Clock-dependent Chromatin Topology Modulates Circadian Transcription and Behavior

Overview

Journal Genes Dev

Specialty Molecular Biology

Date 2018 Mar 25

PMID 29572261

Citations 58

Authors

Jerome Mermet

Jake Yeung

Clemence Hurni

Daniel Mauvoisin

Kyle Gustafson

Celine Jouffe

Damien Nicolas

Yann Emmenegger

Cedric Gobet

Paul Franken

Frederic Gachon

Felix Naef

Affiliations

Soon will be listed here.

Abstract

The circadian clock in animals orchestrates widespread oscillatory gene expression programs, which underlie 24-h rhythms in behavior and physiology. Several studies have shown the possible roles of transcription factors and chromatin marks in controlling cyclic gene expression. However, how daily active enhancers modulate rhythmic gene transcription in mammalian tissues is not known. Using circular chromosome conformation capture (4C) combined with sequencing (4C-seq), we discovered oscillatory promoter-enhancer interactions along the 24-h cycle in the mouse liver and kidney. Rhythms in chromatin interactions were abolished in arrhythmic knockout mice. Deleting a contacted intronic enhancer element in the () gene was sufficient to compromise the rhythmic chromatin contacts in tissues. Moreover, the deletion reduced the daily dynamics of transcriptional burst frequency and, remarkably, shortened the circadian period of locomotor activity rhythms. Our results establish oscillating and clock-controlled promoter-enhancer looping as a regulatory layer underlying circadian transcription and behavior.

Citing Articles

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Clock-dependent chromatin accessibility rhythms regulate circadian transcription.

Yuan Y, Chen Q, Brovkina M, Clowney E, Yadlapalli S PLoS Genet. 2024; 20(5):e1011278.

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Enhancer-promoter interactions become more instructive in the transition from cell-fate specification to tissue differentiation.

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References

Bray N, Pimentel H, Melsted P, Pachter L . Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol. 2016; 34(5):525-7. DOI: 10.1038/nbt.3519. View

Noordermeer D, Leleu M, Schorderet P, Joye E, Chabaud F, Duboule D . Temporal dynamics and developmental memory of 3D chromatin architecture at Hox gene loci. Elife. 2014; 3:e02557. PMC: 4017647. DOI: 10.7554/eLife.02557. View

Gheldof N, Leleu M, Noordermeer D, Rougemont J, Reymond A . Detecting long-range chromatin interactions using the chromosome conformation capture sequencing (4C-seq) method. Methods Mol Biol. 2011; 786:211-25. DOI: 10.1007/978-1-61779-292-2_13. View

DeBruyne J, Noton E, Lambert C, Maywood E, Weaver D, Reppert S . A clock shock: mouse CLOCK is not required for circadian oscillator function. Neuron. 2006; 50(3):465-77. DOI: 10.1016/j.neuron.2006.03.041. View

Kim Y, Marhon S, Zhang Y, Steger D, Won K, Lazar M . Rev-erbα dynamically modulates chromatin looping to control circadian gene transcription. Science. 2018; 359(6381):1274-1277. PMC: 5995144. DOI: 10.1126/science.aao6891. View

Takahashi J . Transcriptional architecture of the mammalian circadian clock. Nat Rev Genet. 2016; 18(3):164-179. PMC: 5501165. DOI: 10.1038/nrg.2016.150. View

Zhang Y, Fang B, Emmett M, Damle M, Sun Z, Feng D . GENE REGULATION. Discrete functions of nuclear receptor Rev-erbα couple metabolism to the clock. Science. 2015; 348(6242):1488-92. PMC: 4613749. DOI: 10.1126/science.aab3021. View

Atger F, Gobet C, Marquis J, Martin E, Wang J, Weger B . Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver. Proc Natl Acad Sci U S A. 2015; 112(47):E6579-88. PMC: 4664316. DOI: 10.1073/pnas.1515308112. View

Fukaya T, Lim B, Levine M . Enhancer Control of Transcriptional Bursting. Cell. 2016; 166(2):358-368. PMC: 4970759. DOI: 10.1016/j.cell.2016.05.025. View

10.

Jouffe C, Cretenet G, Symul L, Martin E, Atger F, Naef F . The circadian clock coordinates ribosome biogenesis. PLoS Biol. 2013; 11(1):e1001455. PMC: 3536797. DOI: 10.1371/journal.pbio.1001455. View

11.

Sanborn A, Rao S, Huang S, Durand N, Huntley M, Jewett A . Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc Natl Acad Sci U S A. 2015; 112(47):E6456-65. PMC: 4664323. DOI: 10.1073/pnas.1518552112. View

12.

Irimia J, Meyer C, Peper C, Zhai L, Bock C, Previs S . Impaired glucose tolerance and predisposition to the fasted state in liver glycogen synthase knock-out mice. J Biol Chem. 2010; 285(17):12851-61. PMC: 2857087. DOI: 10.1074/jbc.M110.106534. View

13.

Sanyal A, Lajoie B, Jain G, Dekker J . The long-range interaction landscape of gene promoters. Nature. 2012; 489(7414):109-13. PMC: 3555147. DOI: 10.1038/nature11279. View

14.

Zhang R, Lahens N, Ballance H, Hughes M, Hogenesch J . A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci U S A. 2014; 111(45):16219-24. PMC: 4234565. DOI: 10.1073/pnas.1408886111. View

15.

Kuznetsova T, Wang S, Rao N, Mandoli A, Martens J, Rother N . Glucocorticoid receptor and nuclear factor kappa-b affect three-dimensional chromatin organization. Genome Biol. 2015; 16:264. PMC: 4665721. DOI: 10.1186/s13059-015-0832-9. View

16.

Bahar Halpern K, Tanami S, Landen S, Chapal M, Szlak L, Hutzler A . Bursty gene expression in the intact mammalian liver. Mol Cell. 2015; 58(1):147-56. PMC: 4500162. DOI: 10.1016/j.molcel.2015.01.027. View

17.

Palstra R, Tolhuis B, Splinter E, Nijmeijer R, Grosveld F, de Laat W . The beta-globin nuclear compartment in development and erythroid differentiation. Nat Genet. 2003; 35(2):190-4. DOI: 10.1038/ng1244. View

18.

Ghavi-Helm Y, Klein F, Pakozdi T, Ciglar L, Noordermeer D, Huber W . Enhancer loops appear stable during development and are associated with paused polymerase. Nature. 2014; 512(7512):96-100. DOI: 10.1038/nature13417. View

19.

Toh K, Jones C, He Y, Eide E, Hinz W, Virshup D . An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science. 2001; 291(5506):1040-3. DOI: 10.1126/science.1057499. View

20.

Cermakian N, Monaco L, Pando M, Dierich A, Sassone-Corsi P . Altered behavioral rhythms and clock gene expression in mice with a targeted mutation in the Period1 gene. EMBO J. 2001; 20(15):3967-74. PMC: 149149. DOI: 10.1093/emboj/20.15.3967. View