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Circadian rhythms. Atomic-scale origins of slowness in the cyanobacterial circadian clock.

Abe J, Hiyama TB, Mukaiyama A, Son S, Mori T, Saito S, Osako M, Wolanin J, Yamashita E, Kondo T, Akiyama S
Science 349 312-6 (2015)
Related entries: 4tl6, 4tl8, 4tl9, 4tla, 4tlb, 4tlc, 4tld, 4tle

Cited: 57 times
EuropePMC logo PMID: 26113637

Abstract

Circadian clocks generate slow and ordered cellular dynamics but consist of fast-moving bio-macromolecules; consequently, the origins of the overall slowness remain unclear. We identified the adenosine triphosphate (ATP) catalytic region [adenosine triphosphatase (ATPase)] in the amino-terminal half of the clock protein KaiC as the minimal pacemaker that controls the in vivo frequency of the cyanobacterial clock. Crystal structures of the ATPase revealed that the slowness of this ATPase arises from sequestration of a lytic water molecule in an unfavorable position and coupling of ATP hydrolysis to a peptide isomerization with high activation energy. The slow ATPase is coupled with another ATPase catalyzing autodephosphorylation in the carboxyl-terminal half of KaiC, yielding the circadian response frequency of intermolecular interactions with other clock-related proteins that influences the transcription and translation cycle.

Articles - 4tl7 mentioned but not cited (3)

  1. Conformational rearrangements of the C1 ring in KaiC measure the timing of assembly with KaiB. Mukaiyama A, Furuike Y, Abe J, Koda SI, Yamashita E, Kondo T, Akiyama S. Sci Rep 8 8803 (2018)
  2. Molecular dynamics simulations of nucleotide release from the circadian clock protein KaiC reveal atomic-resolution functional insights. Hong L, Vani BP, Thiede EH, Rust MJ, Dinner AR. Proc Natl Acad Sci U S A 115 E11475-E11484 (2018)
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Reviews citing this publication (16)

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  5. A thermodynamically consistent model of the post-translational Kai circadian clock. Paijmans J, Lubensky DK, Ten Wolde PR. PLoS Comput Biol 13 e1005415 (2017)
  6. Conversion between two conformational states of KaiC is induced by ATP hydrolysis as a trigger for cyanobacterial circadian oscillation. Oyama K, Azai C, Nakamura K, Tanaka S, Terauchi K. Sci Rep 6 32443 (2016)
  7. Revealing circadian mechanisms of integration and resilience by visualizing clock proteins working in real time. Mori T, Sugiyama S, Byrne M, Johnson CH, Uchihashi T, Ando T. Nat Commun 9 3245 (2018)
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  9. Tuning the circadian period of cyanobacteria up to 6.6 days by the single amino acid substitutions in KaiC. Ito-Miwa K, Furuike Y, Akiyama S, Kondo T. Proc Natl Acad Sci U S A 117 20926-20931 (2020)
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  11. Structural characterization of the circadian clock protein complex composed of KaiB and KaiC by inverse contrast-matching small-angle neutron scattering. Sugiyama M, Yagi H, Ishii K, Porcar L, Martel A, Oyama K, Noda M, Yunoki Y, Murakami R, Inoue R, Sato N, Oba Y, Terauchi K, Uchiyama S, Kato K. Sci Rep 6 35567 (2016)
  12. Damped circadian oscillation in the absence of KaiA in Synechococcus. Kawamoto N, Ito H, Tokuda IT, Iwasaki H. Nat Commun 11 2242 (2020)
  13. Effect of Multiple Clock Gene Ablations on the Circadian Period Length and Temperature Compensation in Mammalian Cells. Tsuchiya Y, Umemura Y, Minami Y, Koike N, Hosokawa T, Hara M, Ito H, Inokawa H, Yagita K. J Biol Rhythms 31 48-56 (2016)
  14. research-article Just-So Stories and Origin Myths: Phosphorylation and Structural Disorder in Circadian Clock Proteins. Dunlap JC, Loros JJ. Mol Cell 69 165-168 (2018)
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  16. Development and Optimization of Expression, Purification, and ATPase Assay of KaiC for Medium-Throughput Screening of Circadian Clock Mutants in Cyanobacteria. Ouyang D, Furuike Y, Mukaiyama A, Ito-Miwa K, Kondo T, Akiyama S. Int J Mol Sci 20 E2789 (2019)
  17. Role of ATP Hydrolysis in Cyanobacterial Circadian Oscillator. Das S, Terada TP, Sasai M. Sci Rep 7 17469 (2017)
  18. Mechanism of autonomous synchronization of the circadian KaiABC rhythm. Sasai M. Sci Rep 11 4713 (2021)
  19. CHRONO and DEC1/DEC2 compensate for lack of CRY1/CRY2 in expression of coherent circadian rhythm but not in generation of circadian oscillation in the neonatal mouse SCN. Ono D, Honma KI, Schmal C, Takumi T, Kawamoto T, Fujimoto K, Kato Y, Honma S. Sci Rep 11 19240 (2021)
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  21. Elucidation of master allostery essential for circadian clock oscillation in cyanobacteria. Furuike Y, Mukaiyama A, Ouyang D, Ito-Miwa K, Simon D, Yamashita E, Kondo T, Akiyama S. Sci Adv 8 eabm8990 (2022)
  22. Monitoring Protein-Protein Interactions in the Cyanobacterial Circadian Clock in Real Time via Electron Paramagnetic Resonance Spectroscopy. Chow GK, Chavan AG, Heisler JC, Chang YG, LiWang A, Britt RD. Biochemistry 59 2387-2400 (2020)
  23. Pressure accelerates the circadian clock of cyanobacteria. Kitahara R, Oyama K, Kawamura T, Mitsuhashi K, Kitazawa S, Yasunaga K, Sagara N, Fujimoto M, Terauchi K. Sci Rep 9 12395 (2019)
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  26. Letter Treasurer's comments on the financial position of the Biophysical Society of Japan. Akiyama S. Biophys Rev 12 209-211 (2020)
  27. Common Patterns of Hydrolysis Initiation in P-loop Fold Nucleoside Triphosphatases. Kozlova MI, Shalaeva DN, Dibrova DV, Mulkidjanian AY. Biomolecules 12 1345 (2022)
  28. KidA, a multi-PAS domain protein, tunes the period of the cyanobacterial circadian oscillator. Kim SJ, Chi C, Pattanayak G, Dinner AR, Rust MJ. Proc Natl Acad Sci U S A 119 e2202426119 (2022)
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  30. Role of the reaction-structure coupling in temperature compensation of the KaiABC circadian rhythm. Sasai M. PLoS Comput Biol 18 e1010494 (2022)
  31. Time from Semiosis: E-series Time for Living Systems. Nomura N, Muranaka T, Tomita J, Matsuno K. Biosemiotics 11 65-83 (2018)
  32. An Adenosine Triphosphate- Dependent 5'-3' DNA Helicase From sk1-Like Lactococcus lactis F13 Phage. Chmielewska-Jeznach M, Steczkiewicz K, Kobyłecki K, Bardowski JK, Szczepankowska AK. Front Microbiol 13 840219 (2022)
  33. Deficiency of circadian clock gene Bmal1 exacerbates noncanonical inflammasome-mediated pyroptosis and lethality via Rev-erbα-C/EBPβ-SAA1 axis. Shim DW, Eo JC, Kim S, Hwang I, Nam B, Shin JE, Han SH, Yu JW. Exp Mol Med 56 370-382 (2024)
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