Phosphorylation of the transcription activator CLOCK regulates progression through a ∼24-h feedback loop to influence the circadian period in drosophila

Journal of Biological Chemistry

Volumn 289, Issue 28, 2014, Pages 19681-19693

  Mahesh, Guruswamy ^a   Jeong, EunHee ^b   Ng, Fanny S ^a   Liu, Yixiao ^a   Gunawardhana, Kushan ^a   Houl, Jerry H ^a   Yildirim, Evrim ^d   Amunugama, Ravi ^c   Jones, Richard ^c   Allen, David L ^c   Edery, Isaac ^d   Kim, Eun Young ^b   Hardin, Paul E ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b Ajou University School of Medicine   (South Korea)

^c MS BIOWORKS   (United States)

^d RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CLOCKS; MASS SPECTROMETRY; TRANSCRIPTION;

CLOCK CYCLES; DAILY RHYTHM; FEED-BACK LOOP; PHOSPHORYLATION SITES; SPECIFIC SITES; SUBCELLULAR LOCALIZATIONS; TRANSCRIPTION ACTIVATORS; TRANSCRIPTIONAL REPRESSION;

PHOSPHORYLATION;

ALANINE; CIRCADIAN RHYTHM SIGNALING PROTEIN; PROTEIN TIMELESS; SERINE; TRANSCRIPTION FACTOR CLOCK;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; CONTROLLED STUDY; DROSOPHILA; FEEDBACK SYSTEM; INHIBITION KINETICS; MALE; MASS SPECTROMETRY; MOLECULAR CLOCK; MOLECULAR DYNAMICS; MUTANT; NONHUMAN; PHOSPHORYLATION SITE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSGENE;

BEHAVIORAL RHYTHMS; CIRCADIAN CLOCK; CLOCK PROTEIN; DROSOPHILA GENETICS; FEEDBACK LOOP; MASS SPECTROMETRY (MS); PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CIRCADIAN RHYTHM; CLOCK PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; PERIOD CIRCADIAN PROTEINS; PHOSPHORYLATION;

EID: 84904201438     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.568493     Document Type: Article

References (59)

1. Bell-Pedersen, D., Cassone, V. M., Earnest, D. J., Golden, S. S., Hardin, P. E., Thomas, T. L., and Zoran, M. J. (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat. Rev. Genet. 6, 544-556 (Pubitemid 40910431)
2. Hardin, P. E. (2011) Molecular genetic analysis of circadian timekeeping in Drosophila. Adv. Genet. 74, 141-173
3. Akten, B., Jauch, E., Genova, G. K., Kim, E. Y., Edery, I., Raabe, T., and Jackson, F. R. (2003) A role for CK2 in the Drosophila circadian oscillator. Nat. Neurosci. 6, 251-257 (Pubitemid 36278283)
4. Ko, H. W., Kim, E. Y., Chiu, J., Vanselow, J. T., Kramer, A., and Edery, I. (2010)Ahierarchical phosphorylation cascade that regulates the timing of PERIOD nuclear entry reveals novel roles for proline-directed kinases and GSK-3β/SGG in circadian clocks. J. Neurosci. 30, 12664-12675
5. Lin, J. M., Kilman, V. L., Keegan, K., Paddock, B., Emery-Le, M., Rosbash, M., and Allada, R. (2002) A role for casein kinase 2 in the Drosophila circadian clock. Nature 420, 816-820 (Pubitemid 36019629)
6. Martinek, S., Inonog, S., Manoukian, A. S., and Young, M. W. (2001) Arole for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 105, 769-779 (Pubitemid 32635106)
7. Kim, E. Y., Jeong, E. H., Park, S., Jeong, H. J., Edery, I., and Cho, J. W. (2012) A role for O-GlcNAcylation in setting circadian clock speed. Genes Dev. 26, 490-502
8. Chiu, J. C., Ko, H. W., and Edery, I. (2011) NEMO/NLK phosphorylates PERIOD to initiate a time-delay phosphorylation circuit that sets circadian clock speed. Cell 145, 357-370
9. Kloss, B., Price, J. L., Saez, L., Blau, J., Rothenfluh, A., Wesley, C. S., and Young, M. W. (1998) The Drosophila clock gene double-time encodes a protein closely related to human casein kinase Iε. Cell 94, 97-107 (Pubitemid 28347473)
10. Price, J. L., Blau, J., Rothenfluh, A., Abodeely, M., Kloss, B., and Young, M. W. (1998) double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94, 83-95 (Pubitemid 28347472)
11. Chiu, J. C., Vanselow, J. T., Kramer, A., and 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)
12. Garbe, D. S., Fang, Y., Zheng, X., Sowcik, M., Anjum, R., Gygi, S. P., and Sehgal, A. (2013) Cooperative interaction between phosphorylation sites on PERIOD maintains circadian period in Drosophila. PLoS Genet. 9, e1003749
13. Kivimäe, S., Saez, L., and Young, M. W. (2008) Activating PER repressor through a DBT-directed phosphorylation switch. PLoS Biol. 6, e183
14. Vanselow, K., Vanselow, J. T., Westermark, P. O., Reischl, S., Maier, B., Korte, T., Herrmann, A., Herzel, H., Schlosser, A., and Kramer, A. (2006) Differential effects of PER2 phosphorylation: molecular basis for the human familial advanced sleep phase syndrome (FASPS). Genes Dev. 20, 2660-2672 (Pubitemid 44498377)
15. Xu, Y., Toh, K. L., Jones, C. R., Shin, J. Y., Fu, Y. H., and Ptácek, L. J. (2007) Modeling of a human circadian mutation yields insights into clock regulation by PER2. Cell 128, 59-70 (Pubitemid 46048889)
16. Lee, C., Bae, K., and Edery, I. (1998) The Drosophila CLOCK protein undergoes daily rhythms in abundance, phosphorylation, and interactions with the PER-TIM complex. Neuron 21, 857-867 (Pubitemid 28498793)
17. Menet, J. S., Abruzzi, K. C., Desrochers, J., Rodriguez, J., and Rosbash, M. (2010) Dynamic PER repression mechanisms in the Drosophila circadian clock: from on-DNA to off-DNA. Genes Dev. 24, 358-367
18. Yu, W., Zheng, H., Houl, J. H., Dauwalder, B., and Hardin, P. E. (2006) PER-dependent rhythms in CLK phosphorylation and E-box binding regulate circadian transcription. Genes Dev. 20, 723-733
19. Kim, E. Y., and 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
20. Yu, W., Zheng, H., Price, J. L., and Hardin, P. E. (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
21. Szabó, A., Papin, C., Zorn, D., Ponien, P., Weber, F., Raabe, T., and Rouyer, F. (2013) The CK2 kinase stabilizes CLOCK and represses its activity in the Drosophila circadian oscillator. PLoS Biol. 11, e1001645
22. Yu, W., Houl, J. H., and Hardin, P. E. (2011) NEMO kinase contributes to core period determination by slowing the pace of the Drosophila circadian oscillator. Curr. Biol. 21, 756-761
23. Lee, C., Etchegaray, J. P., Cagampang, F. R., Loudon, A. S., and Reppert, S. M. (2001) Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107, 855-867 (Pubitemid 34084977)
24. Yoshitane, H., Takao, T., Satomi, Y., Du, N. H., Okano, T., and Fukada, Y. (2009) Roles of CLOCK phosphorylation in suppression of E-box-dependent transcription. Mol. Cell Biol. 29, 3675-3686
25. Spengler, M. L., Kuropatwinski, K. K., Schumer, M., and Antoch, M. P. (2009) A serine cluster mediates BMAL1-dependent CLOCK phosphorylation and degradation. Cell Cycle 8, 4138-4146
26. 2+-dependent protein kinase C mediates resetting of the mammalian circadian clock. EMBO Rep. 8, 366-371
27. Allada, R., White, N. E., So, W. V., Hall, J. C., and Rosbash, M. (1998) A mutant Drosophila homolog of mammalian Clock disrupts circadian rhythms and transcription of period and timeless. Cell 93, 791-804 (Pubitemid 28257585)
28. Darlington, T. K., Wager-Smith, K., Ceriani, M. F., Staknis, D., Gekakis, N., Steeves, T. D., Weitz, C. J., Takahashi, J. S., and Kay, S. A. (1998) Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 280, 1599-1603 (Pubitemid 28277704)
29. Glossop, N. R., Houl, J. H., Zheng, H., Ng, F. S., Dudek, S. M., and Hardin, P. E. (2003) VRILLE feeds back to control circadian transcription of Clock in the Drosophila circadian oscillator. Neuron 37, 249-261 (Pubitemid 36143820)
30. Thibault, S. T., Singer, M. A., Miyazaki, W. Y., Milash, B., Dompe, N. A., Singh, C. M., Buchholz, R., Demsky, M., Fawcett, R., Francis-Lang, H. L., Ryner, L., Cheung, L. M., Chong, A., Erickson, C., Fisher, W. W., Greer, K., Hartouni, S. R., Howie, E., Jakkula, L., Joo, D., Killpack, K., Laufer, A., Mazzotta, J., Smith, R. D., Stevens, L. M., Stuber, C., Tan, L. R., Ventura, R., Woo, A., Zakrajsek, I., Zhao, L., Chen, F., Swimmer, C., Kopczynski, C., Duyk, G., Winberg, M. L., and Margolis, J. (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36, 283-287 (Pubitemid 38282754)
31. Bischof, J., and Basler, K. (2008) Recombinases and their use in gene activation, gene inactivation, and transgenesis. Methods Mol. Biol. 420, 175-195
32. Venken, K. J., He, Y., Hoskins, R. A., and Bellen, H. J. (2006) P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314, 1747-1751 (Pubitemid 44969080)
33. Groth, A. C., Fish, M., Nusse, R., and Calos, M. P. (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166, 1775-1782 (Pubitemid 38621059)
34. Veraksa, A., Bauer, A., and Artavanis-Tsakonas, S. (2005) Analyzing protein complexes in Drosophila with tandem affinity purification-mass spectrometry. Dev. Dyn. 232, 827-834 (Pubitemid 40315300)
35. Yang, P., Sampson, H. M., and Krause, H. M. (2006) A modified tandem affinity purification strategy identifies cofactors of the Drosophila nuclear receptor dHNF4. Proteomics 6, 927-935 (Pubitemid 43260217)
36. Nawathean, P., Menet, J. S., and Rosbash, M. (2005) Assaying the Drosophila negative feedback loop with RNA interference in S2 cells. Methods Enzymol. 393, 610-622 (Pubitemid 40486549)
37. Kim, E. Y., Bae, K., Ng, F. S., Glossop, N. R., Hardin, P. E., and Edery, I. (2002) Drosophila CLOCK protein is under posttranscriptional control and influences light-induced activity. Neuron 34, 69-81 (Pubitemid 34270699)
38. Houl, J. H., Ng, F., Taylor, P., and Hardin, P. E. (2008) CLOCK expression identifies developing circadian oscillator neurons in the brains of Drosophila embryos. BMC Neurosci. 9, 119
39. Pfeiffenberger, C., Lear, B. C., Keegan, K. P., and Allada, R. (2010) Sleep and circadian behavior monitoring in Drosophila in Drosophila neurobiology: A laboratory manual (Zhang, B., Freeman, M. R., and Waddell, S., eds) pp. 483-504, Cold Spring Harbor Press, Cold Spring Harbor, NY
40. Kannan, N., and Neuwald, A. F. (2004) Evolutionary constraints associated with functional specificity of the CMGC protein kinases MAPK, CDK, GSK, SRPK, DYRK, and CK2 . Protein Sci. 13, 2059-2077 (Pubitemid 38989612)
41. Allada, R., Kadener, S., Nandakumar, N., and Rosbash, M. (2003) A recessive mutant of Drosophila Clock reveals a role in circadian rhythm amplitude. EMBO J. 22, 3367-3375 (Pubitemid 36834866)
42. Lear, B. C., Lin, J. M., Keath, J. R., McGill, J. J., Raman, I. M., and Allada, R. (2005) The ion channel narrow abdomen is critical for neural output of the Drosophila circadian pacemaker. Neuron 48, 965-976 (Pubitemid 41814700)
43. Helfrich-Förster, C. (2005) Neurobiology of the fruit fly's circadian clock. Genes Brain Behav. 4, 65-76
44. Kondratov, R. V., Chernov, M. V., Kondratova, A. A., Gorbacheva, V. Y., Gudkov, A. V., and Antoch, M. P. (2003) BMAL1-dependent circadian oscillation of nuclear CLOCK: posttranslational events induced by dimerization of transcriptional activators of the mammalian clock system. Genes Dev. 17, 1921-1932 (Pubitemid 36944568)
45. Bae, K., Lee, C., Hardin, P. E., and 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)
46. Kadener, S., Menet, J. S., Schoer, R., and Rosbash, M. (2008) Circadian transcription contributes to core period determination in Drosophila. PLoS Biol. 6, e119
47. Smith, R. F., and Konopka, R. J. (1981) Circadian clock phenotypes of chromosome aberrations with a breakpoint at the per locus. Mol. Gen. Genet. 183, 243-251 (Pubitemid 12175259)
48. Hung, H. C., Maurer, C., Zorn, D., Chang, W. L., and Weber, F. (2009) Sequential and compartment-specific phosphorylation controls the life cycle of the circadian CLOCK protein. J. Biol. Chem. 284, 23734-23742
49. Houl, J. H., Yu, W., Dudek, S. M., and Hardin, P. E. (2006) Drosophila CLOCK is constitutively expressed in circadian oscillator and non-oscillator cells. J. Biol. Rhythms 21, 93-103
50. Kim, E. Y., Ko, H. W., Yu, W., Hardin, P. E., and 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 (Pubitemid 47016149)
51. Hall, J. C. (2003) Genetics and molecular biology of rhythms in Drosophila and other insects. Adv. Genet. 48, 1-280
52. Hao, H., Glossop, N. R., Lyons, L., Qiu, J., Morrish, B., Cheng, Y., Helfrich-Förster, C., and Hardin, P. (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 (Pubitemid 29066161)
53. Lin, J. M., Schroeder, A., and Allada, R. (2005) In vivo circadian function of casein kinase 2 phosphorylation sites in Drosophila PERIOD. J. Neurosci. 25, 11175-11183 (Pubitemid 43089562)
54. Iitaka, C., Miyazaki, K., Akaike, T., and Ishida, N. (2005) A role for glycogen synthase kinase-3β in the mammalian circadian clock. J. Biol. Chem. 280, 29397-29402 (Pubitemid 41177011)
55. Tsuchiya, Y., Akashi, M., Matsuda, M., Goto, K., Miyata, Y., Node, K., and Nishida, E. (2009) Involvement of the protein kinase CK2 in the regulation of mammalian circadian rhythms. Sci. Signal. 2, ra26
56. Baylies, M. K., Vosshall, L. B., Sehgal, A., and Young, M. W. (1992) New short period mutations of the Drosophila clock gene per. Neuron 9, 575-581
57. Rothenfluh, A., Abodeely, M., and Young, M. W. (2000) Short-period mutations of per affect a double-time-dependent step in the Drosophila circadian clock. Curr. Biol. 10, 1399-1402
58. Toh, K. L., Jones, C. R., He, Y., Eide, E. J., Hinz, W. A., Virshup, D. M., Ptácek, L. J., and Fu, Y. H. (2001) An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 291, 1040-1043 (Pubitemid 32157412)
59. Luo, W., Li, Y., Tang, C. H., Abruzzi, K. C., Rodriguez, J., Pescatore, S., and Rosbash, M. (2012) CLOCK deubiquitylation by USP8 inhibits CLK/CYC transcription in Drosophila. Genes Dev. 26, 2536-2549