A role for the period: Period homodimer in the Drosophila circadian clock

PLoS Biology

Volumn 7, Issue 4, 2009, Pages 0820-0835

  Landskron, Johannes ^a,d   Chen, Ko Fan ^b   Wolf, Eva ^c   Stanewsky, Ralf ^a,b  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; HOMODIMER; PER PROTEIN; PROTEIN TIMELESS; UNCLASSIFIED DRUG; CASEIN KINASE II; CIRCADIAN RHYTHM SIGNALING PROTEIN; NUCLEAR PROTEIN; PER PROTEIN, DROSOPHILA; TIMELESS PROTEIN, DROSOPHILA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CIRCADIAN RHYTHM; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; GENETIC TRANSCRIPTION; MALE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; ANIMAL; BIOLOGICAL RHYTHM; CELL NUCLEUS; CHEMISTRY; DROSOPHILA MELANOGASTER; FEEDBACK SYSTEM; GENE; GENE EXPRESSION REGULATION; GENETICS; LOCOMOTION; METABOLISM; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE;

EUKARYOTA;

ANIMALS; BIOLOGICAL CLOCKS; CASEIN KINASE II; CELL NUCLEUS; CIRCADIAN RHYTHM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; GENES, INSECT; LOCOMOTION; NUCLEAR PROTEINS; PERIOD CIRCADIAN PROTEINS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY;

EID: 65949100602     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000003     Document Type: Article

References (83)

1. Dunlap JC, Loros JJ, DeCoursey PJ (2004) Chronobiology: biological timekeeping. Sunderland (Massachusetts): Sinauer Associates, Inc.
2. Hardin PE (2006) Essential and expendable features of the circadian timekeeping mechanism. Curr Opin Neurobiol 16: 686-692.
3. Stanewsky R (2003) Genetic analysis of the circadian system in Drosophila melanogaster and mammals. J Neurobiol 54: 111-147.
4. Hall JC (2003) Genetics and molecular biology of rhythms in Drosophila and other insects. Adv Genet 48: 1-280.
5. Zeng H, Qian Z, Myers MP, Rosbash M (1996) A light-entrainment mechanism for the Drosophila circadian clock. Nature 380: 129-135.
6. Sehgal A, Price JL, Man B, Young MW (1994) Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 263: 1603-1606.
7. Price JL, Dembinska ME, Young MW, Rosbash M (1995) Suppression of PERIOD protein abundance and circadian cycling by the Drosophila clock mutation timeless. Embo J 14: 4044-4049.
8. Vosshall LB, Price JL, Sehgal A, Saez L, Young MW (1994) Block in nuclear localization of period protein by a second clock mutation, timeless. Science 263: 1606-1609.
9. Sehgal A, Rothenfluh-Hilfiker A, Hunter-Ensor M, Chen Y, Myers MP, et al. (1995) Rhythmic expression of timeless: a basis for promoting circadian cycles in period gene autoregulation. Science 270: 808-810.
10. 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.
11. Saez L, Young MW (1996) Regulation of nuclear entry of the Drosophila clock proteins PERIOD and TIMELESS. Neuron 17: 911-920.
12. Darlington TK, Wager-Smith K, Ceriani MF, Staknis D, Gekakis N, et al. (1998) Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 280: 1599-1603.
13. Rothenfluh A, Young MW, Saez L (2000) A TIMELESS-independent function for PERIOD proteins in the Drosophila clock. Neuron 26: 505-514.
14. Nawathean P, Rosbash M (2004) The doubletime and CKII kinases collaborate to potentiate Drosophila PER transcriptional repressor activity. Mol Cell 13: 213-223.
15. Chang DC, Reppert SM (2003) A novel C-terminal domain of Drosophila PERIOD inhibits dCLOCK:CYCLE-mediated transcription. Curr Biol 13: 758-762.
16. Shafer OT, Rosbash M, Truman JW (2002) Sequential nuclear accumulation of the clock proteins period and timeless in the pacemaker neurons of Drosophila melanogaster. J Neurosci 22: 5946-5954.
17. 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.
18. Weber F, Kay SA (2003) A PERIOD inhibitor buffer introduces a delay mechanism for CLK/CYC-activated transcription. FEBS Lett 555: 341-345.
19. Cyran SA, Buchsbaum AM, Reddy KL, Lin MC, Glossop NR, et al. (2003) vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112: 329-341.
20. Cyran SA, Yiannoulos G, Buchsbaum AM, Saez L, Young MW, et al. (2005) The double-time protein kinase regulates the subcellular localization of the Drosophila clock protein period. J Neurosci 25: 5430-5437.
21. McDonald MJ, Rosbash M (2001) Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107: 567-578.
22. Kloss B, Price JL, Saez L, Blau J, Rothenfluh A, et al. (1998) The Drosophila clock gene double-time encodes a protein closely related to human casein kinase Ie. Cell 94: 97-107.
23. Kloss B, Rothenfluh A, Young MW, Saez L (2001) Phosphorylation of PERIOD is influenced by cycling physical associations of DOUBLE-TIME, PERIOD, and TIMELESS in the Drosophila clock. Neuron 30: 699-706.
24. Chiu JC, Vanselow JT, Kramer A, Edery I (2008) The phospho-occupancy of an atypical SLIMB-binding site on PERIOD that is phosphorylated by DOUBLETIME controls the pace of the clock. Genes Dev 22: 1758-1772.
25. Kivimae S, Saez L, Young MW (2008) Activating PER repressor through a DBT-directed phosphorylation switch. PLoS Biol 6: e183. doi:10.1371/journal. pbio.0060183
26. 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.
27. Kim EY, Edery I (2006) Balance between DBT/CKIe kinase and protein phosphatase activities regulate phosphorylation and stability of Drosophila CLOCK protein. Proc Natl Acad Sci U S A 103: 6178-6183.
28. Kim EY, Ko HW, Yu W, Hardin PE, Edery I (2007) A DOUBLE-TIME kinase binding domain on the Drosophila PERIOD protein is essential for its hyperphosphorylation, transcriptional repression, and circadian clock function. Mol Cell Biol 27: 5014-5028.
29. Nawathean P, Stoleru D, Rosbash M (2007) A small conserved domain of Drosophila PERIOD is important for circadian phosphorylation, nuclear localization, and transcriptional repressor activity. Mol Cell Biol 27: 5002-5013.
30. Akten B, Jauch E, Genova GK, Kim EY, Edery I, et al. (2003) A role for CK2 in the Drosophila circadian oscillator. Nat Neurosci 6: 251-257.
31. Lin JM, Kilman VL, Keegan K, Paddock B, Emery-Le M, et al. (2002) A role for casein kinase 2a in the Drosophila circadian clock. Nature 420: 816-820.
32. Lin JM, Schroeder A, Allada R (2005) In vivo circadian function of casein kinase 2 phosphorylation sites in Drosophila PERIOD. J Neurosci 25: 11175-11183.
33. Smith EM, Lin JM, Meissner RA, Allada R (2008) Dominant-negative CK2a induces potent effects on circadian rhythmicity. PLoS Genet 4: e12. doi:10. 1371/journal.pgen. 0040012
34. Sathyanarayanan S, Zheng X, Xiao R, Sehgal A (2004) Posttranslational regulation of Drosophila PERIOD protein by protein phosphatase 2A. Cell 116: 603-615.
35. Kadener S, Stoleru D, McDonald M, Nawathean P, Rosbash M (2007) Clockwork Orange is a transcriptional repressor and a new Drosophila circadian pacemaker component. Genes Dev 21: 1675-1686.
36. Lim C, Chung BY, Pitman JL, McGill JJ, Pradhan S, et al. (2007) clockwork orange encodes a transcriptional repressor important for circadian-clock amplitude in Drosophila. Curr Biol 17: 1082-1089.
37. Matsumoto A, Ukai-Tadenuma M, Yamada RG, Houl J, Uno KD, et al. (2007) A functional genomics strategy reveals clockwork orange as a transcriptional regulator in the Drosophila circadian clock. Genes Dev 21: 1687-1700.
38. Richier B, Michard-Vanhee C, Lamouroux A, Papin C, Rouyer F (2008) The Clockwork orange Drosophila protein functions as both an activator and a repressor of clock gene expression. J Biol Rhythms 23: 103-116.
39. 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.
40. Wülbeck C, Szabo G, Shafer OT, Helfrich-Forster C, Stanewsky R (2005) The novel Drosophila timblind mutation affects behavioral rhythms but not periodic eclosion. Genetics 169: 751-766.
41. Muskus MJ, Preuss F, Fan JY, Bjes ES, Price JL (2007) Drosophila DBT lacking protein kinase activity produces long-period and arrhythmic circadian behavioral and molecular rhythms. Mol Cell Biol 27: 8049-8064.
42. Huang ZJ, Curtin KD, Rosbash M (1995) PER protein interactions and temperature compensation of a circadian clock in Drosophila. Science 267: 1169-1172.
43. Huang ZJ, Edery I, Rosbash M (1993) PAS is a dimerization domain common to Drosophila PERIOD and several transcription factors. Nature 364: 259-262.
44. Yildiz O, Doi M, Yujnovsky I, Cardone L, Berndt A, et al. (2005) Crystal structure and interactions of the PAS repeat region of the Drosophila clock protein PERIOD. Mol Cell 17: 69-82.
45. Baylies MK, Bargiello TA, Jackson FR, Young MW (1987) Changes in abundance or structure of the per gene product can alter periodicity of the Drosophila clock. Nature 326: 390-392.
46. Gekakis N, Saez L, Delahaye-Brown AM, Myers MP, Sehgal A, et al. (1995) Isolation of timeless by PER protein interaction: defective interaction between TIMELESS protein and long-period mutant PERL. Science 270: 811-815.
47. 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.
48. Hao H, Allen DL, Hardin PE (1997) A circadian enhancer mediates PER-dependent mRNA cycling in Drosophila melanogaster. Mol Cell Biol 17: 3687-3693.
49. Hao H, Glossop NR, Lyons L, Qiu J, Morrish B, et al. (1999) The 69 bp circadian regulatory sequence (CRS) mediates per-like developmental, spatial, and circadian expression and behavioral rescue in Drosophila. J Neurosci 19: 987-994.
50. Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 68: 2112-2116.
51. Edery I, Zwiebel LJ, Dembinska ME, Rosbash M (1994) Temporal phosphorylation of the Drosophila period protein. Proc Natl Acad Sci U S A 91: 2260-2264.
52. Stanewsky R, Frisch B, Brandes C, Hamblen-Coyle MJ, Rosbash M, et al. (1997) 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 17: 676-696.
53. Konopka RJ, Pittendrigh C, Orr D (1989) Reciprocal behaviour associated with altered homeostasis and photosensitivity of Drosophila clock mutants. J Neurogenet 6: 1-10.
54. Hamblen-Coyle MJ, Wheeler DA, Rutila JE, Rosbash M, Hall JC (1992) Behavior of period-altered circadian rhythm mutants of Drosophila in light:dark cycles. J Insect Behav 5: 417-446.
55. 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.
56. Brandes C, Plautz JD, Stanewsky R, Jamison CF, Straume M, et al. (1996) Novel features of Drosophila period transcription revealed by real-time luciferase reporting. Neuron 16: 687-692.
57. Stanewsky R, Jamison CF, Plautz JD, Kay SA, Hall JC (1997) Multiple circadian-regulated elements contribute to cycling period gene expression in Drosophila. Embo J 16: 5006-5018.
58. Chang DC (2006) Neural circuits underlying circadian behavior in Drosophila melanogaster. Behav Processes 71: 211-225.
59. Rutila JE, Maltseva O, Rosbash M (1998) The timSL mutant affects a restricted portion of the Drosophila melanogaster circadian cycle. J Biol Rhythms 13: 380-392.
60. Rutila JE, Zeng H, Le M, Curtin KD, Hall JC, et al. (1996) The timSL mutant of the Drosophila rhythm gene timeless manifests allele-specific interactions with period gene mutants. Neuron 17: 921-929.
61. Kaushik R, Nawathean P, Busza A, Murad A, Emery P, et al. (2007) PER-TIM interactions with the photoreceptor cryptochrome mediate circadian temperature responses in Drosophila. PLoS Biol 5: e146. doi:10.1371/journal.pbio. 0050146
62. Meissner RA, Kilman VL, Lin JM, Allada R (2008) TIMELESS is an important mediator of CK2 effects on circadian clock function in vivo. J Neurosci 28: 9732-9740.
63. 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.
64. Helfrich-Förster 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.
65. Schotland P, Hunter-Ensor M, Lawrence T, Sehgal A (2000) Altered entrainment and feedback loop function effected by a mutant period protein. J Neurosci 20: 958-968.
66. Ashmore LJ, Sathyanarayanan S, Silvestre DW, Emerson MM, Schotland P, et al. (2003) Novel insights into the regulation of the timeless protein. J Neurosci 23: 7810-7819.
67. Vielhaber EL, Duricka D, Ullman KS, Virshup DM (2001) Nuclear export of mammalian PERIOD proteins. J Biol Chem 276: 45921-45927.
68. Rosato E, Codd V, Mazzotta G, Piccin A, Zordan M, et al. (2001) Lightdependent interaction between Drosophila CRY and the clock protein PER mediated by the carboxy terminus of CRY. Curr Biol 11: 909-917.
69. Busza A, Emery-Le M, Rosbash M, Emery P (2004) Roles of the two Drosophila CRYPTOCHROME structural domains in circadian photoreception. Science 304: 1503-1506.
70. Kivimäe S, Saez L, Young MW (2008) Activating PER repressor through a DBT-directed phosphorylation switch. PLoS Biol 6: e183. doi:10.1371/journal. pbio.0060183
71. Fang Y, Sathyanarayanan S, Sehgal A (2007) Post-translational regulation of the Drosophila circadian clock requires protein phosphatase 1 (PP1). Genes Dev 21: 1506-1518.
72. Collins B, Mazzoni EO, Stanewsky R, Blau J (2006) Drosophila CRYPTO-CHROME is a circadian transcriptional repressor. Curr Biol 16: 441-449.
73. Kume K, Zylka MJ, Sriram S, Shearman LP, Weaver DR, et al. (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98: 193-205.
74. Field MD, Maywood ES, O'Brien JA, Weaver DR, Reppert SM, et al. (2000) Analysis of clock proteins in mouse SCN demonstrates phylogenetic divergence of the circadian clockwork and resetting mechanisms. Neuron 25: 437-447.
75. Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. San Diego: Academic Press.
76. Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218: 348-353.
77. Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz DM, Benz WK, et al. (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118: 461-470.
78. Levine JD, Funes P, Dowse HB, Hall JC (2002) Signal analysis of behavioral and molecular cycles. BMC Neurosci 3: 1.
79. Levine JD, Funes P, Dowse HB, Hall JC (2002) Advanced analysis of a cryptochrome mutation's effects on the robustness and phase of molecular cycles in isolated peripheral tissues of Drosophila. BMC Neurosci 3: 5.
80. Veleri S, Brandes C, Helfrich-Forster C, Hall JC, Stanewsky R (2003) A selfsustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr Biol 13: 1758-1767.
81. Stanewsky R, Kaneko M, Emery P, Beretta B, Wager-Smith K, et al. (1998) The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95: 681-692.
82. Locke JC, Southern MM, Kozma-Bognar L, Hibberd V, Brown PE, et al. (2005) Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 1: 2005-2013.
83. Plautz JD, Straume M, Stanewsky R, Jamison CF, Brandes C, et al. (1997) Quantitative analysis of Drosophila period gene transcription in living animals. J Biol Rhythms 12: 204-217.