Two distinct modes of PERIOD recruitment onto dCLOCK reveal a novel role for TIMELESS in circadian transcription

Journal of Neuroscience

Volumn 30, Issue 43, 2010, Pages 14458-14469

  Sun, Woo Chul ^a   Jeong, Eun Hee ^a   Jeong, Hyun Jeong ^a   Ko, Hyuk Wan ^b   Edery, Isaac ^c   Kim, Eun Young ^a  

^a Ajou University School of Medicine   (South Korea)

^b Kyung Hee University Hospital   (South Korea)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; BRAIN REGION; CELL CULTURE; CIRCADIAN RHYTHM; DROSOPHILA; EMBRYO; FEEDBACK SYSTEM; GENE EXPRESSION; GENETIC TRANSCRIPTION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REPRESSOR GENE; TRANSCRIPTION INITIATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; CELLS, CULTURED; CIRCADIAN RHYTHM; CLOCK PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; IMMUNOHISTOCHEMISTRY; LIGHT; MOTOR ACTIVITY; PERIOD CIRCADIAN PROTEINS; PHOSPHORYLATION; PLASMIDS; PROTEIN BINDING; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; TRANSCRIPTION, GENETIC;

EID: 78049340311     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2366-10.2010     Document Type: Article

References (53)

1. Allada R, White NE, So WV, Hall JC, Rosbash M (1998) A mutant Drosophila homolog of mammalian Clock disrupts circadian rhythms and transcription of period and timeless. Cell 93:791-804.
2. Allada R, Emery P, Takahashi JS, Rosbash M (2001) Stopping time: the genetics of fly and mouse circadian clocks. Annu Rev Neurosci 24:1091-1119. (Pubitemid 32695255)
3. Ashmore LJ, Sehgal A (2003) Afly's eye view of circadian entrainment. J Biol Rhythms 18:206-216.
4. Ashmore LJ, Sathyanarayanan S, Silvestre DW, Emerson MM, Schotland P, Sehgal A (2003) Novel insights into the regulation of the timeless protein. J Neurosci 23:7810-7819. (Pubitemid 37052349)
5. Bae K, Edery I (2006) Regulating a circadian clock's period, phase and amplitude by phosphorylation: insights from Drosophila. J Biochem 140:609-617. (Pubitemid 46065487)
6. Bae K, Lee C, Hardin PE, Edery I (2000) dCLOCK is present in limiting amounts and likely mediates daily interactions between the dCLOCK-CYC transcription factor and the PER-TIM complex. J Neurosci 20:1746-1753. (Pubitemid 30220372)
7. Baker CL, Kettenbach AN, Loros JJ, Gerber SA, Dunlap JC (2009) Quantitative proteomics reveals a dynamic interactome and phase-specific phosphorylation in the Neurospora circadian clock. Mol Cell 34:354-363.
8. Ceriani MF, Darlington TK, Staknis D, Más P, Petti AA, Weitz CJ, Kay SA (1999) Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science 285:553-556.
9. Chang DC, Reppert SM (2003) A novel C-terminal domain of Drosophila PERIOD inhibits dCLOCK:CYCLE-mediated transcription. Curr Biol 13:758-762.
10. Chen R, Schirmer A, Lee Y, Lee H, Kumar V, Yoo SH, Takahashi JS, Lee C (2009) Rhythmic PER abundance defines a critical nodal point for negative feedback within the circadian clock mechanism. Mol Cell 36:417-430.
11. Cheng P, He Q, He Q, Wang L, Liu Y (2005) Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev 19:234-241.
12. 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. (Pubitemid 351915501)
13. Colot HV, Hall JC, Rosbash M (1988) Interspecific comparison of the period gene of Drosophila reveals large blocks of non-conserved coding DNA. EMBO J 7:3929-3937.
14. 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.
15. 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.
16. Darlington TK, Wager-Smith K, Ceriani MF, Staknis D, Gekakis N, Steeves TD, Weitz CJ, Takahashi JS, Kay SA (1998) Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 280:1599-1603. (Pubitemid 28277704)
17. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271-290.
18. Edery I (2000) Circadian rhythms in a nutshell. Physiol Genomics 3:59-74.
19. Gallego M, Virshup DM (2007) Post-translational modifications regulate the ticking of the circadian clock. Nat Rev Mol Cell Biol 8:139-148. (Pubitemid 46432533)
20. Hamblen-Coyle MJ, Wheeler DA, Rutila JE, Rosbash M, Hall JC (1992) Behavior of period-altered rhythm mutants of Drosophila in light:dark cycles. J Insect Behav 5:417-446.
21. Hardin PE (2006) Essential and expendable features of the circadian time-keeping mechanism. Curr Opin Neurobiol 16:686-692.
22. Hardin PE, Hall JC, Rosbash M (1990) Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343:536-540.
23. He Q, Cha J, He Q, Lee HC, Yang Y, Liu Y (2006) CKI and CKII mediate the FREQUENCY-dependent phosphorylation of the WHITE COLLAR complex to close the Neurospora circadian negative feedback loop. Genes Dev 20:2552-2565.
24. Kim EY, Edery I (2006) Balance between DBT/CKIepsilon kinase and protein phosphatase activities regulate phosphorylation and stability of Drosophila CLOCK protein. Proc Natl Acad Sci U S A 103:6178-6183.
25. Kim EY, Ko HW, Yu W, Hardin PE, Edery I (2007) A DOUBLETIME 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.
26. Kloss B, Price JL, Saez L, Blau J, Rothenfluh A, Wesley CS, Young MW (1998) The Drosophila clock gene double-time encodes a protein closely related to human casein kinase Iepsilon. Cell 94:97-107.
27. 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. (Pubitemid 32607335)
28. Ko HW, Jiang J, Edery I (2002) Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature 420:673-678.
29. Ko HW, DiMassa S, Kim EY, Bae K, Edery I (2007) Cis-combination of the classic per(S) and per(L) mutations results in arrhythmic Drosophila with ectopic accumulation of hyperphosphorylated PERIOD protein. J Biol Rhythms 22:488-501.
30. Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 68:2112-2116.
31. Lee C, Parikh V, Itsukaichi T, Bae K, Edery I (1996) Resetting the Drosophila clock by photic regulation of PER and a PER-TIM complex. Science 271:1740-1744.
32. Lee C, Bae K, Edery I (1998) The Drosophila CLOCK protein undergoes daily rhythms in abundance, phosphorylation, and interactions with the PER-TIM complex. Neuron 21:857-867.
33. 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.
34. 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. (Pubitemid 38452079)
35. Menet JS, Abruzzi KC, Desrochers J, Rodriguez J, Rosbash M (2010) Dynamic PER repression mechanisms in the Drosophila circadian clock: from on-DNA to off-DNA. Genes Dev 24:358-367.
36. 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.
37. Myers MP, Wager-Smith K, Rothenfluh-Hilfiker A, Young MW (1996) Light-induced degradation of TIMELESS and entrainment of the Drosophila circadian clock. Science 271:1736-1740.
38. 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.
39. Nitabach MN, Taghert PH (2008) Organization of the Drosophila circadian control circuit. Curr Biol 18:R84-R93.
40. 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.
41. 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.
42. 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. (Pubitemid 30017649)
43. Rothenfluh A, Young MW, Saez L (2000) A TIMELESS-independent function for PERIOD proteins in the Drosophila clock. Neuron 26:505-514.
44. Saez L, Young MW (1996) Regulation of nuclear entry of the Drosophila clock proteins period and timeless. Neuron 17:911-920.
45. Schafmeier T, Haase A, Káldi K, Scholz J, Fuchs M, Brunner M (2005) Transcriptional feedback of Neurospora circadian clock gene by phosphorylation-dependent inactivation of its transcription factor. Cell 122:235-246.
46. 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. (Pubitemid 30220452)
47. 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.
48. Sidote D, Majercak J, Parikh V, Edery I (1998) Differential effects of light and heat on the Drosophila circadian clock proteins PER and TIM. Mol Cell Biol 18:2004-2013.
49. 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. (Pubitemid 24128363)
50. Yoshii T, Fujii K, Tomioka K (2007) Induction of Drosophila behavioral and molecular circadian rhythms by temperature steps in constant light. J Biol Rhythms 22:103-114.
51. Yu W, Hardin PE (2006) Circadian oscillators of Drosophila and mammals. J Cell Sci 119:4793-4795.
52. 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.
53. Yu W, Zheng H, Price JL, Hardin PE (2009) DOUBLETIME plays a noncatalytic role to mediate CLOCK phosphorylation and repress CLOCK-dependent transcription within the Drosophila circadian clock. Mol Cell Biol 29:1452-1458.