A Deformation Energy Model Reveals Sequence-dependent Property of Nucleosome Positioning

Overview

Journal Chromosoma

Specialty Molecular Biology

Date 2021 Jan 16

PMID 33452566

Citations 4

Authors

Guoqing Liu

Hongyu Zhao

Hu Meng

Yongqiang Xing

Lu Cai

Affiliations

Soon will be listed here.

Abstract

We present a deformation energy model for predicting nucleosome positioning, in which a position-dependent structural parameter set derived from crystal structures of nucleosomes was used to calculate the DNA deformation energy. The model is successful in predicting nucleosome occupancy genome-wide in budding yeast, nucleosome free energy, and rotational positioning of nucleosomes. Our model also indicates that the genomic regions underlying the MNase-sensitive nucleosomes in budding yeast have high deformation energy and, consequently, low nucleosome-forming ability, while the MNase-sensitive non-histone particles are characterized by much lower DNA deformation energy and high nucleosome preference. In addition, we also revealed that remodelers, SNF2 and RSC8, are likely to act in chromatin remodeling by binding to broad nucleosome-depleted regions that are intrinsically favorable for nucleosome positioning. Our data support the important role of position-dependent physical properties of DNA in nucleosome positioning.

Citing Articles

Bisulfite probing reveals DNA structural intricacies.

Bagshaw A, Gemmell N Nucleic Acids Res. 2023; 51(7):3261-3269.

PMID: 36881756 PMC: 10123088. DOI: 10.1093/nar/gkad115.

DNA Sequence-Dependent Properties of Nucleosome Positioning in Regions of Distinct Chromatin States in Mouse Embryonic Stem Cells.

Liu G, Zhang Z, Dong B, Liu J Int J Mol Sci. 2022; 23(22).

PMID: 36430966 PMC: 9693356. DOI: 10.3390/ijms232214488.

The Active Mechanism of Nucleosome Depletion by Poly(dA:dT) Tracts In Vivo.

Barnes T, Korber P Int J Mol Sci. 2021; 22(15).

PMID: 34360997 PMC: 8347975. DOI: 10.3390/ijms22158233.

Epigenetic Marks and Variation of Sequence-Based Information Along Genomic Regions Are Predictive of Recombination Hot/Cold Spots in .

Liu G, Song S, Zhang Q, Dong B, Sun Y, Liu G Front Genet. 2021; 12:705038.

PMID: 34267784 PMC: 8276760. DOI: 10.3389/fgene.2021.705038.

References

Maeshima K, Imai R, Tamura S, Nozaki T . Chromatin as dynamic 10-nm fibers. Chromosoma. 2014; 123(3):225-37. PMC: 4031381. DOI: 10.1007/s00412-014-0460-2. View

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

Shrader T, Crothers D . Artificial nucleosome positioning sequences. Proc Natl Acad Sci U S A. 1989; 86(19):7418-22. PMC: 298075. DOI: 10.1073/pnas.86.19.7418. View

Kubik S, Bruzzone M, Challal D, Dreos R, Mattarocci S, Bucher P . Opposing chromatin remodelers control transcription initiation frequency and start site selection. Nat Struct Mol Biol. 2019; 26(8):744-754. DOI: 10.1038/s41594-019-0273-3. View

Guo S, Deng E, Xu L, Ding H, Lin H, Chen W . iNuc-PseKNC: a sequence-based predictor for predicting nucleosome positioning in genomes with pseudo k-tuple nucleotide composition. Bioinformatics. 2014; 30(11):1522-9. DOI: 10.1093/bioinformatics/btu083. View

Xing Y, Zhao X, Cai L . Prediction of nucleosome occupancy in Saccharomyces cerevisiae using position-correlation scoring function. Genomics. 2011; 98(5):359-66. DOI: 10.1016/j.ygeno.2011.07.008. View

Zentner G, Tsukiyama T, Henikoff S . ISWI and CHD chromatin remodelers bind promoters but act in gene bodies. PLoS Genet. 2013; 9(2):e1003317. PMC: 3585014. DOI: 10.1371/journal.pgen.1003317. View

Liu G, Liu G, Tan J, Lin H . DNA physical properties outperform sequence compositional information in classifying nucleosome-enriched and -depleted regions. Genomics. 2018; 111(5):1167-1175. DOI: 10.1016/j.ygeno.2018.07.013. View

Cui F, Chen L, LoVerso P, Zhurkin V . Prediction of nucleosome rotational positioning in yeast and human genomes based on sequence-dependent DNA anisotropy. BMC Bioinformatics. 2014; 15:313. PMC: 4261538. DOI: 10.1186/1471-2105-15-313. View

10.

Deniz O, Flores O, Battistini F, Perez A, Soler-Lopez M, Orozco M . Physical properties of naked DNA influence nucleosome positioning and correlate with transcription start and termination sites in yeast. BMC Genomics. 2011; 12:489. PMC: 3224377. DOI: 10.1186/1471-2164-12-489. View

11.

MacAlpine D, Almouzni G . Chromatin and DNA replication. Cold Spring Harb Perspect Biol. 2013; 5(8):a010207. PMC: 3721285. DOI: 10.1101/cshperspect.a010207. View

12.

Bishop T . Geometry of the nucleosomal DNA superhelix. Biophys J. 2008; 95(3):1007-17. PMC: 2479575. DOI: 10.1529/biophysj.107.122853. View

13.

Thastrom A, Lowary P, Widlund H, Cao H, Kubista M, Widom J . Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J Mol Biol. 1999; 288(2):213-29. DOI: 10.1006/jmbi.1999.2686. View

14.

Anselmi C, Bocchinfuso G, De Santis P, Savino M, Scipioni A . Dual role of DNA intrinsic curvature and flexibility in determining nucleosome stability. J Mol Biol. 1999; 286(5):1293-301. DOI: 10.1006/jmbi.1998.2575. View

15.

Gabdank I, Barash D, Trifonov E . Single-base resolution nucleosome mapping on DNA sequences. J Biomol Struct Dyn. 2010; 28(1):107-22. DOI: 10.1080/07391102.2010.10507347. View

16.

Xi Y, Yao J, Chen R, Li W, He X . Nucleosome fragility reveals novel functional states of chromatin and poises genes for activation. Genome Res. 2011; 21(5):718-24. PMC: 3083088. DOI: 10.1101/gr.117101.110. View

17.

Yuan G, Liu J . Genomic sequence is highly predictive of local nucleosome depletion. PLoS Comput Biol. 2008; 4(1):e13. PMC: 2211532. DOI: 10.1371/journal.pcbi.0040013. View

18.

Olson W, Bansal M, Burley S, DICKERSON R, Gerstein M, Harvey S . A standard reference frame for the description of nucleic acid base-pair geometry. J Mol Biol. 2001; 313(1):229-37. DOI: 10.1006/jmbi.2001.4987. View

19.

Kubik S, Bruzzone M, Jacquet P, Falcone J, Rougemont J, Shore D . Nucleosome Stability Distinguishes Two Different Promoter Types at All Protein-Coding Genes in Yeast. Mol Cell. 2015; 60(3):422-34. DOI: 10.1016/j.molcel.2015.10.002. View

20.

De Santis P, Morosetti S, Scipioni A . Prediction of nucleosome positioning in genomes: limits and perspectives of physical and bioinformatic approaches. J Biomol Struct Dyn. 2010; 27(6):747-64. DOI: 10.1080/07391102.2010.10508583. View