ATPase activity of KaiC determines the basic timing for circadian clock of cyanobacteria

Terauchi, Kazuki; Kitayama, Yohko; Nishiwaki, Taeko; Miwa, Koichi; Murayama, Yuko; Oyama, Tokitaka; Kondo, Takao

doi:10.1073/pnas.0706292104

Cited by 244 publications

(452 citation statements)

References 19 publications

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“…Terauchi et al (5) show that the ATPase activity of KaiC is only slightly affected by temperature (Q 10 Ϸ 1.2) in mixtures with KaiA and KaiB, which is consistent with the in vivo rhythm in cyanobacterial gene expression. Interestingly, the ATPase activity of KaiC when incubated without KaiA and KaiB is almost constant across temperatures.…”

supporting

confidence: 50%

“…The activity of KaiC (15 ATP per day) is unusually low. Terauchi et al (5) hypothesize that ATP hydrolysis by KaiC induces conformational change in the KaiC hexamer, which may slow the rate of ATP hydrolysis, and they further speculate that this autoregulation may contribute to temperature compensation. Additional biophysical and structural analyses should enhance understanding of how intra-and intermolecular interactions affect ATPase activity.…”

mentioning

confidence: 99%

“…The kaiABC locus is essential for rhythmicity (2), and recently a self-sustaining and temperaturecompensated circadian rhythm in the phosphorylation of KaiC has been reconstituted in vitro in a minimal system containing the three Kai (Japanese for ''cycle'') proteins plus ATP (3,4). In a recent issue of PNAS, Terauchi et al (5) established that the ATPase activity of KaiC is the fundamental reaction underlying the cyanobacterial circadian oscillation (Fig. 1).…”

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confidence: 99%

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The cyanobacterial circadian clock is based on the intrinsic ATPase activity of KaiC

McClung

2007

Proc. Natl. Acad. Sci. U.S.A.

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confidence: 99%

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The cyanobacterial circadian clock is based on the intrinsic ATPase activity of KaiC

McClung

2007

Proc. Natl. Acad. Sci. U.S.A.

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“…However, the circadian rhythm of KaiC phosphorylation persisted for at least 3 cycles after the rapid disappearance of kaiABC mRNA under continuous dark (DD) conditions even in the presence of excess transcription and translation inhibitors (2). More strikingly, incubating the 3 recombinant Kai proteins with ATP was sufficient to generate a temperature-compensated circadian KaiC phosphorylation cycle in vitro (3,4). Thus, the core process in generating basic oscillation is not a transcription/ translation feedback but is likely to be an enzymatic oscillation of KaiC phosphorylation/ATPase activities.…”

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confidence: 99%

Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus

Ito

Mutsuda²,

Murayama³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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In the unicellular cyanobacterium Synechococcus elongatus PCC 7942, essentially all promoter activities are under the control of the circadian clock under continuous light (LL) conditions. Here, we used high-density oligonucleotide arrays to explore comprehensive profiles of genome-wide Synechococcus gene expression in wild-type, kaiABC-null, and kaiC-overexpressor strains under LL and continuous dark (DD) conditions. In the wild-type strains, >30% of transcripts oscillated significantly in a circadian fashion, peaking at subjective dawn and dusk. Such circadian control was severely attenuated in kaiABC-null strains. Although it has been proposed that KaiC globally represses gene expression, our analysis revealed that dawn-expressed genes were up-regulated by kaiC-overexpression so that the clock was arrested at subjective dawn. Transfer of cells to DD conditions from LL immediately suppressed expression of most of the genes, while the clock kept even time in the absence of transcriptional feedback. Thus, the Synechococcus genome seems to be primarily regulated by light/ dark cycles and is dramatically modified by the protein-based circadian oscillator.circadian clock ͉ cyanobacteria ͉ genome-wide expression ͉ KaiC ͉ light:dark

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“…Among these, studies on a prokaryotic model organism, cyanobacterium (Synechococcus elongatus PCC 7942), demonstrated that circadian oscillation of KaiC phosphorylation could be reconstituted in vitro by incubating the three Kai proteins and adenosine triphosphate (ATP) (3). Further studies have shown that an extremely weak but temperature-compensated ATPase activity of KaiC is tightly linked to the circadian period (4) and coupled to KaiC kinase/phosphatase activities to generate robust circadian oscillation (5). In cyanobacterial cells, time profiles of induction or repression of gene expression by KaiC match the circadian period (6).…”

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confidence: 99%

Nonparametric entrainment of the in vitro circadian phosphorylation rhythm of cyanobacterial KaiC by temperature cycle

Yoshida

Murayama

Ito

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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The three cyanobacterial Kai proteins and ATP are capable of generating an autonomous rhythm of KaiC phosphorylation in a test tube. As the period is Ϸ24 hours and is stable in a wide temperature range, this rhythm is thought to function as the basic oscillator of the cyanobacterial circadian system. We have examined the rhythm under various temperature cycles and found that it was stably entrained by a temperature cycle of 20 -28 hours. As the period length was not altered by temperature, entrainment by period change could be excluded from possible mechanisms. Instead, temperature steps between 30°and 45°C and vice versa shifted the phase of the rhythm in a phase-dependent manner. Based on the phase response curves of the step-up and step-down in temperature, phase shift by single temperature pulse was estimated using a nonparametric entrainment model (discontinuous phase jump by external stimuli). The predicted phase shift was consistent with the experimentally measured phase shift. Next, successive phase shifts caused by repeated temperature cycles were computed by two phase response curves and compared with actual entrainment of the rhythm. As the entrainment pattern observed after various combinations of temperature cycles matched the prediction, it is likely that nonparametric entrainment functions even in the simple three-protein system. We also analyzed entrainment of KaiC phosphorylation by temperature cycle in cyanobacterial cells and found both the parametric and the nonparametric models function in vivo.circadian clock ͉ KaiC phosphorylation rhythm ͉ Phase response ͉ temperature entrainment

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ATPase activity of KaiC determines the basic timing for circadian clock of cyanobacteria

Cited by 244 publications

References 19 publications

The cyanobacterial circadian clock is based on the intrinsic ATPase activity of KaiC

The cyanobacterial circadian clock is based on the intrinsic ATPase activity of KaiC

Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus

Nonparametric entrainment of the in vitro circadian phosphorylation rhythm of cyanobacterial KaiC by temperature cycle

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