675–1686
  • Kaneko M., Helfrich-Forster C., 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 1997; 17: 6745–6760
  • Kaneko M. Neural substrates of Drosophila rhythms revealed by mutants and molecular manipulations. Curr Opin Neurobiol 1998; 8: 652–658
  • Kaneko M., 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 2000; 422: 66–94
  • Kaneko M., Hernandez-Borsetti N., Cahill G. M. Diversity of zebrafish peripheral oscillators revealed by luciferase reporting. Proc Natl Acad Sci U S A 2006; 103: 14614–14619
  • Kaushik R., Nawathean P., Busza A., Murad A., Emery P., Rosbash M. PER-TIM Interactions with the Photoreceptor Cryptochrome Mediate Circadian Temperature Responses in Drosophila. PLoS Biol 2007; 5: e146
  • Kim E. Y., Bae K., Ng F. S., Glossop N. R., Hardin P. E., Edery I. Drosophila CLOCK protein is under posttranscriptional control and influences light-induced activity. Neuron 2002; 34: 69–81
  • Kim E. Y., Edery I. Balance between DBT/CKIepsilon kinase and protein phosphatase activities regulate phosphorylation and stability of Drosophila CLOCK protein. Proc Natl Acad Sci U S A 2006; 103: 6178–6183
  • Kiyohara Y. B., Tagao S., Tamanini F., et al. The BMAL1 C terminus regulates the circadian transcription feedback loop. Proc Natl Acad Sci U S A 2006; 103: 10074–10079
  • Klarsfeld A., Leloup J. C., Rouyer F. Circadian rhythms of locomotor activity in Drosophila. Behav Processes 2003; 64: 161–175
  • Klarsfeld A., Malpel S., Michard-Vanhee C., Picot M., Chelot E., Rouyer F. Novel features of cryptochrome-mediated photoreception in the brain circadian clock of Drosophila. J Neurosci 2004; 24: 1468–1477
  • Kloss B., Price J. L., Saez L., Blau J., Rothenfluh A., Wesley C. S., Young M. W. The Drosophila clock gene double-time encodes a protein closely related to human casein kinase Iepsilon. Cell 1998; 94: 97–107
  • Ko H. W., Jiang J., Edery I. Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature 2002; 420: 673–678
  • Koehler W. K., Fleissner G. Internal desynchronisation of bilaterally organised circadian oscillators in the visual system of insects. Nature 1978; 274: 708–710
  • Koh K., Zheng X., Sehgal A. JETLAG resets the Drosophila circadian clock by promoting light-induced degradation of TIMELESS. Science 2006; 312: 1809–1812
  • Konopka R. J., Benzer S. Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 1971; 68: 2112–2116
  • Konopka R. J., Pittendrigh C., Orr D. Reciprocal behaviour associated with altered homeostasis and photosensitivity of Drosophila clock mutants. J Neurogenet 1989; 6: 1–10
  • Krishnan B., Dryer S. E., Hardin P. E. Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 1999; 400: 375–378
  • Kuhlman S. J., McMahon D. G. Encoding the ins and outs of circadian pacemaking. J Biol Rhythms 2006; 21: 470–481
  • Lakin-Thomas P. L. Transcriptional feedback oscillators: maybe, maybe not. J Biol Rhythms 2006; 21: 83–92
  • Lear B. C., Merrill C. E., Lin J. M., Schroeder A., Zhang L., Allada R. A G protein-coupled receptor, groom-of-PDF, is required for PDF neuron action in circadian behavior. Neuron 2005; 48: 221–227
  • Lee G., Bahn J. H., Park J. H. Sex- and clock-controlled expression of the neuropeptide F gene in Drosophila. Proc Natl Acad Sci U S A 2006; 103: 12580–12585
  • Leise T. L., Moin E. E. A mathematical model of the Drosophila circadian clock with emphasis on posttranslational mechanisms. J Theor Biol 2007; 248: 48–63
  • Lim C., Chung B. Y., Pitman J. L., McGill J. J., Pradhan S., Lee J., Keegan K. P., Choe J., Allada R. Clockwork orange encodes a transcriptional repressor important for circadian-clock amplitude in Drosophila. Curr Biol 2007; 17: 1082–1089
  • Lin J. M., Kilman V. L., Keegan K., Paddock B., Emery-Le M., Rosbash M., Allada R. A role for casein kinase 2alpha in the Drosophila circadian clock. Nature 2002; 420: 816–820
  • Lin Y., Stormo G. D., Taghert P. H. The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J Neurosci 2004; 24: 7951–7957
  • Liu C., Ding J. M., Faiman L. E., Gillette M. U. Coupling of muscarinic cholinergic receptors and cGMP in nocturnal regulation of the suprachiasmatic circadian clock. J Neurosci 1997; 17: 659–666
  • Majercak J., Sidote D., Hardin P. E., Edery I. How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 1999; 24: 219–230
  • Majercak J., Chen W. F., Edery I. Splicing of the period gene 3′-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol Cell Biol 2004; 24: 3359–3372
  • Malpel S., Klarsfeld A., Rouyer F. Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. Development 2002; 129: 1443–1453
  • Martinek S., Inonog S., Manoukian A. S., Young M. W. A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 2001; 105: 769–779
  • Mason R. The effects of continuous light exposure on Syrian hamster suprachiasmatic (SCN) neuronal discharge activity in vitro. Neurosci Lett 1991; 123: 160–163
  • Matsumoto A., Matsumoto N., Harui Y., Sakamoto M., Tomioka K. Light and temperature cooperate to regulate the circadian locomotor rhythm of wild type and period mutants of Drosophila melanogaster. J Insect Physiol 1998; 44: 587–596
  • Matsumoto A., Ukai-Tadenuma M., Yamada R. G., et al. A functional genomics strategy reveals clockwork orange as a transcriptional regulator in the Drosophila circadian clock. Genes Dev 2007; 21: 1687–1700
  • Mazzoni E. O., Desplan C., Blau J. Circadian pacemaker neurons transmit and modulate visual information to control a rapid behavioral response. Neuron 2005; 45: 293–300
  • McMahon D. G., Block G. D. The Bulla ocular circadian pacemaker. I. Pacemaker neuron membrane potential controls phase through a calcium-dependent mechanism. J Comp Physiol [A] 1987; 161: 335–346
  • Mehnert K. I., Beramendi A., Elghazali F., Negro P., Kyriacou C. P., Cantera R. Circadian changes in Drosophila motor terminals. Dev Neurobiol 2007; 67: 415–421
  • Meijer J. H., van der Zee E., Dietz M. The effects of intraventricular carbachol injections on the free-running activity rhythm of the hamster. J Biol Rhythms 1988; 3: 333–348
  • Meijer J. H., Daan S., Overkamp G. J., Hermann P. M. The two-oscillator circadian system of tree shrews (Tupaia belangeri) and its response to light and dark pulses. J Biol Rhythms 1990; 5: 1–16
  • Meijer J. H., Schaap J., Watanabe K., Albus H. Multiunit activity recordings in the suprachiasmatic nuclei: in vivo versus in vitro models. Brain Res 1997; 753: 322–327
  • Mertens I., Vandingenen A., Johnson E. C., Shafer O. T., Li W., Trigg J. S., De Loof A., Schoofs L., Taghert P. H. PDF receptor signaling in Drosophila contributes to both circadian and geotactic behaviors. Neuron 2005; 48: 213–219
  • Meyer P., Saez L., Young M. W. PER-TIM interactions in living Drosophila cells: an interval timer for the circadian clock. Science 2006; 311: 226–229
  • Michel S., Geusz M. E., Zaritsky J. J., Block G. D. Circadian rhythm in membrane conductance expressed in isolated neurons. Science 1993; 259: 239–241
  • Miyasako Y., Umezaki Y., Tomioka K. Separate sets of cerebral clock neurons are responsible for light and temperature entrainment of Drosophila circadian locomotor rhythms. J Biol Rhythms 2007; 22: 115–126
  • Mori T., Williams D. R., Byrne M. O., Qin X., Egli M., McHaourab H. S., Stewart P. L., Johnson C. H. Elucidating the Ticking of an In Vitro Circadian Clockwork. PLoS Biol 2007; 5: e93
  • Murad A., Emery-Le M., Emery P. A subset of dorsal neurons modulates circadian behavior and light responses in Drosophila. Neuron 2007; 53: 689–701
  • Myers E. M., Yu J., Sehgal A. Circadian control of eclosion: interaction between a central and peripheral clock in Drosophila melanogaster. Curr Biol 2003; 13: 526–533
  • Naidoo N., Song W., Hunter-Ensor M., Sehgal A. A role for the proteasome in the light response of the timeless clock protein. Science 1999; 285: 1737–1741
  • Nakajima M., Imai K., Ito H., Nishiwaki T., Murayama Y., Iwasaki H., Oyama T., Kondo T. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 2005; 308: 414–415
  • Nakamura W., Honma S., Shirakawa T., Honma K. Clock mutation lengthens the circadian period without damping rhythms in individual SCN neurons. Nat Neurosci 2002; 5: 399–400
  • Nawathean P., Rosbash M. The doubletime and CKII kinases collaborate to potentiate Drosophila PER transcriptional repressor activity. Mol Cell 2004; 13: 213–223
  • Nawathean P., Stoleru D., Rosbash M. A small conserved domain of Drosophila PERIOD is important for circadian phosphorylation, nuclear localization, and transcriptional repressor activity. Mol Cell Biol 2007; 27: 5002–5013
  • Nitabach M. N., Blau J., Holmes T. C. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 2002; 109: 485–495
  • Nitabach M. N., Holmes T. C., Blau J. Membranes, ions, and clocks: testing the Njus-Sulzman-Hastings model of the circadian oscillator. Methods Enzymol 2005a; 393: 682–693
  • Nitabach M. N., Sheeba V., Vera D. A., Blau J., Holmes T. C. Membrane electrical excitability is necessary for the free-running larval Drosophila circadian clock. J Neurobiol 2005b; 62: 1–13
  • Nitabach M. N., Wu Y., Sheeba V., Lemon W. C., Strumbos J., Zelensky P. K., White B. H., 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 2006; 26: 479–489
  • Nixon J. P., Smale L. Individual differences in wheel-running rhythms are related to temporal and spatial patterns of activation of orexin A and B cells in a diurnal rodent (Arvicanthis niloticus). Neuroscience 2004; 127: 25–34
  • Njus D., Sulzman F. M., Hastings J. W. Membrane model for the circadian clock. Nature 1974; 248: 116–120
  • Njus D., Gooch V. D., Mergenhagen D., Sulzman F., Hastings J. W. Membranes and molecules in circadian systems. Fed Proc 1976; 35: 2353–2357
  • Park D., Griffith L. C. Electrophysiological and anatomical characterization of PDF-positive clock neurons in the intact adult Drosophila brain. J Neurophysiol 2006; 95: 3955–3960
  • Peng Y., Stoleru D., Levine J. D., Hall J. C., Rosbash M. Drosophila free-running rhythms require intercellular communication. PLoS Biol 2003; 1: E13
  • Pennartz C. M., de Jeu M. T., Bos N. P., Schaap J., Geurtsen A. M. Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock. Nature 2002; 416: 286–290
  • Peschel N., Veleri S., Stanewsky R. Veela defines a molecular link between Cryptochrome and Timeless in the light-input pathway to Drosophila's circadian clock. Proc Natl Acad Sci U S A 2006; 103: 17313–17318
  • Petri B., Stengl M. Pigment-dispersing hormone shifts the phase of the circadian pacemaker of the cockroach Leucophaea maderae. J Neurosci 1997; 17: 4087–4093
  • Pickard G. E., Turek F. W. Splitting of the circadian rhythm of activity is abolished by unilateral lesions of the suprachiasmatic nuclei. Science 1982; 215: 1119–1121
  • Pickard G. E., Turek F. W., Sollars P. J. Light intensity and splitting in the golden hamster. Physiol Behav 1993; 54: 1–5
  • Pitman J. L., McGill J. J., Keegan K. P., Allada R. A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 2006; 441: 753–756
  • Pittendrigh C., Daan S. A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker complexity: A clock for all seasons. J Comp Physiol 1976; 106: 333–335
  • Pittendrigh C. S. On temperature independence in the clock system controlling emergence time in Drosophila. Proc Natl Acad Sci U S A 1954; 40: 1018–1029
  • Pittendrigh C. S. Circadian rhythms and the circadian organization of living systems. Cold Spring Harb Symp Quant Biol 1960; 25: 159–184
  • Plautz J. D., Kaneko M., Hall J. C., Kay S. A. Independent photoreceptive circadian clocks throughout Drosophila. Science 1997; 278: 1632–1635
  • Pyza E., Meinertzhagen I. A. Daily and circadian rhythms of synaptic frequency in the first visual neuropile of the housefly's (Musca domestica L.) optic lobe. Proc Biol Sci 1993; 254: 97–105
  • Pyza E., Meinertzhagen I. A. Monopolar cell axons in the first optic neuropil of the housefly, Musca domestica L., undergo daily fluctuations in diameter that have a circadian basis. J Neurosci 1995; 15: 407–418
  • Pyza E., Meinertzhagen I. A. Circadian rhythms in screening pigment and invaginating organelles in photoreceptor terminals of the housefly's first optic neuropile. J Neurobiol 1997; 32: 517–529
  • Pyza E., Meinertzhagen I. A. Daily rhythmic changes of cell size and shape in the first optic neuropil in Drosophila melanogaster. J Neurobiol 1999; 40: 77–88
  • Quintero J. E., Kuhlman S. J., McMahon D. G. The biological clock nucleus: a multiphasic oscillator network regulated by light. J Neurosci 2003; 23: 8070–8076
  • Renn S. C., Park J. H., Rosbash M., Hall J. C., Taghert P. H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 1999; 99: 791–802
  • 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 2003; 18: 377–391
  • Rieger D., Shafer O. T., Tomioka K., Helfrich-Forster C. Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 2006; 26: 2531–2543
  • Rohling J., Wolters L., Meijer J. H. Simulation of day-length encoding in the SCN: from single-cell to tissue-level organization. J Biol Rhythms 2006; 21: 301–313
  • Rosenwasser A. M., Adler N. T. Structure and function in circadian timing systems: evidence for multiple coupled circadian oscillators. Neurosci Biobehav Rev 1986; 10: 431–448
  • Rust M. J., Markson J. S., Lane W. S., Fisher D. S., O'Shea E. K. Ordered Phosphorylation Governs Oscillation of a Three-Protein Circadian Clock. Science 2007; 318: 809–812
  • Sakai T., Ishida N. Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc Natl Acad Sci U S A 2001; 98: 9221–9225
  • Sandrelli F., Tauber E., Pegoraro M., et al. A molecular basis for natural selection at the timeless locus in Drosophila melanogaster. Science 2007; 316: 1898–1900
  • Saper C. B., Lu J., Chou T. C., Gooley J. The hypothalamic integrator for circadian rhythms. Trends Neurosci 2005; 28: 152–157
  • Sathyanarayanan S., Zheng X., Xiao R., Sehgal A. Posttranslational regulation of Drosophila PERIOD protein by protein phosphatase 2A. Cell 2004; 116: 603–615
  • Saunders D. S. The circadian basis of ovarian diapause regulation in Drosophila melanogaster: is the period gene causally involved in photoperiodic time measurement?. J Biol Rhythms 1990; 5: 315–331
  • Saunders D. S. Erwin Bunning and Tony Lees, two giants of chronobiology, and the problem of time measurement in insect photoperiodism. J Insect Physiol 2005; 51: 599–608
  • Schaap J., Albus H., VanderLeest H. T., Eilers P. H., Detari L., Meijer J. H. Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding. Proc Natl Acad Sci U S A 2003; 100: 15994–15999
  • Schardt U., Wilhelm I., Erkert H. G. Splitting of the circadian activity rhythm in common marmosets (Callithrix j. jacchus; primates). Experientia 1989; 45: 1112–1115
  • Schwartz M. D., Nunez A. A., Smale L. Differences in the suprachiasmatic nucleus and lower subparaventricular zone of diurnal and nocturnal rodents. Neuroscience 2004; 127: 13–23
  • Schwartz M. D., Smale L. Individual differences in rhythms of behavioral sleep and its neural substrates in Nile grass rats. J Biol Rhythms 2005; 20: 526–537
  • Schwartz W. J., Gross R. A., Morton M. T. The suprachiasmatic nuclei contain a tetrodotoxin-resistant circadian pacemaker. Proc Natl Acad Sci U S A 1987; 84: 1694–1698
  • Sehgal A., Price J. L., Man B., Young M. W. Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 1994; 263: 1603–1606
  • Shafer O. T., Rosbash M., Truman J. W. Sequential nuclear accumulation of the clock proteins period and timeless in the pacemaker neurons of Drosophila melanogaster. J Neurosci 2002; 22: 5946–5954
  • Shafer O. T., Helfrich-Forster C., Renn S. C., Taghert P. H. Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes. J Comp Neurol 2006; 498: 180–193
  • Shaw P. J., Cirelli C., Greenspan R. J., Tononi G. Correlates of sleep and waking in Drosophila melanogaster. Science 2000; 287: 1834–1837
  • Siwicki K. K., Eastman C., Petersen G., Rosbash M., Hall J. C. Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron 1988; 1: 141–150
  • Smale L., Lee T., Nunez A. A. Mammalian diurnality: some facts and gaps. J Biol Rhythms 2003; 18: 356–366
  • Smietanko A., Engelmann W. Splitting of circadian rhythm of Musca domestica flies with azadirachtin. J Interdiscipl Cycle Res 1989; 20: 71–79
  • Stanewsky R., Kaneko M., Emery P., Beretta B., Wager-Smith K., Kay S. A., Rosbash M., Hall J. C. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 1998; 95: 681–692
  • Stoleru D., Peng Y., Agosto J., Rosbash M. Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 2004; 431: 862–868
  • Stoleru D., Peng Y., Nawathean P., Rosbash M. A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 2005; 438: 238–242
  • Stoleru D., Nawathean P., Fernandez Mde L., Menet J. S., Ceriani M. F., Rosbash M. The Drosophila circadian network is a seasonal timer. Cell 2007; 129: 207–219
  • Suh J., Jackson F. R. Drosophila ebony activity is required in glia for the circadian regulation of locomotor activity. Neuron 2007; 55: 435–447
  • Taghert P. H., Shafer O. T. Mechanisms of clock output in the Drosophila circadian pacemaker system. J Biol Rhythms 2006; 21: 445–457
  • Tanoue S., Krishnan P., Krishnan B., Dryer S. E., Hardin P. E. Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr Biol 2004; 14: 638–649
  • Tauber E., Zordan M., Sandrelli F., et al. Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 2007; 316: 1895–1898
  • Tomita J., Nakajima M., Kondo T., Iwasaki H. No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 2005; 307: 251–254
  • Ueda H. R., Matsumoto A., Kawamura M., Iino M., Tanimura T., Hashimoto S. Genome-wide transcriptional orchestration of circadian rhythms in Drosophila. J Biol Chem 2002; 277: 14048–14052
  • Van Gelder R. N. Timeless genes and jetlag. Proc Natl Acad Sci U S A 2006; 103: 17583–17584
  • Veleri S., Brandes C., Helfrich-Forster C., Hall J. C., Stanewsky R. A self-sustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr Biol 2003; 13: 1758–1767
  • Vosshall L. B., Young M. W. Circadian rhythms in Drosophila can be driven by period expression in a restricted group of central brain cells. Neuron 1995; 15: 345–360
  • Welsh D. K., Logothetis D. E., Meister M., Reppert S. M. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 1995; 14: 697–706
  • Wheeler D. A., Hamblen-Coyle M. J., Dushay M. S., Hall J. C. Behavior in light-dark cycles of Drosophila mutants that are arrhythmic, blind, or both. J Biol Rhythms 1993; 8: 67–94
  • Wijnen H., Naef F., Boothroyd C., Claridge-Chang A., Young M. W. Control of daily transcript oscillations in Drosophila by light and the circadian clock. PLoS Genet 2006; 2: e39
  • Yamaguchi S., Isejima H., Matsuo T., Okura R., Yagita K., Kobayashi M., Okamura H. Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 2003; 302: 1408–1412
  • Yamazaki S., Numano R., Abe M., Hida A., Takahashi R., Ueda M., Block G. D., Sakaki Y., Menaker M., Tei H. Resetting central and peripheral circadian oscillators in transgenic rats. Science 2000; 288: 682–685
  • Yang Z., Sehgal A. Role of molecular oscillations in generating behavioral rhythms in Drosophila. Neuron 2001; 29: 453–467
  • Yoshii T., Sakamoto M., Tomioka K. A temperature-dependent timing mechanism is involved in the circadian system that drives locomotor rhythms in the fruit fly Drosophila melanogaster. Zoolog Sci 2002; 19: 841–850
  • Yoshii T., Funada Y., Ibuki-Ishibashi T., Matsumoto A., Tanimura T., Tomioka K. Drosophila cryb mutation reveals two circadian clocks that drive locomotor rhythm and have different responsiveness to light. J Insect Physiol 2004; 50: 479–488
  • Yoshii T., Heshiki Y., Ibuki-Ishibashi T., Matsumoto A., Tanimura T., Tomioka K. Temperature cycles drive Drosophila circadian oscillation in constant light that otherwise induces behavioural arrhythmicity. Eur J Neurosci 2005; 22: 1176–1184
  • Yu W., Hardin P. E. Circadian oscillators of Drosophila and mammals. J Cell Sci 2006; 119: 4793–4795
  • Yu W., Zheng H., Houl J. H., Dauwalder B., Hardin P. E. PER-dependent rhythms in CLK phosphorylation and E-box binding regulate circadian transcription. Genes Dev 2006; 20: 723–733
  • Yuan Q., Joiner W. J., Sehgal A. A sleep-promoting role for the Drosophila serotonin receptor 1A. Curr Biol 2006; 16: 1051–1062
  • Zeng H., Qian Z., Myers M. P., Rosbash M. A light-entrainment mechanism for the Drosophila circadian clock. Nature 1996; 380: 129–135
  • Zlomanczuk P., Margraf R. R., Lynch G. R. In vitro electrical activity in the suprachiasmatic nucleus following splitting and masking of wheel-running behavior. Brain Res 1991; 559: 94–99

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