Even a stopped clock tells the right time twice a day: Circadian timekeeping in Drosophila

Pflugers Archiv European Journal of Physiology

Volumn 454, Issue 5, 2007, Pages 857-867

  Collins, Ben ^a   Blau, Justin ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Circadian rhythms; Clock inputs; Clock neural circuits; Drosophila

Indexed keywords

NEUROTRANSMITTER;

BEHAVIOR; CIRCADIAN RHYTHM; DROSOPHILA; ENVIRONMENT; LIGHT; LIGHT DARK CYCLE; MEMBRANE DEPOLARIZATION; MOLECULAR BIOLOGY; MOLECULAR CLOCK; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEASONAL VARIATION; SENSORY STIMULATION; SOCIAL BEHAVIOR; TEMPERATURE; TIME PERCEPTION;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; DROSOPHILA; DROSOPHILA PROTEINS; FEEDBACK, BIOCHEMICAL; GENES, INSECT; LIGHT; MODELS, NEUROLOGICAL; MUTAGENESIS, SITE-DIRECTED; NERVE NET; PHOTORECEPTORS, INVERTEBRATE; TEMPERATURE SENSE;

EID: 34250826602     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-006-0188-9     Document Type: Review

References (87)

1. Robinson B (1986) Withnail and I. Bloomsbury Publishing Film Script
2. Recht LD, Lew RA, Schwartz WJ (1995) Baseball teams beaten by jet lag. Nature 377:583
3. Gorbacheva VY, Kondratov RV, Zhang R, Cherukuri S, Gudkov AV, Takahashi JS, Antoch MP (2005) Circadian sensitivity to the chemotherapeutic agent cyclophosphamide depends on the functional status of the CLOCK/BMAL1 transactivation complex. Proc Natl Acad Sci USA 102:3407-3412
4. Matsuo T, Yamaguchi S, Mitsui S, Emi A, Shimoda F, Okamura H (2003) Control mechanism of the circadian clock for timing of cell division in vivo. Science 302:255-259
5. Fu L, Patel MS, Bradley A, Wagner EF, Karsenty G (2005) The molecular clock mediates leptin-regulated bone formation. Cell 122:803-815
6. Lewy AJ, Lefler BJ, Emens JS, Bauer VK (2006) The circadian basis of winter depression. Proc Natl Acad Sci USA 103:7414-7419
7. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR, Eckel RH, Takahashi JS, Bass J (2005) Obesity and metabolic syndrome in circadian clock mutant mice. Science 308:1043-1045
8. Hansen J (2001) Increased breast cancer risk among women who work predominantly at night. Epidemiology 12:74-77
9. Davis S, Mirick DK, Stevens RG (2001) Night shift work, light at night, and risk of breast cancer. J Natl Cancer Inst 93:1557-1562
10. Schernhammer ES, Laden F, Speizer FE, Willett WC, Hunter DJ, Kawachi I, Colditz GA (2001) Rotating night shifts and risk of breast cancer in women participating in the nurses' health study. J Natl Cancer Inst 93:1563-1568
11. Tsai LT, Bainton RJ, Blau J, Heberlein U (2004) Lmo mutants reveal a novel role for circadian pacemaker neurons in cocaine-induced behaviors. PLoS Biol 2:e408
12. Andretic R, Chaney S, Hirsh J (1999) Requirement of circadian genes for cocaine sensitization in Drosophila. Science 285:1066-1068
13. Abarca C, Albrecht U, Spanagel R (2002) Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc Natl Acad Sci USA 99:9026-9030
14. van Oort BE, Tyler NJ, Gerkema MP, Folkow L, Blix AS, Stokkan KA (2005) Circadian organization in reindeer. Nature 438:1095-1096
15. de Mairan JJ (1729) Observation botanique. Histoire de l'Academie Royale des Sciences, pp 5-36
16. Pittendrigh CS (1954) On temperature independence in the clock system controlling emergence time in Drosophila. Proc Natl Acad Sci USA 40:1018-1029
17. Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 68:2112-2116
18. Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in Cyanobacteria. Proc Natl Acad Sci USA 95:8660-8664
19. DeCoursey PJ, Walker JK, Smith SA (2000) A circadian pacemaker in free-living chipmunks: essential for survival? J Comp Physiol [A] 186:169-180
20. Kyriacou CP, Hall JC (1980) Circadian rhythm mutations in Drosophila melanogaster affect short-term fluctuations in the male's courtship song. Proc Natl Acad Sci USA 77:6729-6733
21. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A, Pack AI (2000) Rest in Drosophila is a sleep-like state. Neuron 25:129-138
22. Waddell S, Quinn WG (2001) Flies, genes, and learning. Annu Rev Neurosci 24:1283-1309
23. Price JL, Blau J, Rothenfluh A, Abodeely M, Kloss B, Young MW (1998) double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94:83-95
24. Vitaterna MH, King DP, Chang AM, Kornhauser JM, Lowrey PL, McDonald JD, Dove WF, Pinto LH, Turek FW, Takahashi JS (1994) Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 264:719-725
25. Tanoue S, Krishnan P, Krishnan B, Dryer SE, Hardin PE (2004) Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr Biol 14:638-649
26. b mutation identifies Cryptochrome as a circadian photoreceptor in Drosophila. Cell 95:681-692
27. Hardin PE (2004) Transcription regulation within the circadian clock: the E-box and beyond. J Biol Rhythms 19:348-360
28. Lee C, Bae K, Edery I (1999) PER and TIM inhibit the DNA binding activity of a Drosophila CLOCK-CYC/dBMAL1 heterodimer without disrupting formation of the heterodimer: a basis for circadian transcription. Mol Cell Biol 19:5316-5325
29. Yu W, Zheng H, Houl JH, Dauwalder B, Hardin PE (2006) PER-dependent rhythms in CLK phosphorylation and E-box binding regulate circadian transcription. Genes Dev 20:723-733
30. Martinek S, Inonog S, Manoukian AS, Young MW (2001) A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 105:769-779
31. Akten B, Jauch E, Genova GK, Kim EY, Edery I, Raabe T, Jackson FR (2003) A role for CK2 in the Drosophila circadian oscillator. Nat Neurosci 6:251-257
32. Lin JM, Kilman VL, Keegan K, Paddock B, Emery-Le M, Rosbash M, Allada R (2002) A role for casein kinase 2α in the Drosophila circadian clock. Nature 420:816-820
33. Sathyanarayanan S, Zheng X, Xiao R, Sehgal A (2004) Posttranslational regulation of Drosophila PERIOD protein by Protein Phosphatase 2A. Cell 116:603-615
34. Ko HW, Jiang J, Edery I (2002) Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature 420:673-678
35. Grima B, Lamouroux A, Chelot E, Papin C, Limbourg-Bouchon B, Rouyer F (2002) The F-box protein Slimb controls the levels of clock proteins Period and Timeless. Nature 420:178-182
36. Emery P, So WV, Kaneko M, Hall JC, Rosbash M (1998) CRY, a Drosophila clock and light-regulated Cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95:669-679
37. Collins B, Mazzoni EO, Stanewsky R, Blau J (2006) Drosophila CRYPTOCHROME is a circadian transcriptional repressor. Curr Biol 16:441-449
38. Kim EY, Edery I (2006) Balance between DBT/CKIε kinase and protein phosphatase activities regulate phosphorylation and stability of Drosophila CLOCK protein. Proc Natl Acad Sci USA 103:6178-6183
39. Glossop NR, Houl JH, Zheng H, Ng FS, Dudek SM, Hardin PE (2003) VRILLE feeds back to control circadian transcription of clock in the Drosophila circadian oscillator. Neuron 37:249-261
40. Cyran SA, Buchsbaum AM, Reddy KL, Lin MC, Glossop NR, Hardin PE, Young MW, Storti RV, Blau J (2003) vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112:329-341
41. Blau J, Young MW (1999) Cycling vrille expression is required for a functional Drosophila clock. Cell 99:661-671
42. Nakajima M, Imai K, Ito H, Nishiwaki T, Murayama Y, Iwasaki H, Oyama T, Kondo T (2005) Reconstitution of circadian oscillation of Cyanobacterial KaiC phosphorylation in vitro. Science 308:414-415
43. Meyer P, Saez L, Young MW (2006) PER-TIM interactions in living Drosophila cells: an interval timer for the circadian clock. Science 311:226-229
44. Curtin KD, Huang ZJ, Rosbash M (1995) Temporally regulated nuclear entry of the Drosophila Period protein contributes to the circadian clock. Neuron 14:365-372
45. Shafer OT, Levine JD, Truman JW, Hall JC (2004) Flies by night: effects of changing day length on Drosophila's circadian clock. Curr Biol 14:424-432
46. Ceriani MF, Darlington TK, Staknis D, Mas P, Petti AA, Weitz CJ, Kay SA (1999) Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science 285:553-556
47. Nawathean P, Menet JS, Rosbash M (2005) Assaying the Drosophila negative feedback loop with RNA interference in S2 cells. Methods Enzymol 393:610-622
48. Cyran SA, Yiannoulos G, Buchsbaum AM, Saez L, Young MW, Blau J (2005) The Double-time protein kinase regulates the subcellular localization of the Drosophila clock protein Period. J Neurosci 25:5430-5437
49. Helfrich-Forster C (2005) Neurobiology of the fruit fly's circadian clock. Genes Brain Behav 4:65-76
50. Helfrich-Forster C, Winter C, Hofbauer A, Hall JC, Stanewsky R (2001) The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30:249-261
51. Emery P, Stanewsky R, Hall JC, Rosbash M (2000) A unique circadian-rhythm photoreceptor. Nature 404:456-457
52. b mutation reveals two circadian clocks that drive locomotor rhythm and have different responsiveness to light. J Insect Physiol 50:479-488
53. Rieger D, Shafer OT, Tomioka K, Helfrich-Forster C (2006) Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 26:2531-2543
54. Koh K, Zheng X, Sehgal A (2006) JETLAG resets the Drosophila circadian clock by promoting light-induced degradation of TIMELESS. Science 312:1809-1812
55. Rosato E, Trevisan A, Sandrelli F, Zordan M, Kyriacou CP, Costa R (1997) Conceptual translation of Timeless reveals alternative initiating methionines in Drosophila. Nucleic Acids Res 25:455-458
56. Peschel N, Veleri S, Stanewsky R (2006) Veela defines a molecular link between Cryptochrome and Timeless in the light input pathway to Drosophila's circadian clock. Proc Natl Acad Sci USA 103:17313-17318
57. Majercak J, Sidote D, Hardin PE, Edery I (1999) How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24:219-230
58. Collins BH, Rosato E, Kyriacou CP (2004) Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C. Proc Natl Acad Sci USA 101:1945-1950
59. Majercak J, Chen WF, Edery I (2004) Splicing of the period gene 3′-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol Cell Biol 24:3359-3372
60. Glaser FT, Stanewsky R (2005) Temperature synchronization of the Drosophila circadian clock. Curr Biol 15:1352-1363
61. Costa R, Peixoto AA, Barbujani G, Kyriacou CP (1992) A latitudinal cline in a Drosophila clock gene. Proc Biol Sci 250:43-49
62. Sawyer LA, Hennessy JM, Peixoto AA, Rosato E, Parkinson H, Costa R, Kyriacou CP (1997) Natural variation in a Drosophila clock gene and temperature compensation. Science 278:2117-2120
63. Hamblen MJ, White NE, Emery PT, Kaiser K, Hall JC (1998) Molecular and behavioral analysis of four period mutants in Drosophila melanogaster encompassing extreme short, novel long, and unorthodox arrhythmic types. Genetics 149:165-178
64. rit lengthens circadian period in a temperature-dependent manner through suppression of PERIOD protein cycling and nuclear localization. Mol Cell Biol 19:4343-4354
65. SL mutant of the Drosophila rhythm gene timeless manifests allele-specific interactions with period gene mutants. Neuron 17:921-929
66. Huang ZJ, Curtin KD, Rosbash M (1995) PER protein interactions and temperature compensation of a circadian clock in Drosophila. Science 267:1169-1172
67. Levine JD, Funes P, Dowse HB, Hall JC (2002) Resetting the circadian clock by social experience in Drosophila melanogaster. Science 298:2010-2012
68. Shafer OT, Helfrich-Forster C, Renn SC, Taghert PH (2006) Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes. J Comp Neurol 498:180-193
69. Peng Y, Stoleru D, Levine JD, Hall JC, Rosbash M (2003) Drosophila free-running rhythms require intercellular communication. PLoS Biol 1:E13
70. Kaneko M, Hall JC (2000) 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
71. Helfrich-Forster C (1998) Robust circadian rhythmicity of Drosophila melanogaster requires the presence of lateral neurons: a brain-behavioral study of disconnected mutants. J Comp Physiol [A] 182:435-453
72. Renn SC, Park JH, Rosbash M, Hall JC, Taghert PH (1999) A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99:791-802
73. Pittendrigh C, Dann S (1976) A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: a clock for all seasons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 106:333-355
74. Stoleru D, Peng Y, Agosto J, Rosbash M (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431:862-868
75. Grima B, Chelot E, Xia R, Rouyer F (2004) Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431:869-873
76. Stoleru D, Peng Y, Nawathean P, Rosbash M (2005) A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 438:238-242
77. Hall JC (2003) Genetics and molecular biology of rhythms in Drosophila and other insects. Adv Genet 48:1-280
78. Lin Y, Stormo GD, Taghert PH (2004) The neuropeptide Pigment Dispersing Factor coordinates pacemaker interactions in the Drosophila circadian system. J Neurosci 24:7951-7957
79. Collins BH, Dissel S, Gaten E, Rosato E, Kyriacou CP (2005) Disruption of Cryptochrome partially restores circadian rhythmicity to the arrhythmic period mutant of Drosophila. Proc Natl Acad Sci USA 102:19021-19026
80. Hyun S, Lee Y, Hong ST, Bang S, Paik D, Kang J, Shin J, Lee J, Jeon K, Hwang S, Bae E, Kim J (2005) Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron 48:67-278
81. Lear BC, Merrill CE, Lin JM, Schroeder A, Zhang L, Allada R (2005) A G protein-coupled receptor, groom-of-PDF, is required for PDF neuron action in circadian behavior. Neuron 48:21-227
82. Mertens I, Vandingenen A, Johnson EC, Shafer OT, Li W, Trigg JS, De Loof A, Schoofs L, Taghert PH (2005) PDF receptor signaling in Drosophila contributes to both circadian and geotactic behaviors. Neuron 48:13-219
83. Mazzoni EO, Desplan C, Blau J (2005) Circadian pacemaker neurons transmit and modulate visual information to control a rapid behavioral response. Neuron 45:93-300
84. Welsh DK, Logothetis DE, Meister M, Reppert SM (1995) Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14:97-706
85. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78-83
86. Nitabach MN, Blau J, Holmes TC (2002) Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109:485-495
87. Nitabach MN, Sheeba V, Vera DA, Blau J, Holmes TC (2005) Membrane electrical excitability is necessary for the free-running larval Drosophila circadian clock. J Neurobiol 62:1-13