Role of phosphorylation in the mammalian circadian clock

Cold Spring Harbor Symposia on Quantitative Biology

Volumn 72, Issue , 2007, Pages 167-176

  Vanselow, K ^a   Kramer, A ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; NUCLEAR PROTEIN; PER2 PROTEIN, MOUSE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CLOCK; PER PROTEIN; PHOSPHATASE; PHOSPHOTRANSFERASE; SERINE; UNCLASSIFIED DRUG;

ANIMAL; BIOLOGICAL MODEL; CIRCADIAN RHYTHM; FEEDBACK SYSTEM; GENETICS; HUMAN; MAMMAL; METABOLISM; MOUSE; MUTATION; PHENOTYPE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; REVIEW; CELLULAR DISTRIBUTION; NEGATIVE FEEDBACK; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY;

ANIMALS; CELL CYCLE PROTEINS; CIRCADIAN RHYTHM; FEEDBACK, BIOCHEMICAL; HUMANS; MAMMALS; MICE; MODELS, BIOLOGICAL; MUTATION; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 48249124934     PISSN: 00917451     EISSN: None     Source Type: Book Series    
DOI: 10.1101/sqb.2007.72.036     Document Type: Conference Paper

References (77)

1. Akashi M., Tsuchiya Y., Yoshino T., and Nishida E. 2002. Control of intracellular dynamics of mammalian period proteins by casein kinase I epsilon (CKIepsilon) and CKIdelta in cultured cells. Mol. Cell. Biol. 22: 1693.
2. 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.
3. Balsalobre A., Damiola F., and Schibler U. 1998. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93: 929.
4. Bao S., Rihel J., Bjes E., Fan J.Y., and Price J.L. 2001. The Drosophila double-timeS mutation delays the nuclear accumulation of period protein and affects the feedback regulation of period mRNA. J. Neurosci. 21: 7117.
5. Barnes J.W., Tischkau S.A., Barnes J.A., Mitchell J.W., Burgoon P.W., Hickok J.R., and Gillette M.U. 2003. Requirement of mammalian Timeless for circadian rhythmicity. Science 302: 439.
6. Brown S.A., Ripperger J., Kadener S., Fleury-Olela F., Vilbois F., Rosbash M., and Schibler U. 2005a. PERIOD1-associated proteins modulate the negative limb of the mammalian circadian oscillator. Science 308: 693.
7. Brown S.A., Fleury-Olela F., Nagoshi E., Hauser C., Juge C., Meier C.A., Chicheportiche R., Dayer J.M., Albrecht U., and Schibler U. 2005b. The period length of fibroblast circadian gene expression varies widely among human individuals. PLoS Biol. 3: e338.
8. Busino L., Bassermann F., Maiolica A., Lee C., Nolan P.M., Godinho S.I., Draetta G.F., and Pagano M. 2007. SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science 316: 900.
9. Camacho F., Cilio M., Guo Y., Virshup D.M., Patel K., Khorkova O., Styren S., Morse B., Yao Z., and Keesler G.A. 2001. Human casein kinase Idelta phosphorylation of human circadian clock proteins period 1 and 2. FEBS Lett. 489: 159.
10. Cardone L., Hirayama J., Giordano F., Tamaru T., Palvimo J.J., and Sassone-Corsi P. 2005. Circadian clock control by SUMOylation of BMAL1. Science 309: 1390.
11. Curtin K.D., Huang Z.J., and Rosbash M. 1995. Temporally regulated nuclear entry of the Drosophila period protein contributes to the circadian clock. Neuron 14: 365.
12. Cyran S.A., Yiannoulos G., Buchsbaum A.M., Saez L., Young M.W., and Blau J. 2005. The double-time protein kinase regulates the subcellular localization of the Drosophila clock protein period. J. Neurosci. 25: 5430.
13. Czeisler C.A., Duffy J.F., Shanahan T.L., Brown E.N., Mitchell J.F., Rimmer D.W., Ronda J.M., Silva E.J., Allan J.S., Emens J.S., Dijk D.J., and Kronauer R.E. 1999. Stability, precision, and near-24-hour period of the human circadian pacemaker. Science 284: 2177.
14. Dey J., Carr A.J., Cagampang F.R., Semikhodskii A.S., Loudon A.S., Hastings M.H., and Maywood E.S. 2005. The tau mutation in the Syrian hamster differentially reprograms the circadian clock in the SCN and peripheral tissues. J. Biol. Rhythms 20: 99.
15. Edery I., Zwiebel L.J., Dembinska M.E., and Rosbash M. 1994. Temporal phosphorylation of the Drosophila period protein. Proc. Natl. Acad. Sci. 91: 2260.
16. Eide E.J., Vielhaber E.L., Hinz W.A., and Virshup D.M. 2002. The circadian regulatory proteins BMAL1 and cryptochromes are substrates of casein kinase Iepsilon. J. Biol. Chem. 277: 17248.
17. Eide E.J., Woolf M.F., Kang H., Woolf P., Hurst W., Camacho F., Vielhaber E.L., Giovanni A., and Virshup D.M. 2005. Control of mammalian circadian rhythm by CKIepsilon-regulated proteasome-mediated PER2 degradation. Mol. Cell Biol. 25: 2795.
18. Flotow H., Graves P.R., Wang A.Q., Fiol C.J., Roeske R.W., and Roach P.J. 1990. Phosphate groups as substrate determinants for casein kinase I action. J. Biol. Chem. 265: 14264.
19. Fujimoto Y., Yagita K., and Okamura H. 2006. Does mPER2 protein oscillate without its coding mRNA cycling?: Post-transcriptional regulation by cell clock. Genes Cells 11: 525.
20. Gallego M., Kang H., and Virshup D.M. 2006a. Protein phosphatase 1 regulates the stability of the circadian protein PER2. Biochem. J. 399: 169.
21. Gallego M., Eide E.J., Woolf M.F., Virshup D.M., and Forger D.B. 2006b. An opposite role for tau in circadian rhythms revealed by mathematical modeling. Proc. Natl. Acad. Sci. 103: 10618.
22. Godinho S.I., Maywood E.S., Shaw L., Tucci V., Barnard A.R., Busino L., Pagano M., Kendall R., Quwailid M.M., Romero M.R., O'Neill J., Chesham J.E., Brooker D., Lalanne Z., Hastings M.H., and Nolan P.M. 2007. The after-hours mutant reveals a role for Fbxl3 in determining mammalian circadian period. Science 316: 897.
23. Grima B., Lamouroux A., Chelot E., Papin C., Limbourg-Bouchon B., and Rouyer F. 2002. The F-box protein slimb controls the levels of clock proteins period and timeless. Nature 420: 178.
24. Harada Y., Sakai M., Kurabayashi N., Hirota T., and Fukada Y. 2005. Ser-557-phosphorylated mCRY2 is degraded upon synergistic phosphorylation by glycogen synthase kinase-3 beta. J. Biol. Chem. 280: 31714.
25. Hardin P.E., Hall J.C., and Rosbash M. 1990. Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343: 536.
26. Hofmann K.P., Spahn C.M., Heinrich R., and Heinemann U. 2006. Building functional modules from molecular interactions. Trends Biochem. Sci. 31: 497.
27. Holmberg C.I., Tran S.E., Eriksson J.E., and Sistonen L. 2002. Multisite phosphorylation provides sophisticated regulation of transcription factors. Trends Biochem. Sci. 27: 619.
28. Honma S., Kawamoto T., Takagi Y., Fujimoto K., Sato F., Noshiro M., Kato Y., and Honma K. 2002. Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature 419: 841.
29. Iitaka C., Miyazaki K., Akaike T., and Ishida N. 2005. A role for glycogen synthase kinase-3beta in the mammalian circadian clock. J. Biol. Chem. 280: 29397.
30. Jones C.R., Campbell S.S., Zone S.E., Cooper F., DeSano A., Murphy P.J., Jones B., Czajkowski L., and Ptacek L.J. 1999. Familial advanced sleep-phase syndrome: A short-period circadian rhythm variant in humans. Nat. Med. 5: 1062.
31. Keesler G.A., Camacho F., Guo Y., Virshup D., Mondadori C., and Yao Z. 2000. Phosphorylation and destabilization of human period I clock protein by human casein kinase I epsilon. Neuroreport 11: 951.
32. 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. 103: 6178.
33. 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 Iepsilon. Cell 94: 97.
34. Ko H.W., Jiang J., and Edery I. 2002. Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature 420: 673.
35. Konopka R.J. and Benzer S. 1971. Clock mutants of Drosophila melanogaster. Proc. Natl. Acad. Sci. 68: 2112.
36. 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.
37. 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.
38. Lin J.M., Kilman V.L., Keegan K., Paddock B., Emery-Le M., Rosbash M., and Allada R. 2002. A role for casein kinase 2alpha in the Drosophila circadian clock. Nature 420: 816.
39. Lowrey P.L., Shimomura K., Antoch M.P., Yamazaki S., Zemenides P.D., Ralph M.R., Menaker M., and Takahashi J.S. 2000. Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science 288: 483.
40. Martinek S., Inonog S., Manoukian A.S., and Young M.W. 2001. A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 105: 769.
41. Nakajima M., Imai K., Ito H., Nishiwaki T., Murayama Y., Iwasaki H., Oyama T., and Kondo T. 2005. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308: 414.
42. Nawathean P. and Rosbash M. 2004. The doubletime and CKII kinases collaborate to potentiate Drosophila PER transcriptional repressor activity. Mol. Cell 13: 213.
43. Nishii K., Yamanaka I., Yasuda M., Kiyohara Y.B., Kitayama Y., Kondo T., and Yagita K. 2006. Rhythmic post-transcriptional regulation of the circadian clock protein mPER2 in mammalian cells: A real-time analysis. Neurosci. Lett. 401: 44.
44. O'Gorman S., Fox D.T., and Wahl G.M. 1991. Recombinasemediated gene activation and site-specific integration in mammalian cells. Science 251: 1351.
45. Partch C.L., Shields K.F., Thompson C.L., Selby C.P., and Sancar A. 2006. Posttranslational regulation of the mammalian circadian clock by cryptochrome and protein phosphatase 5. Proc. Natl. Acad. Sci. 103: 10467.
46. Preitner N., Damiola F., Lopez-Molina L., Zakany J., Duboule D., Albrecht U., and Schibler U. 2002. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110: 251.
47. Preuss F., Fan J.Y., Kalive M., Bao S., Schuenemann E., Bjes E.S., and Price J.L. 2004. Drosophila doubletime mutations which either shorten or lengthen the period of circadian rhythms decrease the protein kinase activity of casein kinase I. Mol. Cell. Biol. 24: 886.
48. 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.
49. Ralph M.R. and Menaker M. 1988. A mutation of the circadian system in golden hamsters. Science 241: 1225.
50. Reischl S., Vanselow K., Westermark P.O., Thierfelder N., Maier B., Herzel H., and Kramer A. 2007. β-TrCP1-mediated degradation of PERIOD2 is essential for circadian dynamics. J. Biol. Rhythms 22: 375.
51. Rothenfluh A., Abodeely M., and Young M.W. 2000. Shortperiod mutations of per affect a double-time-dependent step in the Drosophila circadian clock. Curr. Biol. 10: 1399.
52. Sangoram A.M., Saez L., Antoch M.P., Gekakis N., Staknis D., Whiteley A., Fruechte E.M., Vitaterna M.H., Shimomura K., King D.P., Young M.W., Weitz C.J., and Takahashi J.S. 1998. Mammalian circadian autoregulatory loop: A timeless ortholog and mPer1 interact and negatively regulate CLOCKBMAL1-induced transcription. Neuron 21: 1101.
53. Sathyanarayanan S., Zheng X., Xiao R., and Sehgal A. 2004. Posttranslational regulation of Drosophila PERIOD protein by protein phosphatase 2A. Cell 116: 603.
54. Schlosser A., Vanselow J.T., and Kramer A. 2005. Mapping of phosphorylation sites by a multi-protease approach with specific phosphopeptide enrichment and NanoLC-MS/MS analysis. Anal. Chem. 77: 5243.
55. Shirogane T., Jin J., Ang X.L., and Harper J.W. 2005. SCFbeta-TRCP controls clock-dependent transcription via casein kinase 1-dependent degradation of the mammalian period-1 (Per1) protein. J. Biol. Chem. 280: 26863.
56. Siepka S.M., Yoo S.H., Park J., Song W., Kumar V., Hu Y., Lee C., and Takahashi J.S. 2007. Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression. Cell 129: 1011.
57. Sugano S., Andronis C., Ong M.S., Green R.M., and Tobin E.M. 1999. The protein kinase CK2 is involved in regulation of circadian rhythms in Arabidopsis. Proc. Natl. Acad. Sci. 96: 12362.
58. Suri V., Hall J.C., and Rosbash M. 2000. Two novel doubletime mutants alter circadian properties and eliminate the delay between RNA and protein in Drosophila. J. Neurosci. 20: 7547.
59. Takano A. and Nagai K. 2006. Serine 714 might be implicated in the regulation of the phosphorylation in other areas of mPer1 protein. Biochem. Biophys. Res. Commun. 346: 95.
60. Takano A., Isojima Y., and Nagai K. 2004. Identification of mPer1 phosphorylation sites responsible for the nuclear entry. J. Biol. Chem. 279: 32578.
61. Takano A., Shimizu K., Kani S., Buijs R.M., Okada M., and Nagai K. 2000. Cloning and characterization of rat casein kinase 1epsilon. FEBS Lett. 477: 106.
62. Toh K.L., Jones C.R., He Y., Eide E.J., Hinz W.A., Virshup D.M., Ptacek L.J., and Fu Y.H. 2001. An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 291: 1040.
63. Tomita J., Nakajima M., Kondo T., and Iwasaki H. 2005. No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 307: 251.
64. 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.
65. Vielhaber E., Eide E., Rivers A., Gao Z.H., and Virshup D.M. 2000. Nuclear entry of the circadian regulator mPER1 is controlled by mammalian casein kinase I epsilon. Mol. Cell. Biol. 20: 4888.
66. Xu Y., Toh K.L., Jones C.R., Shin J.Y., Fu Y.H., and Ptacek L.J. 2007. Modeling of a human circadian mutation yields insights into clock regulation by PER2. Cell 128: 59.
67. Xu Y., Padiath Q.S., Shapiro R.E., Jones C.R., Wu S.C., Saigoh N., Saigoh K., Ptacek L.J., and Fu Y.H. 2005. Functional consequences of a CKIdelta mutation causing familial advanced sleep phase syndrome. Nature 434: 640.
68. Yagita K., Tamanini F., Der Horst G.T., and Okamura H. 2001. Molecular mechanisms of the biological clock in cultured fibroblasts. Science 292: 278.
69. Yagita K., Tamanini F., Yasuda M., Hoeijmakers J.H., van der Horst G.T., and Okamura H. 2002. Nucleocytoplasmic shuttling and mCRY-dependent inhibition of ubiquitylation of the mPER2 clock protein. EMBO J. 21: 1301.
70. Yang Y., Cheng P., and Liu Y. 2002. Regulation of the Neurospora circadian clock by casein kinase II. Genes Dev. 16: 994.
71. Yang Z. and Sehgal A. 2001. Role of molecular oscillations in generating behavioral rhythms in Drosophila. Neuron 29: 453.
72. Yin L., Wang J., Klein P.S., and Lazar M.A. 2006. Nuclear receptor Rev-erbalpha is a critical lithium-sensitive component of the circadian clock. Science 311: 1002.
73. Yu Q., Jacquier A.C., Citri Y., Hamblen M., Hall J.C., and Rosbash M. 1987. Molecular mapping of point mutations in the period gene that stop or speed up biological clocks in Drosophila melanogaster. Proc. Natl. Acad. Sci. 84: 784.
74. 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.
75. Zeng H., Qian Z., Myers M.P., and Rosbash M. 1996. A lightentrainment mechanism for the Drosophila circadian clock. Nature 380: 129.
76. Zerr D.M., Hall J.C., Rosbash M., and Siwicki K.K. 1990. Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J. Neurosci. 10: 2749.
77. Zhao W.N., Malinin N., Yang F.C., Staknis D., Gekakis N., Maier B., Reischl S., Kramer A., and Weitz C.J. 2007. CIPC is a mammalian circadian clock protein without invertebrate homologues. Nat. Cell Biol. 9: 268.