Phosphorylation of FREQUENCY protein by casein kinase II is necessary for the function of the Neurospora circadian clock

Molecular and Cellular Biology

Volumn 23, Issue 17, 2003, Pages 6221-6228

  Yang, Yuhong ^a   Cheng, Ping ^a   He, Qiyang ^a   Wang, Lixin ^a   Liu, Yi ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; FREQUENCY PROTEIN; FUNGAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CIRCADIAN RHYTHM; CONIDIUM; CYTOPLASM; ENZYME ACTIVE SITE; FEEDBACK SYSTEM; FUNGAL STRAIN; FUNGUS GROWTH; FUNGUS MUTANT; GENE DISRUPTION; GENE MUTATION; NEUROSPORA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY;

BIOLOGICAL CLOCKS; CASEIN KINASE II; CASEIN KINASES; CELL NUCLEUS; CIRCADIAN RHYTHM; CYTOPLASM; DARKNESS; FUNGAL PROTEINS; MUTATION; NEUROSPORA; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN SUBUNITS; PROTEIN-SERINE-THREONINE KINASES;

FUNGI; NEUROSPORA;

EID: 0041387632     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.17.6221-6228.2003     Document Type: Article

References (53)

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. Aronson, B., K. Johnson, J. J. Loros, and J. C. Dunlap. 1994. Negative feedback defining a circadian clock: autoregulation in the clock gene frequency. Science 263:1578-1584.
3. Aronson, B. D., K. A. Johnson, and J. C. Dunlap. 1994. The circadian clock locus frequency: a single ORF defines period length and temperature compensation. Proc. Natl. Acad. Sci. USA 91:7683-7687.
4. Bell-Pedersen, D., J. C. Dunlap, and J. J. Loros. 1996. Distinct cis-acting elements mediate clock, light, and developmental regulation of the Neurospora crassa eas (ccg-2) gene. Mol. Cell. Biol. 16:513-521.
5. Bell-Pedersen, D., J. C. Dunlap, and J. J. Loros. 1992. The Neurospora circadian clock-controlled gene, ccg-2, is allelic to eas and encodes a fungal hydrophobin required for formation of the conidial rodlet layer. Genes Dev. 6:2382-2394.
6. Bidwai, A. P., J. C. Reed, and C. V. Glover. 1995. Cloning and disruption of CKB1, the gene encoding the 38-kDa beta subunit of Saccharomyces cerevisiae casein kinase II (CKII). Deletion of CKII regulatory subunits elicits a salt-sensitive phenotype. J. Biol. Chem. 270:10395-10404.
7. Cheng, P., Y. Yang, K. H. Gardner, and Y. Liu. 2002. PAS domain-mediated WC-1/WC-2 interaction is essential for maintaining the steady state level of WC-1 and the function of both proteins in circadian clock and light responses of Neurospora. Mol. Cell. Biol. 22:517-524.
8. Cheng, P., Y. Yang, C. Heintzen, and Y. Liu. 2001. Coiled-coil domain mediated FRQ-FRQ interaction is essential for its circadian clock function in Neurospora. EMBO J. 20:101-108.
9. Cheng, P., Y. Yang, and Y. Liu. 2001. Interlocked feedback loops contribute to the robustness of the Neurospora circadian clock. Proc. Natl. Acad. Sci. USA 98:7408-7413.
10. Cheng, P., Y. Yang, L. Wang, Q. He, and Y. Liu. 2003. WHITE COLLAR-1, a multifunctional Neurospora protein involved in the circadian feedback loops, light sensing, and transcription repression of wc-2. J. Biol. Chem. 278:3801-3808.
11. Collett, M. A., N. Garceau, J. C. Dunlap, and J. J. Loros. 2002. Light and clock expression of the Neurospora clock gene frequency is differentially driven by but dependent on WHITE COLLAR-2. Genetics 160:149-158.
12. Crosthwaite, S. K., J. C. Dunlap, and J. J. Loros. 1997. Neurospora wc-1 and wc-2: transcription, photoresponses, and the origins of circadian rhythmicity. Science 276:763-769.
13. Crosthwaite, S. K., J. J. Loros, and J. C. Dunlap. 1995. Light-induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript. Cell 81:1003-1012.
14. Davis, R. L., and D. deSerres. 1970. Genetic and microbial research techniques for Neurospora crassa. Methods Enzymol. 27A:79-143.
15. Denault, D. L., J. J. Loros, and J. C. Dunlap. 2001. WC-2 mediates WC-1-FRQ interaction within the PAS protein-linked circadian feedback loop of Neurospora. EMBO J. 20:109-117.
16. Dunlap, J. C. 1999. Molecular bases for circadian clocks. Cell 96:271-290.
17. Edery, I., L. Zweibel, M. Dembinska, and M. Rosbash. 1994. Temporal phosphorylation of the Drosophila period protein. Proc. Natl. Acad. Sci. USA 91:2260-2264.
18. 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.
19. Froehlich, A. C., Y. Liu, J. J. Loros, and J. C. Dunlap. 2002. White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297:815-819.
20. Garceau, N., Y. Liu, J. J. Loros, and J. C. Dunlap. 1997. Alternative initiation of translation and time-specific phosphorylation yield multiple forms of the essential clock protein FREQUENCY. Cell 89:469-476.
21. Gorl, M., M. Merrow, B. Huttner, J. Johnson, T. Roenneberg, and M. Brunner. 2001. A PEST-like element in FREQUENCY determines the length of the circadian period in Neurospora crassa. EMBO J. 20:7074-7084.
22. He, Q., P. Cheng, Y. Yang, L. Wang, K. H. Gardner, and Y. Liu. 2002. White collar-1, a DNA binding transcription factor and a light sensor. Science 297:840-843.
23. Iwasaki, H., S. B. Williams, Y. Kitayama, M. Ishiura, S. S. Golden, and T. Kondo. 2000. A kaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria. Cell 101:223-233.
24. Kloss, B., J. L. Price, L. Saez, J. Blau, A. Rothenfluh, 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.
25. 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.
26. Lakin-Thomas, P., G. Coté, and S. Brody. 1990. Circadian rhythms in Neurospora: biochemistry and genetics. Crit. Rev. Microbiol. 17:365-416.
27. 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.
28. Lee, K., J. C. Dunlap, and J. J. Loros. 2003. Roles for WHITE COLLAR-1 in circadian and general photoperception in Neurospora crassa. Genetics 163:103-114.
29. Lee, K., J. J. Loros, and J. C. Dunlap. 2000. Interconnected feedback loops in the Neurospora circadian system. Science 289:107-110.
30. Lin, J. M., V. L. Kilman, K. Keegan, B. Paddock, M. Emery-Le, M. Rosbash, and R. Allada. 2002. A role for casein kinase 2α in the Drosophila circadian clock. Nature 420:816-820.
31. Linden, H., P. Ballario, and G. Macino. 1997. Blue light regulation in Neurospora crassa. Fungal Genet. Biol. 22:141-150.
32. Liu, Y., N. Garceau, J. J. Loros, and J. C. Dunlap. 1997. Thermally regulated translational control mediates an aspect of temperature compensation in the Neurospora circadian clock. Cell 89:477-486.
33. 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.
34. Loros, J. J., S. A. Denome, and J. C. Dunlap. 1989. Molecular cloning of genes under the control of the circadian clock in Neurospora. Science 243: 385-388.
35. Loros, J. J., and J. C. Dunlap. 2001. Genetic and molecular analysis of circadian rhythms in NEUROSPORA. Annu. Rev. Physiol. 63:757-794.
36. 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.
37. Luo, C., J. J. Loros, and J. C. Dunlap. 1998. Nuclear localization is required for function of the essential clock protein FREQUENCY. EMBO J. 17: 1228-1235.
38. 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.
39. Meggio, F., O. Marin, and L. A. Pinna. 1994. Substrate specificity of protein kinase CK2. Cell Mol. Biol. Res. 40:401-409.
40. Merrow, M., L. Franchi, Z. Dragovic, M. Gorl, J. Johnson, M. Brunner, G. Macino, and T. Roenneberg. 2001. Circadian regulation of the light input pathway in Neurospora crassa. EMBO J. 20:307-315.
41. Pinna, L. A., and F. Meggio. 1997. Protein kinase CK2 ("casein kinase-2") and its implication in cell division and proliferation. Prog. Cell Cycle Res. 3:77-97.
42. Price, J. L., J. Blau, A. Rothenfluh, M. Adodeely, B. Kloss, and M. W. Young. 1998. double-time is a new Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94:83-95.
43. Roussou, I., and G. Draetta. 1994. The Schizosaccharomyces pombe casein kinase II alpha and beta subunits: evolutionary conservation and positive role of the beta subunit. Mol. Cell. Biol. 14:576-586.
44. Schwerdtfeger, C., and H. Linden. 2000. Localization and light-dependent phosphorylation of white collar 1 and 2, the two central components of blue light signaling in Neurospora crassa. Eur. J. Biochem. 267:414-422.
45. Selker, E. U., and P. W. Garrett. 1988. DNA sequence duplications trigger gene inactivation in Neurospora crassa. Proc. Natl. Acad. Sci. USA 85:6870-6874.
46. Sugano, S., C. Andonis, R. Green, Z. Y. Wang, and E. M. Tobin. 1998. Protein kinase CK2 interacts with and phosphorylates the Arabidopsis circadian clock-associated 1 protein. Proc. Natl. Acad. Sci. USA 95:11020-11025.
47. Sugano, S., C. Andronis, M. S. Ong, R. M. Green, and E. M. Tobin. 1999. The protein kinase CK2 is involved in regulation of circadian rhythms in Arabidopsis. Proc. Natl. Acad. Sci. USA. 96:12362-12366.
48. Talora, C., L. Franchi, H. Linden, P. Ballario, and G. Macino. 1999. Role of a white collar-1-white collar-2 complex in blue-light signal transduction. EMBO J. 18:4961-4968.
49. 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.
50. 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 epsilon. Mol. Cell. Biol. 20:4888-4899.
51. Yang, Y., P. Cheng, and Y. Liu. 2002. Regulation of the Neurospora circadian clock by casein kinase II. Genes Dev. 16:994-1006.
52. Yang, Y., P. Cheng, G. Zhi, and Y. Liu. 2001. Identification of a calcium/ calmodulin-dependent protein kinase that phosphorylates the Neurospora circadian clock protein FREQUENCY. J. Biol. Chem. 276:41064-41072.
53. Young, M. W., and S. A. Kay. 2001. Time zones: a comparative genetics of circadian clocks. Nat. Rev. Genet. 2:702-715.