A Role for Casein Kinase 2 in the Mechanism Underlying Circadian Temperature Compensation

Cell

Volumn 137, Issue 4, 2009, Pages 749-760

  Mehra, Arun ^a   Shi, Mi ^a   Baker, Christopher L ^a   Colot, Hildur V ^a   Loros, Jennifer J ^a   Dunlap, Jay C ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

CELLBIO; PROTEINS; SYSBIO

Indexed keywords

CASEIN KINASE II;

ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; TEMPERATURE ACCLIMATIZATION;

NEUROSPORA;

EID: 65549088967     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.03.019     Document Type: Article

References (70)

1. Akman O.E., Locke J.C., Tang S., Carre I., Millar A.J., and Rand D.A. Isoform switching facilitates period control in the Neurospora crassa circadian clock. Mol. Syst. Biol. 4 (2008) 186
2. Akten B., Jauch E., Genova G.K., Kim E.Y., Edery I., Raabe T., and Jackson F.R. A role for CK2 in the Drosophila circadian oscillator. Nat. Neurosci. 6 (2003) 251-257
3. Allada R., and Meissner R.A. Casein kinase 2, circadian clocks, and the flight from mutagenic light. Mol. Cell. Biochem. 274 (2005) 141-149
4. Allada R., Emery P., Takahashi J.S., and Rosbash M. Stopping time: the genetics of fly and mouse circadian clocks. Annu. Rev. Neurosci. 24 (2001) 1091-1119
5. Aronson B.D., Johnson K.A., and Dunlap J.C. Circadian clock locus frequency: protein encoded by a single open reading frame defines period length and temperature compensation. Proc. Natl. Acad. Sci. USA 91 (1994) 7683-7687
6. Baker C.L., Kettenbach A.N., Loros J.J., Gerber S.A., and Dunlap J.C. Quantitative proteomics reveals a dynamic interactome and phase-specific phosphorylation in the Neurospora circadian clock. Mol. Cell 34 (2009) 354-363
7. Barrett R.K., and Takahashi J.S. Temperature compensation and temperature entrainment of the chick pineal cell circadian clock. J. Neurosci. 15 (1995) 5681-5692
8. Brunner M., and Schafmeier T. Transcriptional and post-transcriptional regulation of the circadian clock of cyanobacteria and Neurospora. Genes Dev. 20 (2006) 1061-1074
9. Cheng P., He Q., He Q., Wang L., and Liu Y. Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev. 19 (2005) 234-241
10. Colot H.V., Loros J.J., and Dunlap J.C. Temperature-modulated alternative splicing and promoter use in the circadian clock gene frequency. Mol. Biol. Cell 16 (2005) 5563-5571
11. Colot H.V., Park G., Turner G.E., Ringelberg C., Crew C.M., Litvinkova L., Weiss R.L., Borkovich K.A., and Dunlap J.C. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. USA 103 (2006) 10352-10357
12. Diernfellner A., Colot H.V., Dintsis O., Loros J.J., Dunlap J.C., and Brunner M. Long and short isoforms of Neurospora clock protein FRQ support temperature-compensated circadian rhythms. FEBS Lett. 581 (2007) 5759-5764
13. Diernfellner A.C., Schafmeier T., Merrow M.W., and Brunner M. Molecular mechanism of temperature sensing by the circadian clock of Neurospora crassa. Genes Dev. 19 (2005) 1968-1973
14. Dunlap J.C., and Loros J.J. Analysis of circadian rhythms in Neurospora: overview of assays and genetic and molecular biological manipulation. Methods Enzymol. 393 (2005) 3-22
15. Dunlap J.C., and Loros J.J. How fungi keep time: circadian system in Neurospora and other fungi. Curr. Opin. Microbiol. 9 (2006) 579-587
16. Dunlap J.C., Borkovich K.A., Henn M.R., Turner G.E., Sachs M.S., Glass N.L., McCluskey K., Plamann M., Galagan J.E., Birren B.W., et al. Enabling a community to dissect an organism: overview of the Neurospora functional genomics project. Adv. Genet. 57 (2007) 49-96
17. Dunlap J.C., Loros J.J., Colot H.V., Mehra A., Belden W.J., Shi M., Hong C.I., Larrondo L.F., Baker C.L., Chen C.H., et al. A circadian clock in Neurospora: how genes and proteins cooperate to produce a sustained, entrainable, and compensated biological oscillator with a period of about a day. Cold Spring Harb. Symp. Quant. Biol. 72 (2007) 57-68
18. Dunlap J.C., Loros J.J., and Decoursey P.J. Chronobiology: Biological Timekeeping, 1 edn (2004), Sinauer Associates Incorporated, Sunderland, MA
19. Edwards K.D., Lynn J.R., Gyula P., Nagy F., and Millar A.J. Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics 170 (2005) 387-400
20. Garceau N.Y., Liu Y., Loros J.J., and Dunlap J.C. Alternative initiation of translation and time-specific phosphorylation yield multiple forms of the essential clock protein FREQUENCY. Cell 89 (1997) 469-476
21. Gardner G.F., and Feldman J.F. Temperature compensation of circadian period length in clock mutants of Neurospora crassa. Plant Physiol. 68 (1981) 1244-1248
22. Glaser F.T., and Stanewsky R. Synchronization of the Drosophila circadian clock by temperature cycles. Cold Spring Harb. Symp. Quant. Biol. 72 (2007) 233-242
23. Gorl M., Merrow M., Huttner B., Johnson J., Roenneberg T., and Brunner M. A PEST-like element in FREQUENCY determines the length of the circadian period in Neurospora crassa. EMBO J. 20 (2001) 7074-7084
24. Gould P.D., Locke J.C., Larue C., Southern M.M., Davis S.J., Hanano S., Moyle R., Milich R., Putterill J., Millar A.J., et al. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell 18 (2006) 1177-1187
25. Hastings J.W., and Sweeney B.M. On the mechanism of temperature independence in a biological clock. Proc. Natl. Acad. Sci. USA 43 (1957) 804-811
26. He Q., Cha J., He Q., Lee H.C., Yang Y., and Liu Y. CKI and CKII mediate the FREQUENCY-dependent phosphorylation of the WHITE COLLAR complex to close the Neurospora circadian negative feedback loop. Genes Dev. 20 (2006) 2552-2565
27. Hong C.I., and Tyson J.J. A proposal for temperature compensation of the circadian rhythm in Drosophila based on dimerization of the PER protein. Chronobiol. Int. 14 (1997) 521-529
28. Hong C.I., Conrad E.D., and Tyson J.J. A proposal for robust temperature compensation of circadian rhythms. Proc. Natl. Acad. Sci. USA 104 (2007) 1195-1200
29. Huang G., Chen S., Li S., Cha J., Long C., Li L., He Q., and Liu Y. Protein kinase A and casein kinases mediate sequential phosphorylation events in the circadian negative feedback loop. Genes Dev. 21 (2007) 3283-3295
30. Huang Z.J., Curtin K.D., and Rosbash M. PER protein interactions and temperature compensation of a circadian clock in Drosophila. Science 267 (1995) 1169-1172
31. Kalmus H. Über die nature des zeitgedächtniss der bienen. Zeit. f Vergl. Physiol. 20 (1934) 405-419
32. Kalmus H. Periodizitat und Autochronie (Ideochronie) als zeitregelnde Eigenschaften der Organismen. Biologia Generalis 11 (1935) 93-114
33. Kuenzel E.A., and Krebs E.G. A synthetic peptide substrate specific for casein kinase II. Proc. Natl. Acad. Sci. USA 82 (1985) 737-741
34. Kurosawa G., and Iwasa Y. Temperature compensation in circadian clock models. J. Theor. Biol. 233 (2005) 453-468
35. Lahiri K., Vallone D., Gondi S.B., Santoriello C., Dickmeis T., and Foulkes N.S. Temperature regulates transcription in the zebrafish circadian clock. PLoS Biol. 3 (2005) e351 10.1371/journal.pbio.0030351
36. Lakin-Thomas P.L., Brody S., and Cote G.G. Amplitude model for the effects of mutations and temperature on period and phase resetting of the Neurospora circadian oscillator. J. Biol. Rhythms 6 (1991) 281-297
37. Lambreghts R., Shi M., Belden W.J., Decaprio D., Park D., Henn M.R., Galagan J.E., Basturkmen M., Birren B.W., Sachs M.S., et al. A high-density single nucleotide polymorphism map for Neurospora crassa. Genetics 181 (2009) 767-781
38. Larrondo L.F., Colot H.V., Baker C.L., Loros J.J., and Dunlap J.C. Fungal functional genomics: tunable knockout-knockin-expression and tagging strategies. Eukaryot. Cell (2009) 10.1128/EC.00072-09 Published online March 13, 2009
39. Leloup J.C., and Goldbeter A. Temperature compensation of circadian rhythms: control of the period in a model for circadian oscillations of the PER protein in Drosophila. Chronobiol. Int. 14 (1997) 511-520
40. Lin J.M., Kilman V.L., Keegan K., Paddock B., Emery-Le M., Rosbash M., and Allada R. A role for casein kinase 2 alpha in the Drosophila circadian clock. Nature 420 (2002) 816-820
41. Lin J.M., Schroeder A., and Allada R. In vivo circadian function of casein kinase 2 phosphorylation sites in Drosophila PERIOD. J. Neurosci. 25 (2005) 11175-11183
42. Litchfield D.W. Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem. J. 369 (2003) 1-15
43. Liu Y., and Bell-Pedersen D. Circadian rhythms in Neurospora crassa and other filamentous fungi. Eukaryot. Cell 5 (2006) 1184-1193
44. Liu Y., Garceau N.Y., Loros J.J., and Dunlap J.C. Thermally regulated translational control of FRQ mediates aspects of temperature responses in the Neurospora circadian clock. Cell 89 (1997) 477-486
45. Liu Y., Merrow M., Loros J.J., and Dunlap J.C. How temperature changes reset a circadian oscillator. Science 281 (1998) 825-829
46. Liu Y., Loros J., and Dunlap J.C. 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 (2000) 234-239
47. Mizoguchi T., Putterill J., and Ohkoshi Y. Kinase and phosphatase: the cog and spring of the circadian clock. Int. Rev. Cytol. 250 (2006) 47-72
48. Nawathean P., and Rosbash M. The doubletime and CKII kinases collaborate to potentiate Drosophila PER transcriptional repressor activity. Mol. Cell 13 (2004) 213-223
49. Njus D., McMurry L., and Hastings J.W. Conditionality of circadian rhythmicity: Synergistic action of light and temperature. J. Comp. Physiol. [B] 117 (1977) 335-344
50. Nowrousian M., Duffield G.E., Loros J.J., and Dunlap J.C. The frequency gene is required for temperature-dependent regulation of many clock-controlled genes in Neurospora crassa. Genetics 164 (2003) 923-933
51. Pagano M.A., Sarno S., Poletto G., Cozza G., Pinna L.A., and Meggio F. Autophosphorylation at the regulatory beta subunit reflects the supramolecular organization of protein kinase CK2. Mol. Cell. Biochem. 274 (2005) 23-29
52. Pittendrigh C.S. On temperature independence in the clock system controlling emergence time in Drosophila. Proc. Natl. Acad. Sci. USA 40 (1954) 1018-1029
53. Pittendrigh C.S. Temporal organization: reflections of a Darwinian clock-watcher. Annu. Rev. Physiol. 55 (1993) 16-54
54. Price J. Insights into the molecular mechanisms of temperature compensation from the Drosophila period and timeless mutants. Chronobiol. Int. 14 (1997) 455-468
55. Rothenfluh A., Abodeely M., Price J.L., and Young M.W. Isolation and analysis of six timeless alleles that cause short- or long-period circadian rhythms in Drosophila. Genetics 156 (2000) 665-675
56. Ruoff P., Rensing L., Kommedal R., and Mohsenzadeh S. Modeling temperature compensation in chemical and biological oscillators. Chronobiol. Int. 14 (1997) 499-510
57. Ruoff P., Loros J.J., and Dunlap J.C. The relationship between FRQ-protein stability and temperature compensation in the Neurospora circadian clock. Proc. Natl. Acad. Sci. USA 102 (2005) 17681-17686
58. Sawyer L.A., Hennessy J.M., Peixoto A.A., Rosato E., Parkinson H., Costa R., and Kyriacou C.P. Natural variation in a Drosophila clock gene and temperature compensation. Science 278 (1997) 2117-2120
59. Schibler U., and Sassone-Corsi P. A web of circadian pacemakers. Cell 111 (2002) 919-922
60. Smith F.S., and Konopka R.J. Effects of dosage alterations at the per locus on the period of the circadian clock of Drosophila. Mol. Gen. Genet. 185 (1982) 30-36
61. Sugano S., Andronis C., Green R.M., Wang Z.Y., and Tobin E.M. Protein kinase CK2 interacts with and phosphorylates the Arabidopsis circadian clock-associated 1 protein. Proc. Natl. Acad. Sci. USA 95 (1998) 11020-11025
62. Takeuchi T., Hinohara T., Kurosawa G., and Uchida K. A temperature-compensated model for circadian rhythms that can be entrained by temperature cycles. J. Theor. Biol. 246 (2007) 195-204
63. Taylor S.S., Knighton D.R., Zheng J., Ten Eyck L.F., and Sowadski J.M. Structural framework for the protein kinase family. Annu. Rev. Cell Biol. 8 (1992) 429-462
64. Tosini G., and Menaker M. The tau mutation affects temperature compensation of hamster retinal circadian oscillators. Neuroreport 9 (1998) 1001-1005
65. Wahl O. Neue untersuchungen Über das Zeitgedächtniss der Bienen. Zeit. f Vergl. Physiol. 16 (1932) 529-589
66. Wijnen H., and Young M.W. Interplay of circadian clocks and metabolic rhythms. Annu. Rev. Genet. 40 (2006) 409-448
67. Yang Y., Cheng P., and Liu Y. Regulation of the Neurospora circadian clock by casein kinase II. Genes Dev. 16 (2002) 994-1006
68. Yang Y., Cheng P., He Q., Wang L., and Liu Y. Phosphorylation of FREQUENCY protein by casein kinase II is necessary for the function of the Neurospora circadian clock. Mol. Cell. Biol. 23 (2003) 6221-6228
69. Yang Y., He Q., Cheng P., Wrage P., Yarden O., and Liu Y. Distinct roles for PP1 and PP2A in the Neurospora circadian clock. Genes Dev. 18 (2004) 255-260
70. Yde C.W., Ermakova I., Issinger O.G., and Niefind K. Inclining the purine base binding plane in protein kinase CK2 by exchanging the flanking side-chains generates a preference for ATP as a cosubstrate. J. Mol. Biol. 347 (2005) 399-414