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Chromatin dynamics enable transcriptional rhythms in the cnidarian Nematostella vectensis


Autoři: Eviatar N. Weizman aff001;  Miriam Tannenbaum aff001;  Ann M. Tarrant aff002;  Ofir Hakim aff001;  Oren Levy aff001
Působiště autorů: The Mina & Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, Israel aff001;  Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, United States of America aff002
Vyšlo v časopise: Chromatin dynamics enable transcriptional rhythms in the cnidarian Nematostella vectensis. PLoS Genet 15(11): e32767. doi:10.1371/journal.pgen.1008397
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1008397

Souhrn

In animals, circadian rhythms are driven by oscillations in transcription, translation, and proteasomal degradation of highly conserved genes, resulting in diel cycles in the expression of numerous clock-regulated genes. Transcription is largely regulated through the binding of transcription factors to cis-regulatory elements within accessible regions of the chromatin. Chromatin remodeling is linked to circadian regulation in mammals, but it is unknown whether cycles in chromatin accessibility are a general feature of clock-regulated genes throughout evolution. To assess this, we applied an ATAC-seq approach using Nematostella vectensis, grown under two separate light regimes (light:dark (LD) and constant darkness (DD)). Based on previously identified N. vectensis circadian genes, our results show the coupling of chromatin accessibility and circadian transcription rhythmicity under LD conditions. Out of 180 known circadian genes, we were able to list 139 gene promoters that were highly accessible compared to common promoters. Furthermore, under LD conditions, we identified 259 active enhancers as opposed to 333 active enhancers under DD conditions, with 171 enhancers shared between the two treatments. The development of a highly reproducible ATAC-seq protocol integrated with published RNA-seq and ChIP-seq databases revealed the enrichment of transcription factor binding sites (such as C/EBP, homeobox, and MYB), which have not been previously associated with circadian signaling in cnidarians. These results provide new insight into the regulation of cnidarian circadian machinery. Broadly speaking, this supports the notion that the association between chromatin remodeling and circadian regulation arose early in animal evolution as reflected in this non-bilaterian lineage.

Klíčová slova:

Chromatin – Gene expression – Gene regulation – Sequence motif analysis – Genomic libraries – Circadian rhythms – Transcriptional control – Circadian oscillators


Zdroje

1. Golombek DA, Rosenstein RE. Physiology of circadian entrainment. Physiol Rev. 2010;90: 1063–1102. doi: 10.1152/physrev.00009.2009 20664079

2. Masri S, Sassone-Corsi P. Plasticity and specificity of the circadian epigenome. Nat Neurosci. 2010;13: 1324. doi: 10.1038/nn.2668 20975756

3. Doi M, Hirayama J, Sassone-Corsi P. Circadian regulator CLOCK is a histone acetyltransferase. Cell. 2006;125: 497–508. doi: 10.1016/j.cell.2006.03.033 16678094

4. Nakahata Y, Grimaldi B, Sahar S, Hirayama J, Sassone-Corsi P. Signaling to the circadian clock: plasticity by chromatin remodeling. Curr Opin Cell Biol. 2007;19: 230–237. doi: 10.1016/j.ceb.2007.02.016 17317138

5. Kwok RS, Lam VH, Chiu JC. Understanding the role of chromatin remodeling in the regulation of circadian transcription in Drosophila. Fly (Austin). 2015;9: 145–154. doi: 10.1080/19336934.2016.1143993 26926115

6. Hardin PE, Yu W. Circadian Transcription: Passing the HAT to CLOCK. Cell. 2006;125: 424–426. doi: 10.1016/j.cell.2006.04.010 16678086

7. Kwok RS, Li YH, Lei AJ, Edery I, Chiu JC. The Catalytic and Non-catalytic Functions of the Brahma Chromatin-Remodeling Protein Collaborate to Fine-Tune Circadian Transcription in Drosophila. PLOS Genet. 2015;11: e1005307. doi: 10.1371/journal.pgen.1005307 26132408

8. Tsompana M, Buck MJ. Chromatin accessibility: a window into the genome. Epigenetics Chromatin. 2014;7: 33. doi: 10.1186/1756-8935-7-33 25473421

9. Furey TS. ChIP-seq and Beyond: new and improved methodologies to detect and characterize protein-DNA interactions. Nat Rev Genet. 2012;13: 840–852. doi: 10.1038/nrg3306 23090257

10. Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods. 2013;10: 1213. doi: 10.1038/nmeth.2688 24097267

11. Hendricks WD, Byrum CA, Meyer-Bernstein EL. Characterization of Circadian Behavior in the Starlet Sea Anemone, Nematostella vectensis. PLOS ONE. 2012;7: e46843. doi: 10.1371/journal.pone.0046843 23056482

12. Reitzel AM, Behrendt L, Tarrant AM. Light Entrained Rhythmic Gene Expression in the Sea Anemone Nematostella vectensis: The Evolution of the Animal Circadian Clock. PLOS ONE. 2010;5: e12805. doi: 10.1371/journal.pone.0012805 20877728

13. Hand C, Uhlinger KR. The Culture, Sexual and Asexual Reproduction, and Growth of the Sea Anemone Nematostella vectensis. Biol Bull. 1992;182: 169–176. doi: 10.2307/1542110 29303672

14. Stefanik DJ, Friedman LE, Finnerty JR. Collecting, rearing, spawning and inducing regeneration of the starlet sea anemone, Nematostella vectensis. Nat Protoc. 2013;8: 916. doi: 10.1038/nprot.2013.044 23579780

15. Oren M, Tarrant AM, Alon S, Simon-Blecher N, Elbaz I, Appelbaum L, et al. Profiling molecular and behavioral circadian rhythms in the non-symbiotic sea anemone Nematostella vectensis. Sci Rep. 2015;5: 11418. doi: 10.1038/srep11418 26081482

16. Reitzel AM, Behrendt L, Tarrant AM. Light Entrained Rhythmic Gene Expression in the Sea Anemone Nematostella vectensis: The Evolution of the Animal Circadian Clock. PLOS ONE. 2010;5: e12805. doi: 10.1371/journal.pone.0012805 20877728

17. Reitzel AM, Tarrant AM, Levy O. Circadian Clocks in the Cnidaria: Environmental Entrainment, Molecular Regulation, and Organismal Outputs. Integr Comp Biol. 2013;53: 118–130. doi: 10.1093/icb/ict024 23620252

18. Reitzel AM, Tarrant AM, Levy O. Circadian Clocks in the Cnidaria: Environmental Entrainment, Molecular Regulation, and Organismal Outputs. Integr Comp Biol. 2013;53: 118–130. doi: 10.1093/icb/ict024 23620252

19. Buenrostro JD, Wu B, Chang HY, Greenleaf WJ. ATAC-seq: A Method for Assaying Chromatin Accessibility Genome-Wide. Curr Protoc Mol Biol. 2015;109: 21.29.1–9. doi: 10.1002/0471142727.mb2129s109 25559105

20. Birnbaumer L. G Proteins in Signal Transduction. Annu Rev Pharmacol Toxicol. 1990;30: 675–705. doi: 10.1146/annurev.pa.30.040190.003331 2111655

21. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38: 576–589. doi: 10.1016/j.molcel.2010.05.004 20513432

22. Rath MF, Rohde K, Klein DC, Møller M. Homeobox genes in the rodent pineal gland: roles in development and phenotype maintenance. Neurochem Res. 2013;38: 1100–1112. doi: 10.1007/s11064-012-0906-y 23076630

23. Rohde K, Møller M, Rath MF. Homeobox genes and melatonin synthesis: regulatory roles of the cone-rod homeobox transcription factor in the rodent pineal gland. BioMed Res Int. 2014;2014: 946075. doi: 10.1155/2014/946075 24877149

24. Nguyen NH, Lee H. MYB-related transcription factors function as regulators of the circadian clock and anthocyanin biosynthesis in Arabidopsis. Plant Signal Behav. 2016;11. doi: 10.1080/15592324.2016.1139278 26905954

25. Malt EA, Juhasz K, Malt UF, Naumann T. A Role for the Transcription Factor Nk2 Homeobox 1 in Schizophrenia: Convergent Evidence from Animal and Human Studies. Front Behav Neurosci. 2016;10. doi: 10.3389/fnbeh.2016.00059 27064909

26. Korenčič A, Košir R, Bordyugov G, Lehmann R, Rozman D, Herzel H. Timing of circadian genes in mammalian tissues. Sci Rep. 2014;4: 5782. doi: 10.1038/srep05782 25048020

27. Bozek K, Relógio A, Kielbasa SM, Heine M, Dame C, Kramer A, et al. Regulation of Clock-Controlled Genes in Mammals. PLOS ONE. 2009;4: e4882. doi: 10.1371/journal.pone.0004882 19287494

28. Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi AH, Tanaseichuk O, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019;10: 1523. doi: 10.1038/s41467-019-09234-6 30944313

29. Beckmann A, Özbek S. The nematocyst: a molecular map of the cnidarian stinging organelle. Int J Dev Biol. 2012;56: 577–582. doi: 10.1387/ijdb.113472ab 22689365

30. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature. 2011;470: 279–283. doi: 10.1038/nature09692 21160473

31. Nord AS, Blow MJ, Attanasio C, Akiyama JA, Holt A, Hosseini R, et al. Rapid and Pervasive Changes in Genome-Wide Enhancer Usage During Mammalian Development. Cell. 2013;155: 1521–1531. doi: 10.1016/j.cell.2013.11.033 24360275

32. Schwaiger M, Schönauer A, Rendeiro AF, Pribitzer C, Schauer A, Gilles AF, et al. Evolutionary conservation of the eumetazoan gene regulatory landscape. Genome Res. 2014;24: 639–650. doi: 10.1101/gr.162529.113 24642862

33. Vassilatis DK, Hohmann JG, Zeng H, Li F, Ranchalis JE, Mortrud MT, et al. The G protein-coupled receptor repertoires of human and mouse. Proc Natl Acad Sci U S A. 2003;100: 4903–4908. doi: 10.1073/pnas.0230374100 12679517

34. Müller WEG, Schröder HC, Pisignano D, Markl JS, Wang X. Metazoan Circadian Rhythm: Toward an Understanding of a Light-Based Zeitgeber in Sponges. Integr Comp Biol. 2013;53: 103–117. doi: 10.1093/icb/ict001 23474951

35. Koopman P, Schepers G, Brenner S, Venkatesh B. Origin and diversity of the Sox transcription factor gene family: genome-wide analysis in Fugu rubripes. Gene AmsterdamGene Amst. 2004;328: 177–186.

36. Feillet C, Horst VD, J GT, Levi F, Rand DA, Delaunay F. Coupling between the Circadian Clock and Cell Cycle Oscillators: Implication for Healthy Cells and Malignant Growth. Front Neurol. 2015;6. doi: 10.3389/fneur.2015.00096 26029155

37. Fu L, Kettner NM. The circadian clock in cancer development and therapy. Prog Mol Biol Transl Sci. 2013;119: 221–282. doi: 10.1016/B978-0-12-396971-2.00009-9 23899600

38. Hor CN, Yeung J, Jan M, Emmenegger Y, Hubbard J, Xenarios I, et al. Simple and complex interactions between sleep-wake driven and circadian processes shape daily genome regulatory dynamics in the mouse. bioRxiv. 2019; 677807. doi: 10.1101/677807

39. Fuentes-Pardo B, Inclán-Rubio V. Caudal photoreceptors synchronize the circadian rhythms in crayfish—I. Synchronization of ERG and locomotor circadian rhythms. Comp Biochem Physiol A Physiol. 1987;86: 523–527. doi: 10.1016/0300-9629(87)90536-6

40. Shlyueva D, Stampfel G, Stark A. Transcriptional enhancers: from properties to genome-wide predictions. Nat Rev Genet. 2014;15: 272–286. doi: 10.1038/nrg3682 24614317

41. Rabinowitz C, Moiseeva E, Rinkevich B. In vitro cultures of ectodermal monolayers from the model sea anemone Nematostella vectensis. Cell Tissue Res. 2016;366: 693–705. doi: 10.1007/s00441-016-2495-6 27623804

42. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9: 357–359. doi: 10.1038/nmeth.1923 22388286

43. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based Analysis of ChIP-Seq (MACS). Genome Biol. 2008;9: R137. doi: 10.1186/gb-2008-9-9-r137 18798982

44. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, et al. Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization. Science. 2007;317: 86–94. doi: 10.1126/science.1139158 17615350

45. Levy O, Kaniewska P, Alon S, Eisenberg E, Karako-Lampert S, Bay LK, et al. Complex diel cycles of gene expression in coral-algal symbiosis. Science. 2011;331: 175. doi: 10.1126/science.1196419 21233378

46. Barnett DW, Garrison EK, Quinlan AR, Strömberg MP, Marth GT. BamTools: a C++ API and toolkit for analyzing and managing BAM files. Bioinforma Oxf Engl. 2011;27: 1691–1692. doi: 10.1093/bioinformatics/btr174 21493652

47. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinforma Oxf Engl. 2010;26: 841–842. doi: 10.1093/bioinformatics/btq033 20110278

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