BMAL1-dependent circadian oscillation of nuclear CLOCK: Posttranslational events induced by dimerization of transcriptional activators of the mammalian clock system

Genes and Development

Volumn 17, Issue 15, 2003, Pages 1921-1932

  Kondratov, Roman V ^a   Chernov, Mikhail V ^a   Kondratova, Anna A ^a   Gorbacheva, Victoria Y ^a   Gudkov, Andrei V ^a   Antoch, Marina P ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Circadian rhythm; CLOCK BMAL1 complex; Nuclear entry; Phosphorylation; Transcriptional activation

Indexed keywords

PROTEIN; PROTEIN BMALI; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BIOLOGICAL RHYTHM; CELL NUCLEUS; CELLULAR DISTRIBUTION; CIRCADIAN RHYTHM; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; EMBRYO; FIBROBLAST; GERM LINE; HUMAN; HUMAN CELL; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; TRANSCRIPTION INITIATION;

3T3 CELLS; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; CELL LINE; CELL NUCLEUS; CIRCADIAN RHYTHM; CYTOPLASM; DIMERIZATION; FIBROBLASTS; HUMANS; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MUTATION; OSCILLOMETRY; PHOSPHORYLATION; PLASMIDS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; TIME FACTORS; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFECTION;

ANIMALIA; MAMMALIA;

EID: 0042626226     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1099503     Document Type: Article

References (53)

1. Balsalobre, A., Damiola, F., and Schibler, U. 1998. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93: 929-937.
2. Balsalobre, A., Marcacci, L., and Schibler, U. 2000. Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts. Curr. Biol. 10: 1291-1294.
3. 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 Iδ phosphorylation of human circadian clock proteins period 1 and 2. FEBS Lett. 489: 159-165.
4. II250 is a bipartite protein kinase that phosphorylates the base transcription factor RAP74. Cell 84: 781-790.
5. Dolwick, K.M., Swanson, H.I., and Bradfield, C.A. 1993. In vitro analysis of Ah receptor domains involved in ligand-activated DNA recognition. Proc. Natl. Acad. Sci. 90: 8566-8570.
6. 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 ε. J. Biol. Chem. 277: 17248-17254.
7. Gekakis, N., Staknis, D., Nguyen, H.B., Davis, F.C., Wilsbacher, L.D., King, D.P., Takahashi, J.S., and Weitz, C.J. 1998. Role of the CLOCK protein in the mammalian circadian mechanism. Science 280: 1564-1569.
8. Griffin Jr., E.A., Staknis, D., and Weitz, C.J. 1999. Light-independent role of CRY1 and CRY2 in the mammalian circadian clock. Science 286: 768-771.
9. 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: 178-182.
10. Gu, Y.Z., Hogenesch, J.B., and Bradfield, C.A. 2000. The PAS superfamily: Sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 40: 519-561.
11. Hogenesch, J.B., Chan, W.K., Jackiw, V.H., Brown, R.C., Gu, Y.Z., Pray-Grant, M., Perdew, G.H., and Bradfield, C.A. 1997. Characterization of a subset of the basic-helix-loop-helix-PAS superfamily that interacts with components of the dioxin signaling pathway. J. Biol. Chem. 272: 8581-8593.
12. Hogenesch, J.B., Gu, Y.Z., Jain, S., and Bradfield, C.A. 1998. The basic-helix-loop-helix-PAS orphan MOP3 forms transcriptionally active complexes with circadian and hypoxia factors. Proc. Natl. Acad. Sci. 95: 5474-5479.
13. 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 ε. Neuroreport 11: 951-955.
14. King, D.P. and Takahashi, J.S. 2000. Molecular genetics of circadian rhythms in mammals. Annu. Rev. Neurosci. 23: 713-742.
15. King, D.P., Zhao, Y., Sangoram, A.M., Wilsbacher, L.D., Tanaka, M., Antoch, M.P., Steeves, T.D., Vitaterna, M.H., Kornhauser, J.M., Lowrey, P.L., et al. 1997. Positional cloning of the mouse circadian clock gene. Cell 89: 641-653.
16. Klein, D.C., Moore, R.Y., and Reppert, S.M. 1991. The suprachiasmatic nucleus: The mind's clock. Oxford University Press, New York.
17. 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 I ε. Cell 94: 97-107.
18. Kume, K., Zylka, M.J., Sriram, S., Shearman, L.P., Weaver, D.R., Jin, X., Maywood, E.S., Hastings, M.H., and Reppert, S.M. 1999. mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98: 193-205.
19. Lee, C., Bae, K., and 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.
20. 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.
21. Liu, Y., Loros, J., and Dunlap, J.C. 2000. Phosphorylation of the Neurospora clock protein FREQUENCY determines its degradation rate and strongly influences the period length of the circadian clock. Proc. Nat]. Acad. Sci. 97: 234-239.
22. Lowrey, P.L. and Takahashi, J.S. 2000. Genetics of the mammalian circadian system: Photic entrainment, circadian pacemaker mechanisms, and post-translational regulation. Annu. Rev. Genet. 34: 533-562.
23. Lu, H., Zawel, L., Fisher, L., Egly, J.M., and Reinberg, D. 1992. Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II. Nature 358: 641-645.
24. 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: 769-779.
25. Molinari, E., Gilman, M., and Natesan, S. 1999. Proteasome-mediated degradation of transcriptional activators correlates with activation domain potency in vivo. EMBO J. 18: 6439-6447.
26. Naidoo, N., Song, W., Hunter-Ensor, M., and Sehgal, A. 1999. A role for the proteasome in the light response of the timeless clock protein. Science 285: 1737-1741.
27. Preitner, N., Damiola, F., Lopez-Molina, L., Zakany, J., Duboule, D., Albrecht, U., and Schibler, U. 2002. The orphan nuclear receptor REV-ERBα controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110: 251-260.
28. 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.
29. Price, M.A. and Kalderon, D. 2002. Proteolysis of the Hedgehog signaling effector Cubitus interruptus requires phosphorylation by Glycogen Synthase Kinase 3 and Casein Kinase 1. Cell 108: 823-835.
30. Reppert, S.M. and Weaver, D.R. 2001. Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 63: 647-676.
31. Salghetti, S.E., Kim, S.Y., and Tansey, W.P. 1999. Destruction of Myc by ubiquitin-mediated proteolysis: Cancer-associated and transforming mutations stabilize Myc. EMBO J. 18: 717-726.
32. Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
33. Sanada, K., Okano, T., and Fukada, Y. 2002. Mitogen-activated protein kinase phosphorylates and negatively regulates basic helix-loop-helix-PAS transcription factor BMAL1. J. Biol. Chem. 277: 267-271.
34. Schibler, U. and Sassone-Corsi, P. 2002. A web of circadian pacemakers. Cell 111: 919-922.
35. Shearman, L.P., Zylka, M.J., Weaver, D.R., Kolakowski Jr., L.F., and Reppert, S.M. 1997. Two period homologs: Circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron 19: 1261-1269.
36. Shearman, L.P., Jin, X., Lee, C., Reppert, S.M., and Weaver, D.R. 2000a. Targeted disruption of the mPer3 gene: Subtle effects on circadian clock function. Mol. Cell. Biol. 20: 6269-6275.
37. Shearman, L.P., Sriram, S., Weaver, D.R., Maywood, E.S., Chaves, I., Zheng, B., Kume, K., Lee, C.C., van der Horst, G.T., Hastings, M.H., et al. 2000b. Interacting molecular loops in the mammalian circadian clock. Science 288: 1013-1019.
38. Sun, Z.S., Albrecht, U., Zhuchenko, O., Bailey, J., Eichele, G., and Lee, C.C. 1997. RIGUI, a putative mammalian ortholog of the Drosophila period gene. Cell 90: 1003-1011.
39. Swanson, H.I., Chan, W.K, and Bradfield, C.A. 1995. DNA binding specificities and pairing rules of the Ah receptor, ARNT, and SIM proteins. J. Biol. Chem. 270: 26292-26302.
40. Takahata, S., Sogawa, K., Kobayashi, A., Ema, M., Mimura, J., Ozaki, N., and Fujii-Kuriyama, Y. 1998. Transcriptionally active heterodimer formation of an Arnt-like PAS protein, Arnt3, with HIF-1a, HLF, and clock. Biochem. Biophys. Res. Commun. 248: 789-794.
41. Tansey, W.P. 2001. Transcriptional activation: Risky business. Genes & Dev. 15: 1045-1050.
42. Tel, H., Okamura, H., Shigeyoshi, Y., Fukuhara, C., Ozawa, R., Hirose, M., and Sakaki, Y. 1997. Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature 389: 512-516.
43. 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: 1040-1043.
44. van der Horst, G.T., Muijtjens, M., Kobayashi, K., Takano, R., Kanno, S., Takao, M., de Wit, J., Verkerk, A., Eker, A.P., van Leenen, D., et al. 1999. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398: 627-630.
45. 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 ε. Mol Cell. Biol. 20: 4888-4899.
46. Vitaterna, M.H., Selby, C.P., Todo, T., Niwa, H., Thompson, C., Fruechte, E.M., Hitomi, K., Thresher, R.J., Ishikawa, T., Miyazaki, J., et al. 1999. Differential regulation of mammalian period genes and circadian rhythmicity by cryptochromes 1 and 2. Proc. Natl. Acad. Sci. 96: 12114-12119.
47. Vosshall, L.B., Price, J.L., Sehgal, A., Saez, L., and Young, M.W. 1994. Block in nuclear localization of period protein by a second clock mutation, timeless. Science 263: 1606-1609.
48. Welsh, D., Logothetis, D., Meister, M., and Reppert, S. 1995. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14: 697-706.
49. Wilsbacher, L.D., Yamazaki, S., Herzog, E.D., Song, E.J., Radcliffe, L.A., Abe, M., Block, G., Spitznagel, E., Menaker, M., and Takahashi, J.S. 2002. Photic and circadian expression of luciferase in mPeriod1-luc transgenic mice invivo. Proc. Natl. Acad. Sci. 99: 489-494.
50. Wu, M., Hemesath, T.J., Takemoto, C.M., Horstmann, M.A., Wells, A.G., Price, E.R., Fisher, D.Z., and Fisher, D.E. 2000. c-Kit triggers dual phosphorylations, which couple activation and degradation of the essential melanocyte factor Mi. Genes & Dev. 14: 301-312.
51. 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: 1301-1314.
52. Young, M.W. and Kay, S.A. 2001. Time zones: A comparative genetics of circadian clocks. Nat. Rev. Genet 2: 702-715.
53. Zheng, B., Larkin, D.W., Albrecht, U., Sun, Z.S., Sage, M., Eichele, G., Lee, C.C., and Bradley, A. 1999. The mPer2 gene encodes a functional component of the mammalian circadian clock. Nature 400: 169-173.