Canonical Nucleosome Organization at Promoters Forms During Genome Activation

Overview

Journal Genome Res

Specialty Genetics

Date 2013 Nov 29

PMID 24285721

Citations 55

Authors

Yong Zhang

Nadine L Vastenhouw

Jianxing Feng

Kai Fu

Chenfei Wang

Ying Ge

Andrea Pauli

Paul Van Hummelen

Alexander F Schier

X Shirley Liu

Affiliations

Soon will be listed here.

Abstract

The organization of nucleosomes influences transcriptional activity by controlling accessibility of DNA binding proteins to the genome. Genome-wide nucleosome binding profiles have identified a canonical nucleosome organization at gene promoters, where arrays of well-positioned nucleosomes emanate from nucleosome-depleted regions. The mechanisms of formation and the function of canonical promoter nucleosome organization remain unclear. Here we analyze the genome-wide location of nucleosomes during zebrafish embryogenesis and show that well-positioned nucleosome arrays appear on thousands of promoters during the activation of the zygotic genome. The formation of canonical promoter nucleosome organization is independent of DNA sequence preference, transcriptional elongation, and robust RNA polymerase II (Pol II) binding. Instead, canonical promoter nucleosome organization correlates with the presence of histone H3 lysine 4 trimethylation (H3K4me3) and affects future transcriptional activation. These findings reveal that genome activation is central to the organization of nucleosome arrays during early embryogenesis.

Citing Articles

Screening of functional maternal-specific chromatin regulators in early embryonic development of zebrafish.

Wang Y, Wang X, Wang W, Cao Z, Zhang Y, Liu G Commun Biol. 2024; 7(1):1354.

PMID: 39427068 PMC: 11490497. DOI: 10.1038/s42003-024-06983-z.

H3K4me2 distinguishes a distinct class of enhancers during the maternal-to-zygotic transition.

Hurton M, Miller J, Lee M bioRxiv. 2024; .

PMID: 39253505 PMC: 11383010. DOI: 10.1101/2024.08.26.609713.

Local nuclear to cytoplasmic ratio regulates H3.3 incorporation via cell cycle state during zygotic genome activation.

Bhatt A, Brown M, Wackford A, Shindo Y, Amodeo A bioRxiv. 2024; .

PMID: 39071352 PMC: 11275841. DOI: 10.1101/2024.07.15.603602.

Chromatin conformation and histone modification profiling across human kidney anatomic regions.

Li H, Li D, Humphreys B Sci Data. 2024; 11(1):797.

PMID: 39025878 PMC: 11258246. DOI: 10.1038/s41597-024-03648-8.

The developmental and evolutionary characteristics of transcription factor binding site clustered regions based on an explainable machine learning model.

Ouyang Z, Liu F, Li W, Wang J, Chen B, Zheng Y Nucleic Acids Res. 2024; 52(13):7610-7626.

PMID: 38813828 PMC: 11260490. DOI: 10.1093/nar/gkae441.

References

Schier A . The maternal-zygotic transition: death and birth of RNAs. Science. 2007; 316(5823):406-7. DOI: 10.1126/science.1140693. View

Radman-Livaja M, Rando O . Nucleosome positioning: how is it established, and why does it matter?. Dev Biol. 2009; 339(2):258-66. PMC: 2830277. DOI: 10.1016/j.ydbio.2009.06.012. View

Pauli A, Valen E, Lin M, Garber M, Vastenhouw N, Levin J . Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res. 2011; 22(3):577-91. PMC: 3290793. DOI: 10.1101/gr.133009.111. View

Bernstein B, Mikkelsen T, Xie X, Kamal M, Huebert D, Cuff J . A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006; 125(2):315-26. DOI: 10.1016/j.cell.2006.02.041. View

Yuan G, Liu Y, Dion M, Slack M, Wu L, Altschuler S . Genome-scale identification of nucleosome positions in S. cerevisiae. Science. 2005; 309(5734):626-30. DOI: 10.1126/science.1112178. View

Stein A, Takasuka T, Collings C . Are nucleosome positions in vivo primarily determined by histone-DNA sequence preferences?. Nucleic Acids Res. 2009; 38(3):709-19. PMC: 2817465. DOI: 10.1093/nar/gkp1043. View

Hu G, Schones D, Cui K, Ybarra R, Northrup D, Tang Q . Regulation of nucleosome landscape and transcription factor targeting at tissue-specific enhancers by BRG1. Genome Res. 2011; 21(10):1650-8. PMC: 3202282. DOI: 10.1101/gr.121145.111. View

Zhang Y, Moqtaderi Z, Rattner B, Euskirchen G, Snyder M, Kadonaga J . Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat Struct Mol Biol. 2009; 16(8):847-52. PMC: 2823114. DOI: 10.1038/nsmb.1636. View

Zhang Z, Wippo C, Wal M, Ward E, Korber P, Pugh B . A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science. 2011; 332(6032):977-80. PMC: 4852979. DOI: 10.1126/science.1200508. View

10.

Kane D, Kimmel C . The zebrafish midblastula transition. Development. 1993; 119(2):447-56. DOI: 10.1242/dev.119.2.447. View

11.

Mavrich T, Ioshikhes I, Venters B, Jiang C, Tomsho L, Qi J . A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res. 2008; 18(7):1073-83. PMC: 2493396. DOI: 10.1101/gr.078261.108. View

12.

Bai L, Morozov A . Gene regulation by nucleosome positioning. Trends Genet. 2010; 26(11):476-83. DOI: 10.1016/j.tig.2010.08.003. View

13.

Hughes A, Jin Y, Rando O, Struhl K . A functional evolutionary approach to identify determinants of nucleosome positioning: a unifying model for establishing the genome-wide pattern. Mol Cell. 2012; 48(1):5-15. PMC: 3472102. DOI: 10.1016/j.molcel.2012.07.003. View

14.

Nekrasov M, Amrichova J, Parker B, Soboleva T, Jack C, Williams R . Histone H2A.Z inheritance during the cell cycle and its impact on promoter organization and dynamics. Nat Struct Mol Biol. 2012; 19(11):1076-83. DOI: 10.1038/nsmb.2424. View

15.

Harvey S, Sealy I, Kettleborough R, Fenyes F, White R, Stemple D . Identification of the zebrafish maternal and paternal transcriptomes. Development. 2013; 140(13):2703-10. PMC: 3678340. DOI: 10.1242/dev.095091. View

16.

Reppas N, Wade J, Church G, Struhl K . The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting. Mol Cell. 2006; 24(5):747-757. DOI: 10.1016/j.molcel.2006.10.030. View

17.

Rahl P, Lin C, Seila A, Flynn R, McCuine S, Burge C . c-Myc regulates transcriptional pause release. Cell. 2010; 141(3):432-45. PMC: 2864022. DOI: 10.1016/j.cell.2010.03.030. View

18.

Lindeman L, Andersen I, Reiner A, Li N, Aanes H, Ostrup O . Prepatterning of developmental gene expression by modified histones before zygotic genome activation. Dev Cell. 2011; 21(6):993-1004. DOI: 10.1016/j.devcel.2011.10.008. View

19.

Zhang Y, Shin H, Song J, Lei Y, Liu X . Identifying positioned nucleosomes with epigenetic marks in human from ChIP-Seq. BMC Genomics. 2008; 9:537. PMC: 2596141. DOI: 10.1186/1471-2164-9-537. View

20.

Struhl K, Segal E . Determinants of nucleosome positioning. Nat Struct Mol Biol. 2013; 20(3):267-73. PMC: 3740156. DOI: 10.1038/nsmb.2506. View