A Model for the Circadian Rhythm of Cyanobacteria That Maintains Oscillation Without Gene Expression

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2006 Jun 27

PMID 16798799

Citations 23

Authors

Gen Kurosawa

Kazuyuki Aihara

Yoh Iwasa

Affiliations

Soon will be listed here.

Abstract

An intriguing property of the cyanobacterial circadian clock is that endogenous rhythm persists when protein abundances are kept constant either in the presence of translation and transcription inhibitors or in the constant dark condition. Here we propose a regulatory mechanism of KaiC phosphorylation for the generation of circadian oscillations in cyanobacteria. In the model, clock proteins KaiA and KaiB are assumed to have multiple states, regulating the KaiC phosphorylation process. The model can explain 1), the sustained oscillation of gene expression and protein abundance when the expression of the kaiBC gene is regulated by KaiC protein, and 2), the sustained oscillation of phosphorylated KaiC when transcription and translation processes are inhibited and total protein abundance is fixed. Results of this work suggest that KaiA and KaiB strengthen the nonlinearity of KaiC phosphorylation, thereby promoting the circadian rhythm in cyanobacteria.

Citing Articles

A computational model of mutual antagonism in the mechano-signaling network of RhoA and nitric oxide.

Surendran A, Dewey Jr C, Low B, Tucker-Kellogg L BMC Mol Cell Biol. 2021; 22(Suppl 1):47.

PMID: 34635055 PMC: 8507106. DOI: 10.1186/s12860-021-00383-5.

Transition of Neural Activity From the Chaotic Bipolar-Disorder State to the Periodic Healthy State Using External Feedback Signals.

Doho H, Nobukawa S, Nishimura H, Wagatsuma N, Takahashi T Front Comput Neurosci. 2020; 14:76.

PMID: 32982709 PMC: 7484049. DOI: 10.3389/fncom.2020.00076.

Weak coupling between intracellular feedback loops explains dissociation of clock gene dynamics.

Schmal C, Ono D, Myung J, Pett J, Honma S, Honma K PLoS Comput Biol. 2019; 15(9):e1007330.

PMID: 31513579 PMC: 6759184. DOI: 10.1371/journal.pcbi.1007330.

Heat the Clock: Entrainment and Compensation in Circadian Rhythms.

Avello P, Davis S, Ronald J, Pitchford J J Circadian Rhythms. 2019; 17:5.

PMID: 31139231 PMC: 6524549. DOI: 10.5334/jcr.179.

Non-sinusoidal Waveform in Temperature-Compensated Circadian Oscillations.

Gibo S, Kurosawa G Biophys J. 2019; 116(4):741-751.

PMID: 30712786 PMC: 6383000. DOI: 10.1016/j.bpj.2018.12.022.

References

Leloup J, Gonze D, Goldbeter A . Limit cycle models for circadian rhythms based on transcriptional regulation in Drosophila and Neurospora. J Biol Rhythms. 2000; 14(6):433-48. DOI: 10.1177/074873099129000948. View

Nakajima M, Imai K, Ito H, Nishiwaki T, Murayama Y, Iwasaki H . Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science. 2005; 308(5720):414-5. DOI: 10.1126/science.1108451. View

Xu Y, Mori T, Johnson C . Circadian clock-protein expression in cyanobacteria: rhythms and phase setting. EMBO J. 2000; 19(13):3349-57. PMC: 313937. DOI: 10.1093/emboj/19.13.3349. View

Ueda H, Hagiwara M, Kitano H . Robust oscillations within the interlocked feedback model of Drosophila circadian rhythm. J Theor Biol. 2001; 210(4):401-6. DOI: 10.1006/jtbi.2000.2226. View

YOUNG M, Kay S . Time zones: a comparative genetics of circadian clocks. Nat Rev Genet. 2001; 2(9):702-15. DOI: 10.1038/35088576. View

Kurosawa G, Mochizuki A, Iwasa Y . Comparative study of circadian clock models, in search of processes promoting oscillation. J Theor Biol. 2002; 216(2):193-208. DOI: 10.1006/jtbi.2002.2546. View

Smolen P, Baxter D, Byrne J . A reduced model clarifies the role of feedback loops and time delays in the Drosophila circadian oscillator. Biophys J. 2002; 83(5):2349-59. PMC: 1302324. DOI: 10.1016/S0006-3495(02)75249-1. View

Iwasaki H, Nishiwaki T, Kitayama Y, Nakajima M, Kondo T . KaiA-stimulated KaiC phosphorylation in circadian timing loops in cyanobacteria. Proc Natl Acad Sci U S A. 2002; 99(24):15788-93. PMC: 137794. DOI: 10.1073/pnas.222467299. View

Williams S, Vakonakis I, Golden S, LiWang A . Structure and function from the circadian clock protein KaiA of Synechococcus elongatus: a potential clock input mechanism. Proc Natl Acad Sci U S A. 2002; 99(24):15357-62. PMC: 137721. DOI: 10.1073/pnas.232517099. View

10.

Kurosawa G, Iwasa Y . Saturation of enzyme kinetics in circadian clock models. J Biol Rhythms. 2002; 17(6):568-77. DOI: 10.1177/0748730402238239. View

11.

Kageyama H, Kondo T, Iwasaki H . Circadian formation of clock protein complexes by KaiA, KaiB, KaiC, and SasA in cyanobacteria. J Biol Chem. 2002; 278(4):2388-95. DOI: 10.1074/jbc.M208899200. View

12.

Xu Y, Mori T, Johnson C . Cyanobacterial circadian clockwork: roles of KaiA, KaiB and the kaiBC promoter in regulating KaiC. EMBO J. 2003; 22(9):2117-26. PMC: 156062. DOI: 10.1093/emboj/cdg168. View

13.

Kitayama Y, Iwasaki H, Nishiwaki T, Kondo T . KaiB functions as an attenuator of KaiC phosphorylation in the cyanobacterial circadian clock system. EMBO J. 2003; 22(9):2127-34. PMC: 156084. DOI: 10.1093/emboj/cdg212. View

14.

Leloup J, Goldbeter A . Toward a detailed computational model for the mammalian circadian clock. Proc Natl Acad Sci U S A. 2003; 100(12):7051-6. PMC: 165828. DOI: 10.1073/pnas.1132112100. View

15.

Forger D, Peskin C . A detailed predictive model of the mammalian circadian clock. Proc Natl Acad Sci U S A. 2003; 100(25):14806-11. PMC: 299807. DOI: 10.1073/pnas.2036281100. View

16.

Stelling J, Gilles E, Doyle 3rd F . Robustness properties of circadian clock architectures. Proc Natl Acad Sci U S A. 2004; 101(36):13210-5. PMC: 516549. DOI: 10.1073/pnas.0401463101. View

17.

Nishiwaki T, Satomi Y, Nakajima M, Lee C, Kiyohara R, Kageyama H . Role of KaiC phosphorylation in the circadian clock system of Synechococcus elongatus PCC 7942. Proc Natl Acad Sci U S A. 2004; 101(38):13927-32. PMC: 518855. DOI: 10.1073/pnas.0403906101. View

18.

Goodwin B . Oscillatory behavior in enzymatic control processes. Adv Enzyme Regul. 1965; 3:425-38. DOI: 10.1016/0065-2571(65)90067-1. View

19.

Griffith J . Mathematics of cellular control processes. I. Negative feedback to one gene. J Theor Biol. 1968; 20(2):202-8. DOI: 10.1016/0022-5193(68)90189-6. View

20.

Doolittle W . The cyanobacterial genome, its expression, and the control of that expression. Adv Microb Physiol. 1979; 20:1-102. DOI: 10.1016/s0065-2911(08)60206-4. View