Control of mammalian circadian rhythm by CKIε-regulated proteasome-mediated PER2 degradation

Molecular and Cellular Biology

Volumn 25, Issue 7, 2005, Pages 2795-2807

  Eide, Erik J ^a   Woolf, Margaret F ^a   Kang, Heeseog ^a   Woolf, Peter ^b   Hurst, William ^c   Camacho, Fernando ^c   Vielhaber, Erica L ^c   Giovanni, Andrew ^c   Virshup, David M ^a,d  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c SANOFI   (France)

^d UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALYCULIN A; CASEIN KINASE; PER1 PROTEIN; PER2 PROTEIN; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; PROTEASOME; PROTEIN DERIVATIVE; REGULATOR PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MEMBRANE PERMEABILITY; CHEMICAL ANALYSIS; CIRCADIAN RHYTHM; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RAT; STATISTICAL SIGNIFICANCE; UBIQUITINATION;

ANIMALS; BETA-TRANSDUCIN REPEAT-CONTAINING PROTEINS; CASEIN KINASE IEPSILON; CELL CYCLE PROTEINS; CELL LINE; CIRCADIAN RHYTHM; GENE EXPRESSION REGULATION; HUMANS; MICE; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; RATS; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 15044343742     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.7.2795-2807.2005     Document Type: Article

References (54)

1. Akashi, M., and E. Nishida. 2000. Involvement of the MAP kinase cascade in resetting of the mammalian circadian clock. Genes Dev. 14:645-649.
2. Akashi, M., Y. Tsuchiya, T. Yoshino, and E. Nishida. 2002. Control of intracellular dynamics of mammalian period proteins by casein kinase I ε (CKIε) and CKIδ in cultured cells. Mol. Cell. Biol. 22:1693-1703.
3. 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.
4. Balsalobre, A., F. Damiola, and U. Schibler. 1998. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93:929-937.
5. Balsalobre, A., L. Marcacci, and U. Schibler. 2000. Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts Curr. Biol. 10:1291-1294.
6. Butcher, G. Q., H. Dziema, M. Collamore, P. W. Burgoon, and K. Obrietan. 2002. The p42/44 mitogen-activated protein kinase pathway couples photic input to circadian clock entrainment. J. Biol. Chem. 277:29519-29525.
7. Camacho, F., M. Cilio, Y. Guo, D. Virshup, K. Patel, O. Khorkova, S. Styren, B. Morse, Z. Yao, and G. A. Keesler. 2001. Human casein kinase Iδ phosphorylation of human circadian clock proteins period 1 and 2. FEBS Lett. 489:159-165.
8. Doi, M., T. Okano, I. Yujnovsky, P. Sassone-Corsi, and Y. Fukada. 2004. Negative control of circadian clock regulator E4BP4 by casein kinase Iε-mediated phosphorylation. Curr. Biol. 14:975-980.
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 Iε. J. Biol. Chem. 277:17248-17254.
10. Eide, E. J., and D. M. Virshup. 2001. Casein kinase I: another cog in the circadian clockworks. Chronobiol. Int. 18:389-398.
11. Gao, Z. H., J. Metherall, and D. M. Virshup. 2000. Identification of casein kinase I substrates by in vitro expression cloning screening. Biochem. Biophys. Res. Commun. 268:562-566.
12. Gietzen, K. F., and D. M. Virshup. 1999. Identification of inhibitory autophosphorylation sites in casein kinase I ε. J. Biol. Chem. 274:32063-32070.
13. Grima, B., A. Lamouroux, E. Chélot, 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.
14. Hart, M., J. P. Concordet, I. Lassot, I. Albert, R. del los Santos, H. Durand, C. Perret, B. Rubinfeld, F. Margottin, R. Benarous, and P. Polakis. 1999. The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr. Biol. 9:207-210.
15. He, Q., P. Cheng, Y. Yang, H. Yu, and Y. Liu. 2003. FWD1-mediated degradation of FREQUENCY in Neurospora establishes a conserved mechanism for circadian clock regulation. EMBO J. 22:4421-4430.
16. Honkanen, R. E., and T. Golden. 2002. Regulators of serine/threonine protein phosphatases at the dawn of a clinical era? Curr. Med. Chem. 9:2055-2075.
17. Izumo, M., C. H. Johnson, and S. Yamazaki. 2003. Circadian gene expression in mammalian fibroblasts revealed by real-time luminescence reporting: temperature compensation and damping. Proc. Natl. Acad. Sci. USA 100:16089-16094.
18. Jackson, P. K., A. G. Eldridge, E. Freed, L. Furstenthal, J. Y. Hsu, B. K. Kaiser, and J. D. Reimann. 2000. The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol. 10:429-439.
19. Keesler, G. A., F. Camacho, Y. Guo, D. Virshup, C. Mondadori, and Z. Yao. 2000. Phosphorylation and destabilization of human period I clock protein by human casein kinase I ε. Neuroreport 11:951-955.
20. Kim, D. H., J. G. Kang, S. S. Yang, K. S. Chung, P. S. Song, and C. M. Park. 2002. A phytochrome-associated protein phosphatase 2A modulates light signals in flowering time control in Arabidopsis. Plant Cell 14:3043-3056.
21. 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 Iε. Cell 94:97-107.
22. 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.
23. Kuhlman, S. J., J. E. Quintero, and D. G. McMahon. 2000. GFP fluorescence reports Period 1 circadian gene regulation in the mammalian biological clock. Neuroreport 11:1479-1482.
24. βTrCP ubiquitin ligase. Mol. Cell. Biol. 21:2192-2202.
25. 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.
26. Liu, F., D. M. Virshup, A. C. Nairn, and P. Greengard. 2002. Mechanism of regulation of casein kinase I activity by group I metabotropic glutamate receptors. J. Biol. Chem. 277:45393-45399.
27. Liu, Y., J. Loros, and J. C. Dunlap. 2000. Phosphorylation of the Neurospora clock protein FREQUENCY determines its degradation rate and strongly influences the period length of the circadian clock. Proc. Natl. Acad. Sci. USA 97:234-239.
28. Lowrey, P. L., K. Shimomura, M. P. Antoch, S. Yamazaki, P. D. Zemenides, M. R. Ralph, M. Menaker, and J. S. Takahashi. 2000. Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science 288:483-492.
29. Lowrey, P. L., and J. S. Takahashi. 2000. Genetics of the mammalian circadian system: photic entrainment, circadian pacemaker mechanisms, and posttranslational regulation. Annu. Rev. Genet. 34:533-562.
30. Margottin, F., S. P. Bour, H. Durand, L. Selig, S. Benichou, V. Richard, D. Thomas, K. Strebel, and R. Benarous. 1998. A novel human WD protein, h-βTrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol. Cell 1:565-574.
31. Martinek, S., S. Inonog, A. S. Manoukian, and M. W. Young. 2001. A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 105:769-779.
32. Mashhoon, N., A. J. DeMaggio, V. Tereshko, S. C. Bergmeier, M. Egli, M. F. Hoekstra, and J. Kuret. 2000. Crystal structure of a conformation-selective casein kinase-1 inhibitor. J. Biol. Chem. 275:20052-20060.
33. Miyazaki, K., T. Nagase, M. Mesaki, J. Narukawa, O. Ohara, and N. Ishida. 2004. Phosphorylation of clock protein PER1 regulates its circadian degradation in normal human fibroblasts. Biochem. J. 380:95-103.
34. 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.
35. Obrietan, K., S. Impey, and D. R. Storm. 1998. Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat. Neurosci. 1:693-700.
36. Pickart, C. M. 2001. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70:503-533.
37. Preitner, N., F. Damiola, L. Lopez-Molina, J. Zakany, D. Duboule, U. Albrecht, and U. Schibler. 2002. The orphan nuclear receptor REV-ERBα controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110:251-260.
38. Preuss, F., J.-Y. Fan, M. Kalive, S. Bao, E. Schuenemann, E. S. Bjes, and J. L. Price. 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. 24:886-898.
39. 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.
40. 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.
41. Reppert, S. M., and D. R. Weaver. 2002. Coordination of circadian timing in mammals. Nature 418:935-941.
42. Sathyanarayanan, S., X. Zheng, R. Xiao, and A. Sehgal. 2004. Posttranslational regulation of Drosophila PERIOD protein by protein phosphatase 2A. Cell 116:603-615.
43. Swiatek, W., I.-C. Tsai, L. Klimowski, A. Pepler, J. Barnette, H. J. Yost, and D. M. Virshup. 2004. Regulation of casein kinase Iε activity by Wnt signaling. J. Biol. Chem. 279:13011-13017. [Online.]
44. Toh, K. L., C. R. Jones, Y. He, E. J. Eide, W. A. Hinz, D. M. Virshup, L. J. Ptacek, and Y.-H. Fu. 2001. An hPER2 phosphorylation site mutation in familial advanced sleep-phase syndrome. Science 291:1040-1043.
45. Treier, M., L. M. Staszewski, and D. Bohmann. 1994. Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 78:787-798.
46. Vallone, D., S. B. Gondi, D. Whitmore, and N. S. Foulkes. 2004. E-box function in a period gene repressed by light. Proc. Natl. Acad. Sci. USA 101:4106-4111.
47. Vielhaber, E., E. Eide, A. Rivers, Z.-H. Gao, and D. M. Virshup. 2000. Nuclear entry of the circadian regulator mPER1 is controlled by mammalian casein kinase I ε. Mol. Cell. Biol. 20:4888-4899.
48. Watanabe, N., H. Arai, Y. Nishihara, M. Taniguchi, T. Hunter, and H. Osada. 2004. M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFβ-TrCP. Proc. Natl. Acad. Sci. USA 101:4419-4424. [Online.]
49. β-TrCp1 ubiquitin ligase. Mol. Cell 11:1445-1456.
50. Yagita, K., F. Tamanini, M. Yasuda, J. H. Hoeijmakers, G. T. van der Horst, and H. Okamura. 2002. Nucleocytoplasmic shuttling and mCRY-dependent inhibition of ubiquitylation of the mPER2 clock protein. EMBO J. 21:1301-1314.
51. Yamazaki, S., R. Numano, M. Abe, A. Hida, R. Takahashi, M. Ueda, G. D. Block, Y. Sakaki, M. Menaker, and H. Tei. 2000. Resetting central and peripheral circadian oscillators in transgenic rats. Science 288:682-685.
52. Yang, Y., P. Cheng, Q. He, L. Wang, and Y. Liu. 2003. Phosphorylation of FREQUENCY protein by casein kinase II is necessary for the function of the Neurospora circadian clock. Mol. Cell. Biol. 23:6221-6228.
53. Yang, Y., P. Cheng, and Y. Liu. 2002. Regulation of the Neurospora circadian clock by casein kinase II. Genes Dev. 16:994-1006.
54. Yaron, A., A. Hatzubai, M. Davis, I. Lavon, S. Amit, A. M. Manning, J. S. Andersen, M. Mann, F. Mercurio, and Y. Ben-Neriah. 1998. Identification of the receptor component of the IκBα-ubiquitin ligase. Nature 396:590-594.