Coupling allows robust mammalian redox circadian rhythms despite heterogeneity and noise

Circadian clocks are endogenous oscillators present in almost all cells that drive daily rhythms in physiology and behavior. There are two mechanisms that have been proposed to explain how circadian rhythms are generated in mammalian cells: through a transcription-translation feedback loop (TTFL) an...

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Main Authors: Marta del Olmo, Anton Kalashnikov, Christoph Schmal, Achim Kramer, Hanspeter Herzel
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:Heliyon
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2405844024008041
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author Marta del Olmo
Anton Kalashnikov
Christoph Schmal
Achim Kramer
Hanspeter Herzel
author_facet Marta del Olmo
Anton Kalashnikov
Christoph Schmal
Achim Kramer
Hanspeter Herzel
author_sort Marta del Olmo
collection DOAJ
description Circadian clocks are endogenous oscillators present in almost all cells that drive daily rhythms in physiology and behavior. There are two mechanisms that have been proposed to explain how circadian rhythms are generated in mammalian cells: through a transcription-translation feedback loop (TTFL) and based on oxidation/reduction reactions, both of which are intrinsically stochastic and heterogeneous at the single cell level. In order to explore the emerging properties of stochastic and heterogeneous redox oscillators, we simplify a recently developed kinetic model of redox oscillations to an amplitude-phase oscillator with ‘twist’ (period-amplitude correlation) and subject to Gaussian noise. We show that noise and heterogeneity alone lead to fast desynchronization, and that coupling between noisy oscillators can establish robust and synchronized rhythms with amplitude expansions and tuning of the period due to twist. Coupling a network of redox oscillators to a simple model of the TTFL also contributes to synchronization, large amplitudes and fine-tuning of the period for appropriate interaction strengths. These results provide insights into how the circadian clock compensates randomness from intracellular sources and highlight the importance of noise, heterogeneity and coupling in the context of circadian oscillators.
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spelling doaj.art-7d8ad7d68c1b446f8601106d309ce5672024-02-03T06:38:26ZengElsevierHeliyon2405-84402024-01-01102e24773Coupling allows robust mammalian redox circadian rhythms despite heterogeneity and noiseMarta del Olmo0Anton Kalashnikov1Christoph Schmal2Achim Kramer3Hanspeter Herzel4Institute for Theoretical Biology – Humboldt Universität zu Berlin and Charité Universitätsmedizin Berlin, Philippstraße 13, 10115 Berlin, Germany; Corresponding author.Institute for Theoretical Biology – Humboldt Universität zu Berlin and Charité Universitätsmedizin Berlin, Philippstraße 13, 10115 Berlin, GermanyInstitute for Theoretical Biology – Humboldt Universität zu Berlin and Charité Universitätsmedizin Berlin, Philippstraße 13, 10115 Berlin, GermanyInstitute for Medical Immunology – Laboratory of Chronobiology, Charité Universitätsmedizin Berlin, Charitéplatz 1, 10117 Berlin, GermanyInstitute for Theoretical Biology – Humboldt Universität zu Berlin and Charité Universitätsmedizin Berlin, Philippstraße 13, 10115 Berlin, GermanyCircadian clocks are endogenous oscillators present in almost all cells that drive daily rhythms in physiology and behavior. There are two mechanisms that have been proposed to explain how circadian rhythms are generated in mammalian cells: through a transcription-translation feedback loop (TTFL) and based on oxidation/reduction reactions, both of which are intrinsically stochastic and heterogeneous at the single cell level. In order to explore the emerging properties of stochastic and heterogeneous redox oscillators, we simplify a recently developed kinetic model of redox oscillations to an amplitude-phase oscillator with ‘twist’ (period-amplitude correlation) and subject to Gaussian noise. We show that noise and heterogeneity alone lead to fast desynchronization, and that coupling between noisy oscillators can establish robust and synchronized rhythms with amplitude expansions and tuning of the period due to twist. Coupling a network of redox oscillators to a simple model of the TTFL also contributes to synchronization, large amplitudes and fine-tuning of the period for appropriate interaction strengths. These results provide insights into how the circadian clock compensates randomness from intracellular sources and highlight the importance of noise, heterogeneity and coupling in the context of circadian oscillators.http://www.sciencedirect.com/science/article/pii/S2405844024008041Circadian clocksRedoxModelingNoiseHeterogeneity
spellingShingle Marta del Olmo
Anton Kalashnikov
Christoph Schmal
Achim Kramer
Hanspeter Herzel
Coupling allows robust mammalian redox circadian rhythms despite heterogeneity and noise
Heliyon
Circadian clocks
Redox
Modeling
Noise
Heterogeneity
title Coupling allows robust mammalian redox circadian rhythms despite heterogeneity and noise
title_full Coupling allows robust mammalian redox circadian rhythms despite heterogeneity and noise
title_fullStr Coupling allows robust mammalian redox circadian rhythms despite heterogeneity and noise
title_full_unstemmed Coupling allows robust mammalian redox circadian rhythms despite heterogeneity and noise
title_short Coupling allows robust mammalian redox circadian rhythms despite heterogeneity and noise
title_sort coupling allows robust mammalian redox circadian rhythms despite heterogeneity and noise
topic Circadian clocks
Redox
Modeling
Noise
Heterogeneity
url http://www.sciencedirect.com/science/article/pii/S2405844024008041
work_keys_str_mv AT martadelolmo couplingallowsrobustmammalianredoxcircadianrhythmsdespiteheterogeneityandnoise
AT antonkalashnikov couplingallowsrobustmammalianredoxcircadianrhythmsdespiteheterogeneityandnoise
AT christophschmal couplingallowsrobustmammalianredoxcircadianrhythmsdespiteheterogeneityandnoise
AT achimkramer couplingallowsrobustmammalianredoxcircadianrhythmsdespiteheterogeneityandnoise
AT hanspeterherzel couplingallowsrobustmammalianredoxcircadianrhythmsdespiteheterogeneityandnoise