DNA Replication Is Required for Circadian Clock Function by Regulating Rhythmic Nucleosome Composition

Although the coupling between circadian and cell cycles allows circadian clocks to gate cell division and DNA replication in many organisms, circadian clocks were thought to function independently of cell cycle. Here, we show that DNA replication is required for circadian clock function in Neurospor...

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Bibliographic Details
Published in:Molecular cell 2017-07, Vol.67 (2), p.203-213.e4
Main Authors: Liu, Xiao, Dang, Yunkun, Matsu-ura, Toru, He, Yubo, He, Qun, Hong, Christian I., Liu, Yi
Format: Article
Language:English
Subjects:
Animals
cell cycle
circadian clock
Circadian Clocks
Circadian Rhythm
DNA Replication
DNA, Fungal - chemistry
DNA, Fungal - genetics
DNA, Fungal - metabolism
Fungal Proteins - genetics
Fungal Proteins - metabolism
Gene Expression Regulation, Fungal
High Mobility Group Proteins - genetics
High Mobility Group Proteins - metabolism
histone H2A.Z
Histones - genetics
Histones - metabolism
Neurospora - genetics
Neurospora - metabolism
Nucleic Acid Conformation
nucleosome composition
Nucleosomes - chemistry
Nucleosomes - genetics
Nucleosomes - metabolism
Proliferating Cell Nuclear Antigen - genetics
Proliferating Cell Nuclear Antigen - metabolism
Promoter Regions, Genetic
Protein Conformation
Structure-Activity Relationship
Time Factors
Transcription, Genetic
Transcriptional Elongation Factors - genetics
Transcriptional Elongation Factors - metabolism
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Summary:Although the coupling between circadian and cell cycles allows circadian clocks to gate cell division and DNA replication in many organisms, circadian clocks were thought to function independently of cell cycle. Here, we show that DNA replication is required for circadian clock function in Neurospora. Genetic and pharmacological inhibition of DNA replication abolished both overt and molecular rhythmicities by repressing frequency (frq) gene transcription. DNA replication is essential for the rhythmic changes of nucleosome composition at the frq promoter. The FACT complex, known to be involved in histone disassembly/reassembly, is required for clock function and is recruited to the frq promoter in a replication-dependent manner to promote replacement of histone H2A.Z by H2A. Finally, deletion of H2A.Z uncoupled the dependence of the circadian clock on DNA replication. Together, these results establish circadian clock and cell cycle as interdependent coupled oscillators and identify DNA replication as a critical process in the circadian mechanism. [Display omitted] •DNA replication is required for circadian clock function•DNA replication regulates the rhythmic changes of nucleosome composition•FACT mediates replacement of H2A.Z with H2A in a replication-dependent manner•Deletion of H2A.Z uncouples the dependence of circadian clock on DNA replication Liu et al. show that DNA replication is required for circadian clock function by regulating rhythmic nucleosome composition changes at the clock gene locus frq, establishing circadian clock and cell cycle as interdependent coupled oscillators.
ISSN:1097-2765
1097-4164
DOI:10.1016/j.molcel.2017.05.029