Kinase and Phosphatase: The Cog and Spring of the Circadian Clock

International Review of Cytology

Volumn 250, Issue , 2006, Pages 47-72

  Mizoguchi, Tsuyoshi ^a   Putterill, Johanna ^b   Ohkoshi, Yuri ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Arabidopsis; Casein kinase II (CK2); Circadian rhythms; LHY CCA1; Photoperiod; Protein kinase; Protein phosphatase; Protein phosphorylation

Indexed keywords

CASEIN KINASE II; PHOSPHATASE; PHOSPHOENOLPYRUVATE CARBOXYLASE; PHOSPHOTRANSFERASE; STAUROSPORINE;

ANIMAL; BACTERIUM; CELL CYCLE; CIRCADIAN RHYTHM; CYANOBACTERIUM; EUKARYOTE; FUNGUS; GENE; GENOMICS; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; PLANT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REVIEW; TWO HYBRID SYSTEM; YEAST;

ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL CLOCKS; CELL CYCLE; CIRCADIAN RHYTHM; EVOLUTION; FUNGAL PROTEINS; GENE EXPRESSION REGULATION; ISOENZYMES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PLANT PROTEINS; PROTEIN KINASES; PROTEIN SUBUNITS;

ANIMALIA; ARABIDOPSIS; EUKARYOTA; FUNGI; NEUROSPORA;

EID: 33745999820     PISSN: 00747696     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0074-7696(06)50002-6     Document Type: Review

References (93)

1. Ahmad M., Jarillo J.A., Smirnova O., and Cashmore A.R. The CRY1 blue light photoreceptor of Arabidopsis interacts with phytochrome A in vitro. Mol. Cell 1 (1998) 939-948
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. Alabadí D., Oyama T., Yanovsky M.J., Harmon F.G., Mas P., and Kay S.A. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293 (2001) 880-883
4. Alabadí D., Yanovsky M.J., Mas P., Harmer S.L., and Kay S.A. Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Curr. Biol. 12 (2002) 757-761
5. Alonso J.M., Stepanova A.N., Leisse T.J., et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 (2003) 653-657
6. The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408 (2000) 796-815
7. Bao S., Rihel J., Bjes E., Fan J.Y., and Price J.L. The Drosophila double-timeS mutation delays the nuclear accumulation of period protein and affects the feedback regulation of period mRNA. J. Neurosci. 21 (2001) 7117-7126
8. Barak S., Tobin E.M., Andronis C., Sugano S., and Green R.M. All in good time: The Arabidopsis circadian clock. Trends Plant Sci. 5 (2000) 517-522
9. Chicurel M. Mutant genes speeds up the human clock. Science 291 (2001) 226-227
10. Comolli J.C., and Hastings J.W. Novel effects on the Gonyaulax circadian system produced by the protein kinase inhibitor staurosporine. J. Biol. Rhythms 14 (1999) 11-19
11. Daniel X., Sugano S., and Tobin E.M. CK2 phosphorylation of CCA1 is necessary for its circadian oscillator function in Arabidopsis. Proc. Natl. Acad. Sci. USA 101 (2004) 3292-3297
12. Doyle M.R., Davis S.J., Bastow R.M., McWatters H.G., Kozma-Bognar L., Nagy F., Millar A.J., and Amasino R.M. The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 419 (2002) 74-77
13. Dunlap J.C. Molecular bases for circadian clocks. Cell 96 (1999) 271-290
14. Fankhauser C., Yeh K.C., Lagarias J.C., Zhang H., Elich T.D., and Chory J. PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science 284 (1999) 1539-1541
15. Fowler S., Lee K., Onouchi H., Samach A., Richardson K., Morris B., Coupland G., and Putterill J. GIGANTEA: A circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 18 (1999) 4769-4788
16. Glossop N.R., Lyons L.C., and Hardin P.E. Interlocked feedback loops within the Drosophila circadian oscillator. Science 286 (1999) 766-768
17. Green R.M., and Tobin E.M. Loss of the circadian clock-associated protein 1 in Arabidopsis results in altered clock-regulated gene expression. Proc. Natl. Acad. Sci. USA 96 (1999) 4176-4179
18. Green R.M., Tingay S., Wang Z.Y., and Tobin E.M. Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol. 129 (2002) 576-584
19. Grima B., Lamouroux A., Chelot E., Papin C., Limbourg-Bouchon B., and Rouyer F. The F-box protein slimb controls the levels of clock proteins period and timeless. Nature 420 (2002) 178-182
20. Groves M.R., Hanlon N., Turowski P., Hemmings B.A., and Barford D. The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs. Cell 96 (1999) 99-110
21. Hall A., Bastow R.M., Davis S.J., Hanano S., McWatters H.G., Hibberd V., Doyle M.R., Sung S., Halliday K.J., Amasino R.M., and Millar A.J. The TIME FOR COFFEE gene maintains the amplitude and timing of Arabidopsis circadian clocks. Plant Cell 15 (2003) 2719-2729
22. Harmer S.L., Hogenesch J.B., Straume M., Chang H.S., Han B., Zhu T., Wang X., Kreps J.A., and Kay S.A. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290 (2000) 2110-2113
23. Hartwell J., Gill A., Nimmo G.A., Wilkins M.B., Jenkins G.I., and Nimmo H.G. Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression. Plant J. 20 (1999) 333-342
24. He Q., Cheng P., Yang Y., He Q., Yu H., and Liu Y. FWD1-mediated degradation of FREQUENCY in Neurospora establishes a conserved mechanism for circadian clock regulation. EMBO J. 22 (2003) 4421-4430
25. Imai K., Nishiwaki T., Kondo T., and Iwasaki H. Circadian rhythms in the synthesis and degradation of a master clock protein KaiC in cyanobacteria. J. Biol. Chem. 279 (2004) 36534-36539
26. Ishiura M., Kutsuna S., Aoki S., Iwasaki H., Andersson C.R., Tanabe A., Golden S.S., Johnson C.H., and Kondo T. Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science 281 (1998) 1519-1523
27. Iwasaki H., and Kondo T. Circadian timing mechanism in the prokaryotic clock system of cyanobacteria. J. Biol. Rhythms 19 (2004) 436-444
28. Iwasaki H., Nishiwaki T., Kitayama Y., Nakajima M., and Kondo T. KaiA-stimulated KaiC phosphorylation in circadian timing loops in cyanobacteria. Proc. Natl. Acad. Sci. USA 99 (2002) 15788-15793
29. Janssens V., and Goris J. Protein phosphatase 2A: A highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem. J. 353 (2001) 417-439
30. Kerk D., Bulgrein J., Smith D.W., Barsam B., Veretrik S., and Grivskov M. The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiol. 129 (2002) 908-925
31. Kitayama Y., Iwasaki H., Nishiwaki T., and Kondo T. KaiB functions as an attenuator of KaiC phosphorylation in the cyanobacterial circadian clock system. EMBO J. 22 (2003) 2127-2134
32. Kiyosue T., and Wada M. LKP1 (LOV kelch protein 1): A factor involved in the regulation of flowering time in Arabidopsis. Plant J. 23 (2000) 807-815
33. Kloss B., Price J.L., Saez L., Blau J., Rothenfluh A., Wesley C.S., and Young M.W. The Drosophila clock gene double-time encodes a protein closely related to human casein kinase Iepsilon. Cell 94 (1998) 97-107
34. Lin J.M., Kilman V.L., Keegan K., Paddock B., Emery-Le M., Rosbash M., and Allada R. A role for casein kinase 2alpha in the Drosophila circadian clock. Nature 420 (2002) 816-820
35. Loros J.J., and Dunlap J.C. Genetic and molecular analysis of circadian rhythms in Neurospora. Annu. Rev. Physiol. 63 (2001) 757-794
36. Loschelder H., Homann A., Ogrzewalla K., and Link G. Proteomics-based sequence analysis of plant gene expression-the chloroplast transcription apparatus. Phytochemistry 65 (2004) 1785-1793
37. Lowrey P.L., Shimomura K., Antoch M.P., Yamazaki S., Zemenides P.D., Ralph M.R., Menaker M., and Takahashi J.S. Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science 288 (2000) 483-491
38. Makino S., Kiba T., Imamura A., Hanaki N., Nakamura A., Suzuki T., Taniguchi M., Ueguchi C., Sugiyama T., and Mizuno T. Genes encoding pseudo-response regulators: Insight into His-to-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana. Plant Cell Physiol. 41 (2000) 791-803
39. Martinek S., Inonog S., Manoukian A.S., and Young M.W. A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 105 (2001) 769-779
40. Mas P., Alabadí D., Yanovsky M.J., Oyama T., and Kay S.A. Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. Plant Cell 15 (2003) 223-236
41. Matsuo T., Yamaguchi S., Mitsui S., Emi A., Shimoda F., and Okamura H. Control mechanism of the circadian clock for timing of cell division in vivo. Science 302 (2003) 255-259
42. Matsushika A., Makino S., Kojima M., and Mizuno T. Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: Insight into the plant circadian clock. Plant Cell Physiol. 41 (2000) 1002-1012
43. Matsushika A., Makino S., Kojima M., Yamashino T., and Mizuno T. The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana: II. Characterization with CCA1-overexpressing plants. Plant Cell Physiol. 43 (2002) 118-122
44. McClung C.R., Salomé P.A., and Michael T.P. The Arabidopsis circadian system. In: Somerville C.R., and Meyerowitz E.M. (Eds). "The Arabidopsis Book" (2002), American Society of Plant Biologists, Rockville, MD. Available online at www.aspb.org/publications/arabidopsis/ 10.1199/tab.0044
45. McDonald M.J., and Rosbash M. Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107 (2001) 567-578
46. Michael T.P., Salom P.A., Yu H.J., Spencer T.R., Sharp E.L., McPeek M.A., Alonso J.M., Ecker J.R., and McClung C.R. Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302 (2003) 1049-1053
47. Millar A.J., Carre I.A., Strayer C.A., Chua N.H., and Kay S.A. Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science 267 (1995) 1161-1163
48. Mizoguchi T., and Coupland G. ZEITLUPE and FKF1: Novel connections between flowering time and circadian clock control. Trends Plant Sci. 5 (2000) 409-411
49. Mizoguchi T., Yamaguchi-Shinozaki K., Hayashida N., Kamada H., and Shinozaki K. Cloning and characterization of two cDNAs encoding casein kinase II catalytic subunits in Arabidopsis thaliana. Plant Mol. Biol. 21 (1993) 279-289
50. Mizoguchi T., Wheatley K., Hanzawa Y., Wright L., Mizoguchi M., Song H.R., Carre I.A., and Coupland G. LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev. Cell 2 (2002) 629-641
51. Mizoguchi T., Wright L., Fujiwara S., Cremer F., Lee K., Onouchi H., Mouradov A., Fowler S., Kamada H., Putterill J., and Coupland G. Distinct roles for GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17 (2005) 2255-2270
52. Mizuno T., and Nakamichi N. Pseudo-response regulators (PRRs) or true oscillator components (TOCs). Plant Cell Physiol. 46 (2005) 677-685
53. Murakami-Kojima M., Nakamichi N., Yamashino T., and Mizuno T. The APRR3 component of the clock-associated APRR1/TOC1 quintet is phosphorylated by a novel protein kinase belonging to the WNK family, the gene for which is also transcribed rhythmically in Arabidopsis thaliana. Plant Cell Physiol. 43 (2002) 675-683
54. Murakami M., Yamashino T., and Mizuno T. Characterization of circadian-associated APRR3 pseudo-response regulator belonging to the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol. 45 (2004) 645-650
55. Nakajima M., Imai K., Ito H., Nishiwaki T., Murayama Y., Iwasaki H., Oyama T., and Kondo T. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308 (2005) 414-415
56. Nakamichi N., Murakami-Kojima M., Sato E., Kishi Y., Yamashino T., and Mizuno T. Compilation and characterization of a novel WNK family of protein kinases in Arabidopsis thaliana with reference to circadian rhythms. Biosci. Biotechnol. Biochem. 66 (2002) 2429-2436
57. Nelson D.C., Lasswell J., Rogg L.E., Cohen M.A., and Bartel B. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101 (2000) 331-340
58. Nimmo H.G. The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends Plant Sci. 5 (2000) 75-80
59. Nishiwaki T., Iwasaki H., Ishiura M., and Kondo T. Nucleotide binding and autophosphorylation of the clock protein KaiC as a circadian timing process of cyanobacteria. Proc. Natl. Acad. Sci. USA 97 (2000) 495-499
60. Ogrzewalla K., Piotrowski M., Reinbothe S., and Link G. The plastid transcription kinase from mustard (Sinapis alba L.). A nuclear-encoded CK2-type chloroplast enzyme with redox-sensitive function. Eur. J. Biochem. 269 (2002) 3329-3337
61. Park D.H., Somers D.E., Kim Y.S., Choy Y.H., Lim H.K., Soh M.S., Kim H.J., Kay S.A., and Nam H.G. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285 (1999) 1579-1582
62. Pennisi E. Syngenta donates 48,000 mutant Arabidopsis plants. Science 304 (2004) 1426
63. Price J.L., Blau J., Rothenfluh A., Abodeely M., Kloss B., and Young M.W. double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94 (1998) 83-95
64. Roenneberg T., and Merrow M. "What watch?...such much!" Complexity and evolution of circadian clocks. Cell Tissue Res. 309 (2002) 3-9
65. Ryu J.S., Kim J.I., Kunkel T., Kim B.C., Cho D.S., Hong S.H., Kim S.H., Fernandez A.P., Kim Y., Alonso J.M., Ecker J.R., Nagy F., Lim P.O., Song P.S., Schafer E., and Nam H.G. Phytochrome-specific type 5 phosphatase controls light signal flux by enhancing phytochrome stability and affinity for a signal transducer. Cell 120 (2005) 395-406
66. Sathyanarayanan S., Zheng X., Xiao R., and Sehgal A. Posttranslational regulation of Drosophila PERIOD protein by protein phosphatase 2A. Cell 116 (2004) 603-615
67. Schaffer R., Ramsay N., Samach A., Corden S., Putterill J., Carre I.A., and Coupland G. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93 (1998) 1219-1229
68. Schaffer R., Landgraf J., Accerbi M., Simon V., Larson M., and Wisman E. Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13 (2001) 113-123
69. Schoning J.C., and Straiger D. At the pulse of time: Protein interactions determine the pace of circadian clocks. FEBS Lett. 579 (2005) 3246-3252
70. Schultz T.F., Kiyosue T., Yanovsky M., Wada M., and Kay S.A. A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell 13 (2001) 2659-2670
71. Shalitin D., Yang H., Mockler T.C., Maymon M., Guo H., Whitelam G.C., and Lin C. Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation. Nature 417 (2002) 763-767
72. Somers D.E. The physiology and molecular bases of the plant circadian clock. Plant Physiol. 121 (1999) 9-20
73. Somers D.E., Webb A.A., Pearson M., and Kay S.A. The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development 125 (1998) 485-494
74. Somers D.E., Schultz T.F., Milnamow M., and Kay S.A. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101 (2000) 319-329
75. Strayer C., Oyama T., Schultz T.F., Raman R., Somers D.E., Mas P., Panda S., Kreps J.A., and Kay S.A. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289 (2000) 768-771
76. 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
77. Sugano S., Andronis C., Ong M.S., Green R.M., and Tobin E.M. The protein kinase CK2 is involved in regulation of circadian rhythms in Arabidopsis. Proc. Natl. Acad. Sci. USA 96 (1999) 12362-12366
78. Takahashi Y., Shomura A., Sasaki T., and Yano M. Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc. Natl. Acad. Sci. USA 98 (2001) 7922-7927
79. Toh K.L., Jones C.R., He Y., Eide E.J., Hinz W.A., Virshup D.M., Ptacek L.J., and Fu Y.H. An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 291 (2001) 1040-1043
80. Tomita J., Nakajima M., Kondo T., and Iwasaki H. No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 307 (2005) 251-254
81. Virshup D.M. Protein phosphatase 2A: A panoply of enzymes. Curr. Opin. Cell Biol. 12 (2000) 180-185
82. Wang D., Harper J.F., and Gribskov M. Systematic trans-genomic comparison of protein kinases between Arabidopsis and Saccharomyces cerevisiae. Plant Physiol. 132 (2003) 2152-2165
83. Wang Z.Y., and Tobin E.M. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93 (1998) 1207-1217
84. Wang Z.Y., Kenigsbuch D., Sun L., Harel E., Ong M.S., and Tobin E.M. A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 9 (1997) 491-507
85. Wilson F.H., Disse-Nicodeme S., Choate K.A., Ishikawa K., Nelson-Williams C., Desitter I., Gunel M., Milford D.V., Lipkin G.W., Achard J.M., Feely M.P., Dussol B., Berland Y., Unwin R.J., Mayan H., Simon D.B., Farfel Z., Jeunemaitre X., and Lifton R.P. Human hypertension caused by mutations in WNK kinases. Science 293 (2001) 1107-1112
86. Xu Y., Mori T., and Johnson C.H. Cyanobacterial circadian clockwork: Roles of KaiA, KaiB and the kaiBC promoter in regulating KaiC. EMBO J. 22 (2003) 2117-2126
87. 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. Functional consequences of a CKIdelta mutation causing familial advanced sleep phase syndrome. Nature 434 (2005) 640-644
88. Yang Y., Cheng P., Zhi G., and Liu Y. Identification of a calcium/calmodulin-dependent protein kinase that phosphorylates the Neurospora circadian clock protein FREQUENCY. J. Biol. Chem. 276 (2001) 41064-41072
89. Yang Y., Cheng P., and Liu Y. Regulation of the Neurospora circadian clock by casein kinase II. Genes Dev. 16 (2002) 994-1006
90. 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
91. 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
92. Yeh K.C., and Lagarias J.C. Eukaryotic phytochromes: Light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl. Acad. Sci. USA 95 (1998) 13976-13981
93. Young M.W., and Kay S.A. Time zones: A comparative genetics of circadian clocks. Nat. Rev. Genet. 2 (2001) 702-715