Molecular genetics of the fruit-fly circadian clock

European Journal of Human Genetics

Volumn 14, Issue 6, 2006, Pages 729-738

  Rosato, Ezio ^a   Tauber, Eran ^a   Kyriacou, Charalambos P ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Circadian clock; Drosophila; Molecular genetics

Indexed keywords

BETA CATENIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA TOPOISOMERASE; GENE PRODUCT; HYBRID PROTEIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; ISOPROTEIN; MESSENGER RNA; NEUROPEPTIDE; RHODOPSIN; TRANSCRIPTION FACTOR; VASOACTIVE INTESTINAL POLYPEPTIDE;

BEHAVIOR GENETICS; CHRONOBIOLOGY; CIRCADIAN RHYTHM; CIRCADIAN RHYTHM SLEEP DISORDER; DROSOPHILA; EVOLUTIONARY HOMOLOGY; GENE DUPLICATION; GENETIC MODEL; GENETIC SIMILARITY; GENETIC VARIABILITY; HUMAN; LIGHT; MAMMAL; MOLECULAR CLOCK; MOLECULAR GENETICS; MOLECULAR MECHANICS; MOLECULAR PHYLOGENY; MUTATIONAL ANALYSIS; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NONHUMAN; PHYLUM; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION; SPECIES COMPARISON;

ANIMALS; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; DROSOPHILA; EVOLUTION, MOLECULAR; HUMANS; SPECIES SPECIFICITY;

ANIMALIA; MAMMALIA;

EID: 33744454649     PISSN: 10184813     EISSN: 14765438     Source Type: Journal    
DOI: 10.1038/sj.ejhg.5201547     Document Type: Review

References (135)

1. Hastings MHC Reddy AB, Maywood ES: A clockwork web: circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci 2003; 4: 649-661.
2. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G: Correlates of sleep and waking in Drosophila melanogaster. Science 2000; 287: 1834-1837.
3. Shaw PJ, Tononi G, Greenspan RJ, Robinson DF: Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 2002; 417: 287-291.
4. Hendricks JC, Finn SM, Panckeri KA et al: Rest in Drosophila is a sleep-like state. Neuron 2000; 25: 129-138.
5. Hendricks JC, Williams JA, Panckeri K et al: A non-circadian role for cAMP signaling and CREB activity in Drosophila rest homeostasis. Nat Neurosci 2001; 4: 1108-1115.
6. Tsai LT, Bainton RJ, Blau J, Heberlein U: Lmo mutants reveal a novel role for circadian pacemaker neurons in cocaine-induced behaviors. PLoS Biol 2004; 2: E408.
7. Andretic R, Chaney S, Hirsh J: Requirement of circadian genes for cocaine sensitization in Drosophila. Science 1999; 285: 1066-1068.
8. Toh KL, Jones CR, He Y et al: An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 2001; 291: 1040-1043.
9. Konopka RJ, Benzer S: Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 1971; 68: 2112-2116.
10. Yu Q, Jacquier AC, Citri Y, Hamblen M, Hall JC, Rosbash M: Molecular mapping of point mutations in the period gene that stop or speed up biological clocks in Drosophila melanogaster. Proc Natl Acad Sci USA 1987; 84: 784-788.
11. Rothenfluh A, Abodeely M, Young MW: Short-period mutations of per affect a double-time-dependent step in the Drosophila circadian clock. Curr Biol 2000; 10: 1399-1402.
12. Clayton JD, Kyriacou CP, Reppert SM: Keeping time with the human genome. Nature 2001; 409: 829-831.
13. Gotter AL, Reppert SM: Analysis of human Per4. Brain Res Mol Brain Res 2001; 92: 19-26.
14. Xu Y, Padiath QS, Shapiro RE et al: Functional consequences of a CKI delta mutation causing familial advanced sleep phase syndrome. Nature 2005; 434: 640-644.
15. Price JL, Blau J, Rothenfluh A, Abodeely M, Kloss B, Young MW: double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell 1998; 94: 83-95.
16. Vitaterna MH, King DP, Chang AM et al: Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 1994; 264: 719-725.
17. Antoch MP, Song EJ, Chang AM et al: Functional identification of the mouse circadian Clock gene by transgenic BAC rescue. Cell 1997; 89: 655-667.
18. King DP, Zhao Y, Sangoram AM et al: Positional cloning of the mouse circadian clock gene. Cell 1997; 89: 641-653.
19. Allada R, White NE, So WV, Hall JC, Rosbash M: A mutant Drosophila homolog of mammalian Clock disrupts circadian rhythms and transcription of period and timeless. Cell 1998; 93: 791-804.
20. Kyriacou CP, Hall JC: Circadian rhythm mutations in Drosophila melanogaster affect short-term fluctuations in the male's courtship song. Proc Natl Acad Sci USA 1980; 77: 6729-6733.
21. Kyriacou CP. Oldroyd M, Wood J, Sharp M, Hill M: Clock mutations alter developmental timing in Drosophila. Heredity 1990; 64 (Part 3): 395-401.
22. Beaver LM, Giebultowicz JM: Regulation of copulation duration by period and timeless in Drosophila melanogaster. Curr Biol 2004; 14: 1492-1497.
23. Beaver LM, Gvakharia BO, Vollintine TS, Hege DM, Stanewsky R, Giebultowicz JM: Loss of circadian clock function decreases reproductive fitness in males of Drosophila melanogaster. Proc Natl Acad Sci USA 2002; 99: 2134-2139.
24. Bargiello TA, Jackson FR, Young MW: Restoration of circadian behavioural rhythms by gene transfer in Drosophila. Nature 1984; 312: 752-754.
25. Zehring WA, Wheeler DA, Reddy P et al: P-element transformation with period locus DNA restores rhythmicity to mutant, arrhythmic Drosophila melanogaster. Cell 1984; 39: 369-376.
26. Sehgal A, Price JL, Man B, Young MW: Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 1994; 263: 1603-1606.
27. Myers MP, Wager-Smith K, Wesley CS, Young MW, Sehgal A: Positional cloning and sequence analysis of the Drosophila clock gene, timeless. Science 1995; 270: 805-808.
28. Gekakis N, Saez L, Delahaye-Brown AM et al: Isolation of timeless by PER protein interaction: Defective interaction between timeless protein and long-period mutant PERL. Science 1995; 270: 811-815.
29. Huang ZJ, Edery I, Rosbash M: PAS is a dimerization domain common to Drosophila period and several transcription factors. Nature 1993; 364: 259-262.
30. Pellequer JL, Mrudler R, Getzoff ED: Biological sensors: more than one way to sense oxygen. Curr Biol 1999; 9: R416-R418.
31. Pellequer JL, Wager-Smith KA, Kay SA, Getzoff ED: Photoactive yellow protein: A structural prototype for the three-dimensional fold of the PAS domain superfamily. Proc Natl Acad Sci USA 1998; 95: 5884-5890.
32. Crosson S, RajagoPal S, Moffat K: The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 2003; 42: 2-10.
33. Gehring W, Rosbash M: The coevolution of blue-light photoreception and circadian rhythms. J Mol Evol 2003; 57 (Suppl 1): S286-S289.
34. Hardin PE, Hall JC, Rosbash M: Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 1990; 343: 536-540.
35. Edery I, Zwiebel LJ, Dembinska ME, Rosbash M: Temporal phosphorylation of the Drosophila period protein. Proc Natl Acad Sci USA 1994; 91: 2260-2264.
36. Sehgal A, Rothenfluh-Hilfiker A, Hunter-Ensor M, Chen Y, Myers MP, Young MW: Rhythmic expression of Aimeless: a basis for promoting circadian cycles in period gene autoregulation. Science 1995; 270: 808-810.
37. Myers MP, Wager-Smith K, Rothenfluh-Hilfiker A, Young MW: Light-induced degradation of TIMELESS and entrainment of the Drosophila circadian clock. Science 1996; 271: 1736-1740.
38. Curtin KD, Huang ZJ, Rosbash M: Temporally regulated nuclear entry of the Drosophila period protein contributes to the circadian clock. Neuron 1995; 14: 365-372.
39. Siwicki KK, Eastman C, Petersen G, Rosbash M, Hall JC: Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron 1988; 1: 141-150.
40. Zerr DM, Hall JC, Rosbash M, Siwicki KK: Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J Neurosci 1990; 10: 2749-2762.
41. Rothenfluh A, Young MW, Saez L: A TIMELESS-independent function for PERIOD proteins in the Drosophila clock. Neuron 2000; 26: 505-514.
42. Hastings M, Maywood ES: Circadian clocks in the mammalian brain. Bioessays 2000; 22: 23-31.
43. Rutila JE, Suri V, Le M, So WV, Rosbash M, Hall JC: CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 1998; 93: 805-814.
44. Lee C, Bae K, Edery I: PER and TIM inhibit the DNA binding activity of a Drosophila CLOCK-CYC/dBMALl heterodimer without disrupting formation of the heterodimer: A basis for circadian transcription. Mol Cell Biol 1999; 19: 5316-5325.
45. Chang DC, Reppert SM: A novel C-terminal domain of Drosophila PERIOD inhibits dCLOCK : CYCLE-mediated transcription. Current Biology 2003; 13: 758-762.
46. Kloss B, Price JL, Saez L et al: The Drosophila clock gene double-time encodes a protein closely related to human casein kinase I epsilon. Cell 1998; 94: 97-107.
47. Akten B, Jauch E, Genova GK et al: A role for CK2 in the Drosophila circadian oscillator. Nat Neurosci 2003; 6: 251-257.
48. Lin JM, Kilman VL, Keegan K et al: A role for casein kinase 2alpha in the Drosophila circadian clock. Nature 2002; 420: 816-820.
49. s mutation delays the nuclear accumulation of period protein and affects the feedback regulation of period mRNA. J Neurosci 2001; 21: 7117-7126.
50. Sathyanarayanan S, Zheng X, Xiao R, Sehgal A: Posttranslational regulation of Drosophila PERIOD protein by protein phosphatase 2A. Cell 2004; 116: 603-615.
51. 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.
52. Ko HW, Jiang J, Edery I: Role for Slimb in the degradation of Drosophila period protein phosphorylated by Doubletime. Nature 2002; 420: 673-678.
53. Martinek S, Inonog S, Manoukian AS, Young MW: A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 2001; 105: 769-779.
54. Cyran SA, Yiannoulos G, Buchsbaum AM, Saez L, Young MW, Blau J: The double-time protein kinase regulates the subcellular localization of the Drosophila clock protein period. J Neurosci 2005; 25: 5430-5437.
55. Ashmore LJ, Sathyanarayanan S, Silvestre DW, Emerson MM, Schotland P, Sehgal A: Novel insights into the regulation of the timeless protein. J Neurosci 2003; 23: 7810-7819.
56. Shafer OT, Rosbash M, Truman JW: Sequential nuclear accumulation of the clock proteins period and timeless in the pace-maker neurons of Drosophila melanogaster. J Neurosci 2002; 22: 5946-5954.
57. Saez L, Young MW: Regulation of nuclear entry of the Drosophila clock proteins period and timeless. Neuron 1996; 17: 911-920.
58. Glossop NR, Lyons LC, Hardin PE: Interlocked feedback loops within the Drosophila circadian oscillator. Science 1999; 286: 766-768.
59. Cyran SA, Buchsbaum AM, Reddy KL et al: Vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 2003; 112: 329-341.
60. Rosato E, Codd V, Mazzotta G et al: Light-dependent interaction between Drosophila CRY and the clock protein PER mediated by the carboxy terminus of CRY. Curr Biol 2001; 11: 909-917.
61. Ceriani MF, Darlington TK, Staknis D et al: Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science 1999; 285: 553-556.
62. 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.
63. Lin FJ, Song W, Meyer-Bernstein E, Naidoo N, Sehgal A: Photic signaling by cryptochrome in the Drosophila circadian system. Mol Cell Biol 2001; 21: 7287-7294.
64. b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 1998; 95: 681-692.
65. Dissel S, Codd V, Fedic R et al: A constitutively active cryptochrome in Drosophila melanogaster. Nat Neurosci 2004; 7: 834-840.
66. Emery P, Stanewsky R, Hall JC, Rosbash M: A unique circadian-rhythm photoreceptor. Nature 2000; 404: 456-457.
67. Yang Z, Emerson M, Su HS, Sehgal A: Response of the timeless protein to light correlates with behavioral entrainment and suggests a nonvisual pathway for circadian photoreception. Neuron 1998; 21: 215-223.
68. Suri V, Qian Z, Hall JC, Rosbash M: Evidence that the TIM light response is relevant to light-induced phase shifts in Drosophila melanogaster. Neuron 1998; 21: 225-234.
69. 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.
70. Zeng H, Qian Z, Myers MP, Rosbash M: A light-entrainment mechanism for the Drosophila circadian clock. Nature 1996; 380: 129-135.
71. Plautz JD, Kaneko M, Hall JC, Kay SA: Independent photoreceptive circadian clocks throughout Drosophila. Science 1997; 278: 1632-1635.
72. Akhtar RA, Reddy AB, Maywood ES et al: Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 2002; 12: 540-550.
73. Yamazaki S, Numano R, Abe M et al: Resetting central and peripheral circadian oscillators in transgenic rats. Science 2000; 288: 682-685.
74. Yoo SH, Yamazaki S, Lowrey PL et al: PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA 2004; 101: 5339-5346.
75. Krishnan B, Levine JD, Lynch MK et al: A new role for cryptochrome in a Drosophila circadian oscillator. Nature 2001; 411: 313-317.
76. Shearman LP, Sriram S, Weaver DR et al: Interacting molecular loops in the mammalian circadian clock. Science 2000; 288: 1013-1019.
77. Sato TK, Panda S, Miraglia LJ et al: A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 2004; 43: 527-537.
78. Preitner N, Damiola F, Lopez-Molina L et al: The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 2002; 110: 251-260.
79. Looby P, Loudon AS: Gene duplication and complex circadian clocks in mammals. Trends Genet 2005; 21: 46-53.
80. Tauber E, Last KS, Olive PJ, Kyriacou CP: Clock gene evolution and functional divergence. J Biol Rhythms 2004; 19: 445-458.
81. Ohno S: Evolution by Gene Duplication. London, New York: Allen & Unwin, Springer-Verlag, 1970.
82. Shearman LP, Jin X, Lee C, Reppert SM, Weaver DR: Targeted disruption of the mPer3 gene: Subtle effects on circadian clock function. Mol Cell Biol 2000; 20: 6269-6275.
83. Zylka MJ, Shearman LP, Weaver DR, Reppert SM: Three period homologs in mammals: Differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron 1998; 20: 1103-1110.
84. Bae K, Jin X, Maywood ES, Hastings MH, Reppert SM, Weaver DR: Differential functions of mPer1, mPer2, and mPer3 in the SCN circadian clock. Neuron 2001; 30: 525-536.
85. Masubuchi S, Kataoka N, Sassone-Corsi P, Okamura H: Mouse Period1 (mPER1) acts as a circadian adaptor to entrain the oscillator to environmental light/dark cycles by regulating mPER2 protein. J Neurosci 2005; 25: 4719-4724.
86. Gotter AL, Levine JD, Reppert SM: Sex-linked period genes in the silkmoth, Antheraea pernyi: Implications for circadian clock regulation and the evolution of sex chromosomes. Neuron 1999; 24: 953-965.
87. Benna C, Scannapieco P, Piccin A et al: A second timeless gene in Drosophila shares greater sequence similarity with mammalian tim. Curr Biol 2000; 10: R512-R513.
88. Gotter AL, Manganaro T, Weaver DR et al: A time-less function for mouse timeless. Nat Neurosci 2000; 3: 755-756.
89. Barnes JW, Tischkau SA, Barnes JA et al: Requirement of mammalian timeless for circadian rhythmicity. Science 2003; 302: 439-442.
90. Unsal-Kacmaz K, Mullen TE, Kaufmann WK, Sancar A: Coupling of human circadian and cell cycles by the timeless protein. Mol Cell Biol 2005; 25: 3109-3116.
91. Krings G, Bastia D: Swi1- and swi3-dependent and independent replication fork arrest at the ribosomal DNA of Schizosaccharomyces pombe. Proc Natl Acad Sci USA 2004; 101: 14085-14090.
92. Katou Y, Kanoh Y, Bando M et al: S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 2003; 424: 1078-1083.
93. Chan RC, Chan A, Jeon M et al: Chromosome cohesion is regulated by a clock gene paralogue TIM-1. Nature 2003; 424: 1002-1009.
94. Perry J: Weighing in on a Timeless controversy. Proteins 2005 (in Press).
95. Kyriacou CP, Odell M: No ARM in it ? Reply to Kippert and Gerloff. Curr Biol 2004; 14: R652-R653.
96. Vodovar N, Clayton JD, Costa R, Odell M, Kyriacou CP: The Drosophila clock protein Timeless is a member of the Arm/HEAT family. Curr Biol 2002; 12: R610-R611.
97. Kippert F, GerloffADL: Timeless and Armadillo: a link too far [Comment on Vodovar et al (2002) Curr Biol 12; R610-R611]. Curr Biol (2004); 14: R650-R651; author reply R652-R653.
98. Kopelman NM, Lancet D, Yanai I: Alternative splicing and gene duplication are inversely correlated evolutionary mechanisms. Nat Genet 2005; 37: 588-589.
99. Collins BH, Rosato E, Kyriacou CP: Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C. Proc Natl Acad Sci USA 2004; 101: 1945-1950.
100. Majercak J, Chen WF, 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.
101. Majercak J, Sidote D, Hardin PE, Edery I: How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 1999; 24: 219-230.
102. Kaneko M, Helfrich-Forster 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 1997; 17: 6745-6760.
103. Ewer J, Frisch B, Hamblen-Coyle MJ, Rosbash M, Hall JC: 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.
104. Helfrich-Forster C: Robust circadian rhythmicity of Drosophila melanogaster requires the presence of lateral neurons: A brain-behavioral study of disconnected mutants. J Comp Physiol A 1998; 182: 435-453.
105. 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 USA 1995; 92: 612-616.
106. Renn SC, 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 1999; 99: 791-802.
107. Park JH, Helfrich-Forster C, Lee G, Liu L, Rosbash M, Hall JC: Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Natl Acad Sci USA 2000; 97: 3608-3613.
108. Lin Y, Stormo GD, Taghert PH: The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J Neurosci 2004; 24: 7951-7957.
109. Helfrich-Forster C: Neurobiology of the fruit fly's circadian clock. Genes Brain Behav 2005; 4: 65-76.
110. Helfrich-Forster C: The neuroarchitecture of the circadian clock in the brain of Drosophila melanogaster. Microsc Res Technol 2003; 62: 94-102.
111. 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 2000; 422: 66-94.
112. Helfrich-Forster C, Edwards T, Yasuyama K et al: The extraretinal eyelet of Drosophila: Development, ultrastructure, and putative circadian function. J Neurosci 2002; 22: 9255-9266.
113. Veleri S, Brandes C, Helfrich-Forster C, Hall JC, Stanewsky R: A self-sustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr Biol 2003; 13: 1758-1767.
114. Miskiewicz K, Pyza E, Schurmann FW: Ultrastructural characteristics of circadian pacemaker neurones, immunoreactive to an antibody against a pigment-dispersing hormone in the fly's brain. Neurosci Lett 2004; 363: 73-77.
115. Kaneko M, Park JH, Cheng Y, Hardin PE, Hall JC: Disruption of synaptic transmission or clock-gene-product oscillations in circadian pacemaker cells of Drosophila cause abnormal behavioral rhythms. J Neurobiol 2000; 43: 207-233.
116. Piggins HD, Antle MC, Rusak B: Neuropeptides phase shift the mammalian circadian pacemaker. J Neurosci 1995; 15: 5612-5622.
117. Piggins HD, Marchant EG, Goguen D, Rusak B: Phase-shifting effects of pituitary adenylate cyclase activating polypeptide on hamster wheel-running rhythms. Neurosci Lett 2001; 305: 25-28.
118. Shen S, Spratt C, Sheward WJ et al: Overexpression of the human VPAC2 receptor in the suprachiasmatic nucleus alters the circadian phenotype of mice. Proc Natl Acad Sci USA 2000; 97: 11575-11580.
119. Romijn HJ, Sluiter AA, Pool CW, Wortel J, Buijs RM: Differences in colocalization between Fos and PHI, GRP, VIP and VP in neurons of the rat suprachiasmatic nucleus after a light stimulus during the phase delay versus the phase advance period of the night. J Comp Neurol 1996; 372: 1-8.
120. Hannibal J: Pituitary adenylate cyclase-activating peptide in the rat central nervous system: An immunohistochemical and in situ hybridization study. J Comp Neurol 2002; 453: 389-417.
121. Harmar AJ, Marston HM, Shen S et al: The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 2002; 109: 497-508.
122. Aton SJ, Colwell CS, Harmar AJ, Waschek J, Herzog ED: Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat Neurosci 2005; 8: 476-483.
123. Stoleru D, Peng Y, Agosto J, Rosbash M: Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 2004; 431: 862-868.
124. 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.
125. Lee HS, Billings HJ, LeAman MN: The suprachiasmatic nucleus: a clock of multiple components. J Biol Rhythms 2003; 18: 435-449.
126. Jagota A, de la Iglesia HO, Schwartz WJ: Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro. Nat Neurosci 2000; 3: 372-376.
127. Pittendrigh C, Daan S: A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: A clock for all seasons. J Comp Physiol A 1976; 106: 333-355.
128. Daan S, Berde C: TwS coupled oscillators: simulations of the circadian pacemaker in mammalian activity rhythms. J Theor Biol 1978; 70: 297-313.
129. Ueda HR, 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.
130. Lin Y, Han M, Shimada B et al: Influence of the period-dependent circadian clock on diurnal, circadian, and aperiodic gene expression in Drosophila melanogaster. Proc Natl Acad Sci USA 2002; 99: 9562-9567.
131. Ceriani MF, Hogenesch JB, Yanovsky M, Panda S, Straume M, Kay SA: Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. J Neurosci 2002; 22: 9305-9319.
132. Claridge-Chang A, Wijnen H, Naef F, Boothroyd C, Rajewsky N, Young MW: Circadian regulation of gene expression systems in the Drosophila head. Neuron 2001; 32: 657-671.
133. McDonald MJ, Rosbash M: Microarray analysis and organization of circadian gene expression in Drosophila. Cell 2001; 107: 567-578.
134. Levine JD, Funes P, Dowse HB, Hall JC: Resetting the circadian clock by social experience in Drosophila melanogaster. Science 2002; 298: 2010-2012.
135. Stanewsky R, Frisch B, Brandes C, Hamblen-Coyle MJ, Rosbash M, Hall JC: Temporal and spatial expression patterns of transgenes containing increasing amounts of the Drosophila clock gene period and a lacZ reporter: Mapping elements of the PER protein involved in circadian cycling. J Neurosci 1997; 17: 676-696.