Oscillating and stable genome topologies underlie hepatic physiological rhythms during the circadian cycle


Autoři: Jérôme Mermet aff001;  Jake Yeung aff001;  Felix Naef aff001
Působiště autorů: The Institute of Bioengineering (IBI), School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland aff001
Vyšlo v časopise: Oscillating and stable genome topologies underlie hepatic physiological rhythms during the circadian cycle. PLoS Genet 17(2): e1009350. doi:10.1371/journal.pgen.1009350
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009350

Souhrn

The circadian clock drives extensive temporal gene expression programs controlling daily changes in behavior and physiology. In mouse liver, transcription factors dynamics, chromatin modifications, and RNA Polymerase II (PolII) activity oscillate throughout the 24-hour (24h) day, regulating the rhythmic synthesis of thousands of transcripts. Also, 24h rhythms in gene promoter-enhancer chromatin looping accompany rhythmic mRNA synthesis. However, how chromatin organization impinges on temporal transcription and liver physiology remains unclear. Here, we applied time-resolved chromosome conformation capture (4C-seq) in livers of WT and arrhythmic Bmal1 knockout mice. In WT, we observed 24h oscillations in promoter-enhancer loops at multiple loci including the core-clock genes Period1, Period2 and Bmal1. In addition, we detected rhythmic PolII activity, chromatin modifications and transcription involving stable chromatin loops at clock-output gene promoters representing key liver function such as glucose metabolism and detoxification. Intriguingly, these contacts persisted in clock-impaired mice in which both PolII activity and chromatin marks no longer oscillated. Finally, we observed chromatin interaction hubs connecting neighbouring genes showing coherent transcription regulation across genotypes. Thus, both clock-controlled and clock-independent chromatin topology underlie rhythmic regulation of liver physiology.

Klíčová slova:

Circadian oscillators – DNA transcription – Genetic oscillators – Genomic signal processing – Hypersensitivity – Chromatin – Mammalian genomics – Transcriptional control


Zdroje

1. Dibner C, Schibler U, Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annual review of physiology. 2010;72:517–49. doi: 10.1146/annurev-physiol-021909-135821 20148687

2. Nagoshi E, Saini C, Bauer C, Laroche T, Naef F, Schibler U. Circadian gene expression in individual fibroblasts: cell-autonomous and self-sustained oscillators pass time to daughter cells. Cell. 2004;119(5):693–705. doi: 10.1016/j.cell.2004.11.015 15550250

3. Takahashi JS. Transcriptional architecture of the mammalian circadian clock. Nature reviews Genetics. 2017;18(3):164–79. doi: 10.1038/nrg.2016.150 27990019

4. Zhang R, Lahens NF, Ballance HI, Hughes ME, Hogenesch JB. A circadian gene expression atlas in mammals: implications for biology and medicine. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(45):16219–24. doi: 10.1073/pnas.1408886111 25349387

5. Yeung J, Mermet J, Jouffe C, Marquis J, Charpagne A, Gachon F, et al. Transcription factor activity rhythms and tissue-specific chromatin interactions explain circadian gene expression across organs. Genome research. 2018;28(2):182–91. doi: 10.1101/gr.222430.117 29254942

6. Rey G, Cesbron F, Rougemont J, Reinke H, Brunner M, Naef F. Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLoS biology. 2011;9(2):e1000595. doi: 10.1371/journal.pbio.1000595 21364973

7. Koike N, Yoo SH, Huang HC, Kumar V, Lee C, Kim TK, et al. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science. 2012;338(6105):349–54. doi: 10.1126/science.1226339 22936566

8. Sobel JA, Krier I, Andersin T, Raghav S, Canella D, Gilardi F, et al. Transcriptional regulatory logic of the diurnal cycle in the mouse liver. PLoS biology. 2017;15(4):e2001069. doi: 10.1371/journal.pbio.2001069 28414715

9. Wang J, Symul L, Yeung J, Gobet C, Sobel J, Luck S, et al. Circadian clock-dependent and -independent posttranscriptional regulation underlies temporal mRNA accumulation in mouse liver. Proc Natl Acad Sci U S A. 2018;115(8):E1916–E25. doi: 10.1073/pnas.1715225115 29432155

10. Mermet J, Yeung J, Naef F. Systems Chronobiology: Global Analysis of Gene Regulation in a 24-Hour Periodic World. Cold Spring Harbor perspectives in biology. 2017;9(3).

11. Mauvoisin D, Atger F, Dayon L, Nunez Galindo A, Wang J, Martin E, et al. Circadian and Feeding Rhythms Orchestrate the Diurnal Liver Acetylome. Cell reports. 2017;20(7):1729–43. doi: 10.1016/j.celrep.2017.07.065 28813682

12. Wong DC, O'Neill JS. Non-transcriptional processes in circadian rhythm generation. Current opinion in physiology. 2018;5:117–32. doi: 10.1016/j.cophys.2018.10.003 30596188

13. Yeung J, Naef F. Rhythms of the Genome: Circadian Dynamics from Chromatin Topology, Tissue-Specific Gene Expression, to Behavior. Trends in genetics: TIG. 2018;34(12):915–26. doi: 10.1016/j.tig.2018.09.005 30309754

14. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326(5950):289–93. doi: 10.1126/science.1181369 19815776

15. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485(7398):376–80. doi: 10.1038/nature11082 22495300

16. Sanyal A, Lajoie BR, Jain G, Dekker J. The long-range interaction landscape of gene promoters. Nature. 2012;489(7414):109–13. doi: 10.1038/nature11279 22955621

17. Fulco CP, Munschauer M, Anyoha R, Munson G, Grossman SR, Perez EM, et al. Systematic mapping of functional enhancer-promoter connections with CRISPR interference. Science. 2016;354(6313):769–73. doi: 10.1126/science.aag2445 27708057

18. Vermunt MW, Zhang D, Blobel GA. The interdependence of gene-regulatory elements and the 3D genome. The Journal of cell biology. 2019;218(1):12–26. doi: 10.1083/jcb.201809040 30442643

19. Aguilar-Arnal L, Hakim O, Patel VR, Baldi P, Hager GL, Sassone-Corsi P. Cycles in spatial and temporal chromosomal organization driven by the circadian clock. Nature structural & molecular biology. 2013;20(10):1206–13. doi: 10.1038/nsmb.2667 24056944

20. Zhao H, Sifakis EG, Sumida N, Millan-Arino L, Scholz BA, Svensson JP, et al. PARP1- and CTCF-Mediated Interactions between Active and Repressed Chromatin at the Lamina Promote Oscillating Transcription. Molecular cell. 2015;59(6):984–97. doi: 10.1016/j.molcel.2015.07.019 26321255

21. Brunet A, Forsberg F, Fan Q, Saether T, Collas P. Nuclear Lamin B1 Interactions With Chromatin During the Circadian Cycle Are Uncoupled From Periodic Gene Expression. Front Genet. 2019;10:917. doi: 10.3389/fgene.2019.00917 31632442

22. Kim YH, Marhon SA, Zhang Y, Steger DJ, Won KJ, Lazar MA. Rev-erbalpha dynamically modulates chromatin looping to control circadian gene transcription. Science. 2018;359(6381):1274–7. doi: 10.1126/science.aao6891 29439026

23. Mermet J, Yeung J, Hurni C, Mauvoisin D, Gustafson K, Jouffe C, et al. Clock-dependent chromatin topology modulates circadian transcription and behavior. Genes & development. 2018;32(5-6):347–58. doi: 10.1101/gad.312397.118 29572261

24. Beytebiere JR, Trott AJ, Greenwell BJ, Osborne CA, Vitet H, Spence J, et al. Tissue-specific BMAL1 cistromes reveal that rhythmic transcription is associated with rhythmic enhancer-enhancer interactions. Genes & development. 2019;33(5-6):294–309. doi: 10.1101/gad.322198.118 30804225

25. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, et al. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nature genetics. 2006;38(11):1348–54. doi: 10.1038/ng1896 17033623

26. Le Martelot G, Canella D, Symul L, Migliavacca E, Gilardi F, Liechti R, et al. Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. PLoS biology. 2012;10(11):e1001442. doi: 10.1371/journal.pbio.1001442 23209382

27. Gachon F, Olela FF, Schaad O, Descombes P, Schibler U. The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell metabolism. 2006;4(1):25–36. doi: 10.1016/j.cmet.2006.04.015 16814730

28. Lamia KA, Storch KF, Weitz CJ. Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci U S A. 2008;105(39):15172–7. doi: 10.1073/pnas.0806717105 18779586

29. Aviram R, Manella G, Kopelman N, Neufeld-Cohen A, Zwighaft Z, Elimelech M, et al. Lipidomics Analyses Reveal Temporal and Spatial Lipid Organization and Uncover Daily Oscillations in Intracellular Organelles. Molecular cell. 2016;62(4):636–48. doi: 10.1016/j.molcel.2016.04.002 27161994

30. Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P. Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science. 2009;324(5927):654–7. doi: 10.1126/science.1170803 19286518

31. Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, et al. Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science. 2009;324(5927):651–4. doi: 10.1126/science.1171641 19299583

32. Peek CB, Affinati AH, Ramsey KM, Kuo HY, Yu W, Sena LA, et al. Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science. 2013;342(6158):1243417. doi: 10.1126/science.1243417 24051248

33. Zhang Y, Fang B, Emmett MJ, Damle M, Sun Z, Feng D, et al. GENE REGULATION. Discrete functions of nuclear receptor Rev-erbalpha couple metabolism to the clock. Science. 2015;348(6242):1488–92. doi: 10.1126/science.aab3021 26044300

34. Ghavi-Helm Y, Klein FA, Pakozdi T, Ciglar L, Noordermeer D, Huber W, et al. Enhancer loops appear stable during development and are associated with paused polymerase. Nature. 2014;512(7512):96–100. doi: 10.1038/nature13417 25043061

35. Hakim O, Sung MH, Voss TC, Splinter E, John S, Sabo PJ, et al. Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome research. 2011;21(5):697–706. doi: 10.1101/gr.111153.110 21471403

36. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, et al. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nature genetics. 2010;42(1):53–61. doi: 10.1038/ng.496 20010836

37. Sexton T, Kurukuti S, Mitchell JA, Umlauf D, Nagano T, Fraser P. Sensitive detection of chromatin coassociations using enhanced chromosome conformation capture on chip. Nature protocols. 2012;7(7):1335–50. doi: 10.1038/nprot.2012.071 22722369

38. Johnson BP, Walisser JA, Liu Y, Shen AL, McDearmon EL, Moran SM, et al. Hepatocyte circadian clock controls acetaminophen bioactivation through NADPH-cytochrome P450 oxidoreductase. Proc Natl Acad Sci U S A. 2014;111(52):18757–62. doi: 10.1073/pnas.1421708111 25512522

39. Consortium EP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489(7414):57–74. doi: 10.1038/nature11247 22955616

40. Vietri Rudan M, Barrington C, Henderson S, Ernst C, Odom Duncan T, Tanay A, et al. Comparative Hi-C Reveals that CTCF Underlies Evolution of Chromosomal Domain Architecture. Cell reports. 2015;10(8):1297–309. doi: 10.1016/j.celrep.2015.02.004 25732821

41. Ando-Kuri M, Arzate-Mejía RG, Morf J, Cairns J, Poot-Hernández CA, Andrews S, et al. 2020.

42. Lee YJ, Han DH, Pak YK, Cho SH. Circadian regulation of low density lipoprotein receptor promoter activity by CLOCK/BMAL1, Hes1 and Hes6. Exp Mol Med. 2012;44(11):642–52. doi: 10.3858/emm.2012.44.11.073 22913986

43. Xu Y, Guo W, Li P, Zhang Y, Zhao M, Fan Z, et al. Long-Range Chromosome Interactions Mediated by Cohesin Shape Circadian Gene Expression. PLoS genetics. 2016;12(5):e1005992. doi: 10.1371/journal.pgen.1005992 27135601

44. Nicolas D, Phillips NE, Naef F. What shapes eukaryotic transcriptional bursting? Molecular bioSystems. 2017;13(7):1280–90. doi: 10.1039/c7mb00154a 28573295

45. Bartman CR, Hsu SC, Hsiung CC, Raj A, Blobel GA. Enhancer Regulation of Transcriptional Bursting Parameters Revealed by Forced Chromatin Looping. Molecular cell. 2016;62(2):237–47. doi: 10.1016/j.molcel.2016.03.007 27067601

46. David FP, Delafontaine J, Carat S, Ross FJ, Lefebvre G, Jarosz Y, et al. HTSstation: a web application and open-access libraries for high-throughput sequencing data analysis. PLoS One. 2014;9(1):e85879. doi: 10.1371/journal.pone.0085879 24475057

47. Atger F, Gobet C, Marquis J, Martin E, Wang J, Weger B, et al. 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. doi: 10.1073/pnas.1515308112 26554015

48. Zhang Y, Fang B, Emmett MJ, Damle M, Sun Z, Feng D, et al. Discrete functions of nuclear receptor Rev-erb couple metabolism to the clock. Science. 2015;348(6242):1488–92. doi: 10.1126/science.aab3021 26044300


Článek vyšel v časopise

PLOS Genetics


2021 Číslo 2
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Důležitost adherence při depresivním onemocnění
nový kurz
Autoři: MUDr. Eliška Bartečková, Ph.D.

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková, Ph.D.

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se