Doubletime plays a noncatalytic role to mediate Clock phosphorylation and repress Clock-dependent transcription within the Drosophila circadian clock

Molecular and Cellular Biology

Volumn 29, Issue 6, 2009, Pages 1452-1458

  Yu, Wangjie ^a   Zheng, Hao ^a,c   Price, Jeffrey L ^b   Hardin, Paul E ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^c Shanghai Hengrui Pharmaceuticals Co Ltd   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN DOUBLETIME; PROTEIN KINASE; PROTEIN PERIOD; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG;

ARTICLE; DROSOPHILA; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION;

ANIMALS; CASEIN KINASE IEPSILON; CIRCADIAN RHYTHM; DROSOPHILA; DROSOPHILA PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

DROSOPHILA MELANOGASTER; MAMMALIA;

EID: 62849110192     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01777-08     Document Type: Article

References (41)

1. Akten, B., E. Jauch, G. K. Genova, E. Y. Kim, I. Edery, T. Raabe, and F. R. Jackson. 2003. A role for CK2 in the Drosophila circadian oscillator. Nat. Neurosci. 6:251-257.
2. Allada, R., N. E. White, W. V. So, J. C. Hall, and M. Rosbash. 1998. A mutant Drosophila homolog of mammalian Clock disrupts circadian rhythms and transcription of period and timeless. Cell 93:791-804.
3. Bae, K., C. Lee, P. E. Hardin, and I. Edery. 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.
4. Bell-Pedersen, D., V. M. Cassone, D. J. Earnest, S. S. Golden, P. E. Hardin, T. L. Thomas, and M. J. Zoran. 2005. Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat. Rev. Genet. 6:544-556.
5. Chang, D. C., and S. M. Reppert. 2003. A novel C-terminal domain of Drosophila PERIOD inhibits dCLOCK:CYCLE-mediated transcription. Curr. Biol. 13:758-762.
6. Chiu, J. C., J. T. Vanselow, A. Kramer, and I. Edery. 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.
7. Cyran, S. A., G. Yiannoulos, A. M. Buchsbaum, L. Saez, M. W. Young, and J. Blau. 2005. The double-time protein kinase regulates the subcellular localization of the Drosophila clock protein period. J. Neurosci. 25:5430-5437.
8. Darlington, T. K., K. Wager-Smith, M. F. Ceriani, D. Staknis, N. Gekakis, T. D. Steeves, C. J. Weitz, J. S. Takahashi, and S. A. Kay. 1998. Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 280:1599-1603.
9. Eide, E. J., E. L. Vielhaber, W. A. Hinz, and D. M. Virshup. 2002. The circadian regulatory proteins BMAL1 and cryptochromes are substrates of casein kinase I(epsilon). J. Biol. Chem. 277:17248-17254.
10. Emery, P., W. V. So, M. Kaneko, J. C. Hall, and M. Rosbash. 1998. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95:669-679.
11. Grima, B., A. Lamouroux, E. Chelot, C. Papin, B. Limbourg-Bouchon, and F. Rouyer. 2002. The F-box protein Slimb controls the levels of clock proteins period and timeless. Nature 420:178-182.
12. Hao, H., D. L. Allen, and P. E. Hardin. 1997. A circadian enhancer mediates PER-dependent mRNA cycling in Drosophila melanogaster. Mol. Cell. Biol. 17:3687-3693.
13. Hao, H., N. R. Glossop, L. Lyons, J. Qiu, B. Morrish, Y. Cheng, C. Helfrich-Forster, and P. Hardin. 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.
14. He, Q., J. Cha, Q. He, H. C. Lee, Y. Yang, and Y. Liu. 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.
15. Houl, J. H., W. Yu, S. M. Dudek, and P. E. Hardin. 2006. Drosophila CLOCK is constitutively expressed in circadian oscillator and non-oscillator cells. J. Biol. Rhythms 21:93-103.
16. Kim, E. Y., and I. Edery. 2006. Balance between DBT/CKI(epsilon) kinase and protein phosphatase activities regulate phosphorylation and stability of Drosophila CLOCK protein. Proc. Natl. Acad. Sci. USA 103:6178-6183.
17. Kim, E. Y., H. W. Ko, W. Yu, P. E. Hardin, and I. Edery. 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.
18. Kivimae, S., L. Saez, and M. W. Young. 2008. Activating PER repressor through a DBT-directed phosphorylation switch. PLoS Biol. 6:e183.
19. Kloss, B., J. L. Price, L. Saez, J. Blau, A. Rothenfluh, C. S. Wesley, and M. W. Young. 1998. The Drosophila clock gene double-time encodes a protein closely related to human casein kinase I(epsilon). Cell 94:97-107.
20. Kloss, B., A. Rothenfluh, M. W. Young, and L. Saez. 2001. Phosphorylation of period is influenced by cycling physical associations of double-time, period, and timeless in the Drosophila clock. Neuron 30:699-706.
21. Ko, H. W., J. Jiang, and I. Edery. 2002. Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature 420:673-678.
22. Lee, C., K. Bae, and I. Edery. 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.
23. Lee, C., K. Bae, and I. Edery. 1998. The Drosophila CLOCK protein undergoes daily rhythms in abundance, phosphorylation, and interactions with the PER-TIM complex. Neuron 21:857-867.
24. Lee, C., J. P. Etchegaray, F. R. Cagampang, A. S. Loudon, and S. M. Reppert. 2001. Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107:855-867.
25. Lin, J. M., V. L. Kilman, K. Keegan, B. Paddock, M. Emery-Le, M. Rosbash, and R. Allada. 2002. A role for casein kinase 2alpha in the Drosophila circadian clock. Nature 420:816-820.
26. Muskus, M. J., F. Preuss, J. Y. Fan, E. S. Bjes, and J. L. Price. 2007. Drosophila DBT lacking protein kinase activity produces long-period and arrhythmic circadian behavioral and molecular rhythms. Mol. Cell. Biol. 27:8049-8064.
27. Naidoo, N., W. Song, M. Hunter-Ensor, and A. Sehgal. 1999. A role for the proteasome in the light response of the timeless clock protein. Science 285:1737-1741.
28. Nawathean, P., and M. Rosbash. 2004. The doubletime and CKII kinases collaborate to potentiate Drosophila PER transcriptional repressor activity. Mol. Cell 13:213-223.
29. Nawathean, P., D. Stoleru, and M. Rosbash. 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. Price, J. L., J. Blau, A. Rothenfluh, M. Abodeely, B. Kloss, and M. W. Young. 1998. double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94:83-95.
31. Price, J. L., M. E. Dembinska, M. W. Young, and M. Rosbash. 1995. Suppression of PERIOD protein abundance and circadian cycling by the Drosophila clock mutation timeless. EMBO J. 14:4044-4049.
32. Ripperger, J. A., and U. Schibler. 2006. Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat. Genet. 38:369-374.
33. Rothenfluh, A., M. Abodeely, and M. W. Young. 2000. Short-period mutations of per affect a double-time-dependent step in the Drosophila circadian clock. Curr. Biol. 10:1399-1402.
34. Rothenfluh, A., M. W. Young, and L. Saez. 2000. A TIMELESS-independent function for PERIOD proteins in the Drosophila clock. Neuron 26:505-514.
35. Rutila, J. E., V. Suri, M. Le, W. V. So, M. Rosbash, and J. C. Hall. 1998. CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 93:805-814.
36. Schafmeier, T., A. Haase, K. Kaldi, J. Scholz, M. Fuchs, and M. Brunner. 2005. Transcriptional feedback of Neurospora circadian clock gene by phosphorylation-dependent inactivation of its transcription factor. Cell 122:235-246.
37. Sidote, D., J. Majercak, V. Parikh, and I. Edery. 1998. Differential effects of light and heat on the Drosophila circadian clock proteins PER and TIM. Mol. Cell. Biol. 18:2004-2013.
38. Smith, E. M., J. M. Lin, R. A. Meissner, and R. Allada. 2008. Dominant-negative CK2alpha induces potent effects on circadian rhythmicity. PLoS Genet. 4:e12.
39. Taylor, P., and P. E. Hardin. 2008. Rhythmic E-box binding by CLK-CYC controls daily cycles in per and tim transcription and chromatin modifications. Mol. Cell. Biol. 28:4642-4652.
40. Vanselow, K., J. T. Vanselow, P. O. Westermark, S. Reischl, B. Maier, T. Korte, A. Herrmann, H. Herzel, A. Schlosser, and A. Kramer. 2006. Differential effects of PER2 phosphorylation: molecular basis for the human familial advanced sleep phase syndrome (FASPS). Genes Dev. 20:2660-2672.
41. Yu, W., H. Zheng, J. H. Houl, B. Dauwalder, and P. E. Hardin. 2006. PER-dependent rhythms in CLK phosphorylation and E-box binding regulate circadian transcription. Genes Dev. 20:723-733.