Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver

Nov 11, 2015Proceedings of the National Academy of Sciences of the United States of America

Daily body clock and eating patterns differently influence rhythmic gene activity and protein production in mouse liver

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Abstract

Rhythmic transcription drives rhythmic mRNA accumulation and translation for a majority of genes.

Both circadian clock and feeding rhythms significantly impact rhythmic gene expression in mice.
Bmal1 deletion affects transcription and translation levels, indicating its role in regulating gene expression.
Translation efficiency of genes with 5'-Terminal Oligo Pyrimidine tract sequences is differentially regulated throughout the day.
Feeding rhythms primarily drive increased translation efficiency for 5'-TOP and TISU genes.
Bmal1 deletion alters the amplitude and phase of translation for TISU genes, suggesting complex interactions between transcription and translation processes.

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Diurnal oscillations of gene expression are a hallmark of rhythmic physiology across most living organisms. Such oscillations are controlled by the interplay between the circadian clock and feeding rhythms. Although rhythmic mRNA accumulation has been extensively studied, comparatively less is known about their transcription and translation. Here, we quantified simultaneously temporal transcription, accumulation, and translation of mouse liver mRNAs under physiological light-dark conditions and ad libitum or night-restricted feeding in WT and brain and muscle Arnt-like 1 (Bmal1)-deficient animals. We found that rhythmic transcription predominantly drives rhythmic mRNA accumulation and translation for a majority of genes. Comparison of wild-type and Bmal1 KO mice shows that circadian clock and feeding rhythms have broad impact on rhythmic gene expression, Bmal1 deletion affecting surprisingly both transcriptional and posttranscriptional levels. Translation efficiency is differentially regulated during the diurnal cycle for genes with 5'-Terminal Oligo Pyrimidine tract (5'-TOP) sequences and for genes involved in mitochondrial activity, many harboring a Translation Initiator of Short 5'-UTR (TISU) motif. The increased translation efficiency of 5'-TOP and TISU genes is mainly driven by feeding rhythms but Bmal1 deletion also affects amplitude and phase of translation, including TISU genes. Together this study emphasizes the complex interconnections between circadian and feeding rhythms at several steps ultimately determining rhythmic gene expression and translation.

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Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver

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