Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Science 15 April 2005:
Vol. 308. no. 5720, pp. 414 - 415
DOI: 10.1126/science.1108451

Reports

Reconstitution of Circadian Oscillation of Cyanobacterial KaiC Phosphorylation in Vitro

Masato Nakajima, Keiko Imai, Hiroshi Ito, Taeko Nishiwaki, Yoriko Murayama, Hideo Iwasaki, Tokitaka Oyama, Takao Kondo*

Kai proteins globally regulate circadian gene expression of cyanobacteria. The KaiC phosphorylation cycle, which persists even without transcription or translation, is assumed to be a basic timing process of the circadian clock. We have reconstituted the self-sustainable oscillation of KaiC phosphorylation in vitro by incubating KaiC with KaiA, KaiB, and adenosine triphosphate. The period of the in vitro oscillation was stable despite temperature change (temperature compensation), and the circadian periods observed in vivo in KaiC mutant strains were consistent with those measured in vitro. The enigma of the circadian clock can now be studied in vitro by examining the interactions between three Kai proteins.

Division of Biological Science, Graduate School of Science, Nagoya University, and the Core Research for Evolutional Science and Technology (CREST) of the Japan Science and Technology Agency (JST), Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan.

* To whom correspondence should be addressed. E-mail: kondo{at}bio.nagoya-u.ac.jp

Read the Full Text



THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Basis of Robustness and Resilience in the Suprachiasmatic Nucleus: Individual Neurons Form Nodes in Circuits that Cycle Daily.
M. P. Butler and R. Silver (2009)
J Biol Rhythms 24, 340-352
   Abstract »    PDF »
CKI{varepsilon}/{delta}-dependent phosphorylation is a temperature-insensitive, period-determining process in the mammalian circadian clock.
Y. Isojima, M. Nakajima, H. Ukai, H. Fujishima, R. G. Yamada, K.-h. Masumoto, R. Kiuchi, M. Ishida, M. Ukai-Tadenuma, Y. Minami, et al. (2009)
PNAS 106, 15744-15749
   Abstract »    Full Text »    PDF »
Biochemical Evidence for a Timing Mechanism in Prochlorococcus.
I. M. Axmann, U. Duhring, L. Seeliger, A. Arnold, J. T. Vanselow, A. Kramer, and A. Wilde (2009)
J. Bacteriol. 191, 5342-5347
   Abstract »    Full Text »    PDF »
The Rolex and the Hourglass: a Simplified Circadian Clock in Prochlorococcus?.
C. W. Mullineaux and R. Stanewsky (2009)
J. Bacteriol. 191, 5333-5335
   Full Text »    PDF »
Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus.
H. Ito, M. Mutsuda, Y. Murayama, J. Tomita, N. Hosokawa, K. Terauchi, C. Sugita, M. Sugita, T. Kondo, and H. Iwasaki (2009)
PNAS 106, 14168-14173
   Abstract »    Full Text »    PDF »
A Novel Allele of kaiA Shortens the Circadian Period and Strengthens Interaction of Oscillator Components in the Cyanobacterium Synechococcus elongatus PCC 7942.
Y. Chen, Y.-I. Kim, S. R. Mackey, C. K. Holtman, A. LiWang, and S. S. Golden (2009)
J. Bacteriol. 191, 4392-4400
   Abstract »    Full Text »    PDF »
The Evolution of the Cyanobacterial Posttranslational Clock from a Primitive "Phoscillator".
M. J.P. Simons (2009)
J Biol Rhythms 24, 175-182
   Abstract »    PDF »
Nonparametric entrainment of the in vitro circadian phosphorylation rhythm of cyanobacterial KaiC by temperature cycle.
T. Yoshida, Y. Murayama, H. Ito, H. Kageyama, and T. Kondo (2009)
PNAS 106, 1648-1653
   Abstract »    Full Text »    PDF »
Stability and lability of circadian period of gene expression in the cyanobacterium Synechococcus elongatus.
E. M. Clerico, V. M. Cassone, and S. S. Golden (2009)
Microbiology 155, 635-641
   Abstract »    Full Text »    PDF »
Glucocorticoids and the circadian clock.
T. Dickmeis (2009)
J. Endocrinol. 200, 3-22
   Abstract »    Full Text »    PDF »
Functionally important structural elements of the cyanobacterial clock-related protein Pex.
S. Kurosawa, R. Murakami, K. Onai, M. Morishita, D. Hasegawa, R. Iwase, T. Uzumaki, F. Hayashi, T. Kitajima-Ihara, S. Sakata, et al. (2009)
Genes Cells 14, 1-16
   Abstract »    Full Text »    PDF »
Drosophila and Vertebrate Casein Kinase I{delta} Exhibits Evolutionary Conservation of Circadian Function.
J.-Y. Fan, F. Preuss, M. J. Muskus, E. S. Bjes, and J. L. Price (2009)
Genetics 181, 139-152
   Abstract »    Full Text »    PDF »
The Role of {beta}-TrCP1 and {beta}-TrCP2 in Circadian Rhythm Generation by Mediating Degradation of Clock Protein PER2.
K. Ohsaki, K. Oishi, Y. Kozono, K. Nakayama, K. I. Nakayama, and N. Ishida (2008)
J. Biochem. 144, 609-618
   Abstract »    Full Text »    PDF »
Structural Insights into a Circadian Oscillator.
C. H. Johnson, M. Egli, and P. L. Stewart (2008)
Science 322, 697-701
   Abstract »    Full Text »    PDF »
The day/night switch in KaiC, a central oscillator component of the circadian clock of cyanobacteria.
Y.-I. Kim, G. Dong, C. W. Carruthers Jr, S. S. Golden, and A. LiWang (2008)
PNAS 105, 12825-12830
   Abstract »    Full Text »    PDF »
Robust, Tunable Biological Oscillations from Interlinked Positive and Negative Feedback Loops.
T. Y.-C. Tsai, Y. S. Choi, W. Ma, J. R. Pomerening, C. Tang, and J. E. Ferrell Jr. (2008)
Science 321, 126-129
   Abstract »    Full Text »    PDF »
PERspective on PER phosphorylation.
J. Blau (2008)
Genes & Dev. 22, 1737-1740
   Abstract »    Full Text »    PDF »
Genome Streamlining Results in Loss of Robustness of the Circadian Clock in the Marine Cyanobacterium Prochlorococcus marinus PCC 9511.
J. Holtzendorff, F. Partensky, D. Mella, J.-F. Lennon, W. R. Hess, and L. Garczarek (2008)
J Biol Rhythms 23, 187-199
   Abstract »    PDF »
Lego clocks: building a clock from parts.
M. Brunner, M. J.P. Simons, and M. Merrow (2008)
Genes & Dev. 22, 1422-1426
   Abstract »    Full Text »    PDF »
Dual KaiC-based oscillations constitute the circadian system of cyanobacteria.
Y. Kitayama, T. Nishiwaki, K. Terauchi, and T. Kondo (2008)
Genes & Dev. 22, 1513-1521
   Abstract »    Full Text »    PDF »
cAMP-Dependent Signaling as a Core Component of the Mammalian Circadian Pacemaker.
J. S. O'Neill, E. S. Maywood, J. E. Chesham, J. S. Takahashi, and M. H. Hastings (2008)
Science 320, 949-953
   Abstract »    Full Text »    PDF »
Proteins Found in a CikA Interaction Assay Link the Circadian Clock, Metabolism, and Cell Division in Synechococcus elongatus.
S. R. Mackey, J.-S. Choi, Y. Kitayama, H. Iwasaki, G. Dong, and S. S. Golden (2008)
J. Bacteriol. 190, 3738-3746
   Abstract »    Full Text »    PDF »
The green yeast uses its plant-like clock to regulate its animal-like tail.
M. Brunner and M. Merrow (2008)
Genes & Dev. 22, 825-831
   Full Text »    PDF »
ATPase activity and its temperature compensation of the cyanobacterial clock protein KaiC..
R. Murakami, A. Miyake, R. Iwase, F. Hayashi, T. Uzumaki, and M. Ishiura (2008)
Genes Cells 13, 387-395
   Abstract »    Full Text »    PDF »
A systematic forward genetic analysis identified components of the Chlamydomonas circadian system.
T. Matsuo, K. Okamoto, K. Onai, Y. Niwa, K. Shimogawara, and M. Ishiura (2008)
Genes & Dev. 22, 918-930
   Abstract »    Full Text »    PDF »
Regulation of Circadian Clock Gene Expression by Phosphorylation States of KaiC in Cyanobacteria.
Y. Murayama, T. Oyama, and T. Kondo (2008)
J. Bacteriol. 190, 1691-1698
   Abstract »    Full Text »    PDF »
Probing the Relative Importance of Molecular Oscillations in the Circadian Clock.
X. Zheng and A. Sehgal (2008)
Genetics 178, 1147-1155
   Abstract »    Full Text »    PDF »
Casein kinase I{varepsilon} Does Not Rescue double-time Function in Drosophila Despite Evolutionarily Conserved Roles in the Circadian Clock.
T. Sekine, T. Yamaguchi, K. Hamano, M. W. Young, M. Shimoda, and L. Saez (2008)
J Biol Rhythms 23, 3-15
   Abstract »    PDF »
Protein kinase A and casein kinases mediate sequential phosphorylation events in the circadian negative feedback loop.
G. Huang, S. Chen, S. Li, J. Cha, C. Long, L. Li, Q. He, and Y. Liu (2007)
Genes & Dev. 21, 3283-3295
   Abstract »    Full Text »    PDF »
Drosophila DBT Lacking Protein Kinase Activity Produces Long-Period and Arrhythmic Circadian Behavioral and Molecular Rhythms.
M. J. Muskus, F. Preuss, J.-Y. Fan, E. S. Bjes, and J. L. Price (2007)
Mol. Cell. Biol. 27, 8049-8064
   Abstract »    Full Text »    PDF »
Circadian rhythms of superhelical status of DNA in cyanobacteria.
M. A. Woelfle, Y. Xu, X. Qin, and C. H. Johnson (2007)
PNAS 104, 18819-18824
   Abstract »    Full Text »    PDF »
Intracellular Ca2+ Regulates Free-Running Circadian Clock Oscillation In Vivo.
M. C. Harrisingh, Y. Wu, G. A. Lnenicka, and M. N. Nitabach (2007)
J. Neurosci. 27, 12489-12499
   Abstract »    Full Text »    PDF »
Ordered Phosphorylation Governs Oscillation of a Three-Protein Circadian Clock.
M. J. Rust, J. S. Markson, W. S. Lane, D. S. Fisher, and E. K. O'Shea (2007)
Science 318, 809-812
   Abstract »    Full Text »    PDF »
The Circadian Clock-Related Gene pex Regulates a Negative cis Element in the kaiA Promoter Region.
S. Kutsuna, T. Kondo, H. Ikegami, T. Uzumaki, M. Katayama, and M. Ishiura (2007)
J. Bacteriol. 189, 7690-7696
   Abstract »    Full Text »    PDF »
The cyanobacterial circadian clock is based on the intrinsic ATPase activity of KaiC.
C. R. McClung (2007)
PNAS 104, 16727-16728
   Full Text »    PDF »
ATPase activity of KaiC determines the basic timing for circadian clock of cyanobacteria.
K. Terauchi, Y. Kitayama, T. Nishiwaki, K. Miwa, Y. Murayama, T. Oyama, and T. Kondo (2007)
PNAS 104, 16377-16381
   Abstract »    Full Text »    PDF »
A DOUBLETIME Kinase Binding Domain on the Drosophila PERIOD Protein Is Essential for Its Hyperphosphorylation, Transcriptional Repression, and Circadian Clock Function.
E. Y. Kim, H. W. Ko, W. Yu, P. E. Hardin, and I. Edery (2007)
Mol. Cell. Biol. 27, 5014-5028
   Abstract »    Full Text »    PDF »
A Functional Link between Rhythmic Changes in Chromatin Structure and the Arabidopsis Biological Clock.
M. Perales and P. Mas (2007)
PLANT CELL 19, 2111-2123
   Abstract »    Full Text »    PDF »
An allosteric model of circadian KaiC phosphorylation.
J. S. van Zon, D. K. Lubensky, P. R. H. Altena, and P. R. ten Wolde (2007)
PNAS 104, 7420-7425
   Abstract »    Full Text »    PDF »
Cyanobacterial clock, a stable phase oscillator with negligible intercellular coupling.
M. Amdaoud, M. Vallade, C. Weiss-Schaber, and I. Mihalcescu (2007)
PNAS 104, 7051-7056
   Abstract »    Full Text »    PDF »
A Mathematical Model for the Kai-Protein-Based Chemical Oscillator and Clock Gene Expression Rhythms in Cyanobacteria.
F. Miyoshi, Y. Nakayama, K. Kaizu, H. Iwasaki, and M. Tomita (2007)
J Biol Rhythms 22, 69-80
   Abstract »    PDF »
Label-free Kinase Profiling Using Phosphate Affinity Polyacrylamide Gel Electrophoresis.
E. Kinoshita-Kikuta, Y. Aoki, E. Kinoshita, and T. Koike (2007)
Mol. Cell. Proteomics 6, 356-366
   Abstract »    Full Text »    PDF »
Structural and Biochemical Characterization of a Cyanobacterium Circadian Clock-modifier Protein.
K. Arita, H. Hashimoto, K. Igari, M. Akaboshi, S. Kutsuna, M. Sato, and T. Shimizu (2007)
J. Biol. Chem. 282, 1128-1135
   Abstract »    Full Text »    PDF »
Biological Rhythms Workshop I: Introduction to Chronobiology.
S. J. Kuhlman, S. R. Mackey, and J. F. Duffy (2007)
Cold Spring Harb Symp Quant Biol 72, 1-6
   Abstract »    PDF »
Biological Rhythms Workshop IA: Molecular Basis of Rhythms Generation.
S. R. Mackey (2007)
Cold Spring Harb Symp Quant Biol 72, 7-19
   Abstract »    PDF »
A Cyanobacterial Circadian Clock Based on the Kai Oscillator.
T. Kondo (2007)
Cold Spring Harb Symp Quant Biol 72, 47-55
   Abstract »    PDF »
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.
J.C. Dunlap, J.J. Loros, H.V. Colot, A. Mehra, W.J. Belden, M. Shi, C.I. Hong, L.F. Larrondo, C.L. Baker, C.-H. Chen, et al. (2007)
Cold Spring Harb Symp Quant Biol 72, 57-68
   Abstract »    PDF »
Transcriptional Feedback and Definition of the Circadian Pacemaker in Drosophila and Animals.
M. Rosbash, S. Bradley, S. Kadener, Y. Li, W. Luo, J. S. Menet, E. Nagoshi, K. Palm, R. Schoer, Y. Shang, et al. (2007)
Cold Spring Harb Symp Quant Biol 72, 75-83
   Abstract »    PDF »
The Multiple Facets of Per2.
U. Albrecht, A. Bordon, I. Schmutz, and J. Ripperger (2007)
Cold Spring Harb Symp Quant Biol 72, 95-104
   Abstract »    PDF »
Role of Phosphorylation in the Mammalian Circadian Clock.
K. Vanselow and A. Kramer (2007)
Cold Spring Harb Symp Quant Biol 72, 167-176
   Abstract »    PDF »
Posttranslational Control of the Neurospora Circadian Clock.
J. Cha, G. Huang, J. Guo, and Y. Liu (2007)
Cold Spring Harb Symp Quant Biol 72, 185-191
   Abstract »    PDF »
Circadian Entrainment of Neurospora crassa.
M. Merrow and T. Roenneberg (2007)
Cold Spring Harb Symp Quant Biol 72, 279-285
   Abstract »    PDF »
Integrating the Circadian Oscillator into the Life of the Cyanobacterial Cell.
S. S. Golden (2007)
Cold Spring Harb Symp Quant Biol 72, 331-338
   Abstract »    PDF »
Systems Biology of Mammalian Circadian Clocks.
H. R. Ueda (2007)
Cold Spring Harb Symp Quant Biol 72, 365-380
   Abstract »    PDF »
Bacterial Circadian Programs.
C. H. Johnson (2007)
Cold Spring Harb Symp Quant Biol 72, 395-404
   Abstract »    PDF »
Thermosensitive Splicing of a Clock Gene and Seasonal Adaptation.
W.-F. Chen, K. H. Low, C. Lim, and I. Edery (2007)
Cold Spring Harb Symp Quant Biol 72, 599-606
   Abstract »    PDF »
labA: a novel gene required for negative feedback regulation of the cyanobacterial circadian clock protein KaiC.
Y. Taniguchi, M. Katayama, R. Ito, N. Takai, T. Kondo, and T. Oyama (2007)
Genes & Dev. 21, 60-70
   Abstract »    Full Text »    PDF »
No Promoter Left Behind: Global Circadian Gene Expression in Cyanobacteria.
M. A. Woelfle and C. H. Johnson (2006)
J Biol Rhythms 21, 419-431
   Abstract »    PDF »
Properties, Entrainment, and Physiological Functions of Mammalian Peripheral Oscillators.
M. Stratmann and U. Schibler (2006)
J Biol Rhythms 21, 494-506
   Abstract »    PDF »
Quinone sensing by the circadian input kinase of the cyanobacterial circadian clock.
N. B. Ivleva, T. Gao, A. C. LiWang, and S. S. Golden (2006)
PNAS 103, 17468-17473
   Abstract »    Full Text »    PDF »
Regulating a Circadian Clock's Period, Phase and Amplitude by Phosphorylation: Insights from Drosophila.
K. Bae and I. Edery (2006)
J. Biochem. 140, 609-617
   Abstract »    Full Text »    PDF »
The right place at the right time: regulation of daily timing by phosphorylation.
M. Merrow, G. Mazzotta, Z. Chen, and T. Roenneberg (2006)
Genes & Dev. 20, 2629-2633
   Full Text »    PDF »
Differential effects of PER2 phosphorylation: molecular basis for the human familial advanced sleep phase syndrome (FASPS).
K. Vanselow, J. T. Vanselow, P. O. Westermark, S. Reischl, B. Maier, T. Korte, A. Herrmann, H. Herzel, A. Schlosser, and A. Kramer (2006)
Genes & Dev. 20, 2660-2672
   Abstract »    Full Text »    PDF »
Two-component signaling provides the major output from the cyanobacterial circadian clock.
C. R. McClung (2006)
PNAS 103, 11819-11820
   Full Text »    PDF »
From the Cover: A KaiC-associating SasA-RpaA two-component regulatory system as a major circadian timing mediator in cyanobacteria.
N. Takai, M. Nakajima, T. Oyama, R. Kito, C. Sugita, M. Sugita, T. Kondo, and H. Iwasaki (2006)
PNAS 103, 12109-12114
   Abstract »    Full Text »    PDF »
Clock-Gated Photic Stimulation of Timeless Expression at Cold Temperatures and Seasonal Adaptation in Drosophila.
W.-F. Chen, J. Majercak, and I. Edery (2006)
J Biol Rhythms 21, 256-271
   Abstract »    PDF »
The BMAL1 C terminus regulates the circadian transcription feedback loop.
Y. B. Kiyohara, S. Tagao, F. Tamanini, A. Morita, Y. Sugisawa, M. Yasuda, I. Yamanaka, H. R. Ueda, G. T. J. van der Horst, T. Kondo, et al. (2006)
PNAS 103, 10074-10079
   Abstract »    Full Text »    PDF »
Circadian rhythms in gene transcription imparted by chromosome compaction in the cyanobacterium Synechococcus elongatus.
R. M. Smith and S. B. Williams (2006)
PNAS 103, 8564-8569
   Abstract »    Full Text »    PDF »
Transcriptional and post-transcriptional regulation of the circadian clock of cyanobacteria and Neurospora..
M. Brunner and T. Schafmeier (2006)
Genes & Dev. 20, 1061-1074
   Abstract »    Full Text »    PDF »
Transcriptional Feedback Oscillators: Maybe, Maybe Not....
P. L. Lakin-Thomas (2006)
J Biol Rhythms 21, 83-92
   Abstract »    PDF »
Plant circadian rhythms..
C. R. McClung (2006)
PLANT CELL 18, 792-803
   Full Text »    PDF »
Phosphorylation-dependent maturation of Neurospora circadian clock protein from a nuclear repressor toward a cytoplasmic activator.
T. Schafmeier, K. Kaldi, A. Diernfellner, C. Mohr, and M. Brunner (2006)
Genes & Dev. 20, 297-306
   Abstract »    Full Text »    PDF »
In Vivo Circadian Function of Casein Kinase 2 Phosphorylation Sites in Drosophila PERIOD.
J.-M. Lin, A. Schroeder, and R. Allada (2005)
J. Neurosci. 25, 11175-11183
   Abstract »    Full Text »    PDF »
Structure of a nonheme globin in environmental stress signaling.
J. W. Murray, O. Delumeau, and R. J. Lewis (2005)
PNAS 102, 17320-17325
   Abstract »    Full Text »    PDF »
PHYTOCLOCK 1 encoding a novel GARP protein essential for the Arabidopsis circadian clock.
K. Onai and M. Ishiura (2005)
Genes Cells 10, 963-972
   Abstract »    Full Text »    PDF »
Stability of the Synechococcus elongatus PCC 7942 circadian clock under directed anti-phase expression of the kai genes.
J. L. Ditty, S. R. Canales, B. E. Anderson, S. B. Williams, and S. S. Golden (2005)
Microbiology 151, 2605-2613
   Abstract »    Full Text »    PDF »
Reconstitution of Circadian Oscillation of Cyanobacterial KaiC Phosphorylation in Vitro.
M. Nakajima, K. Imai, H. Ito, T. Nishiwaki, Y. Murayama, H. Iwasaki, T. Oyama, and T. Kondo (2005)
Science 308, 414-415
   Abstract »    Full Text »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)