High-resolution Biophysical Analysis of the Dynamics of Nucleosome Formation

Overview

Journal Sci Rep

Specialty Science

Date 2016 Jun 7

PMID 27263658

Citations 5

Authors

Akiko Hatakeyama

Brigitte Hartmann

Andrew Travers

Claude Nogues

Malcolm Buckle

Affiliations

Soon will be listed here.

Abstract

We describe a biophysical approach that enables changes in the structure of DNA to be followed during nucleosome formation in in vitro reconstitution with either the canonical "Widom" sequence or a judiciously mutated sequence. The rapid non-perturbing photochemical analysis presented here provides 'snapshots' of the DNA configuration at any given moment in time during nucleosome formation under a very broad range of reaction conditions. Changes in DNA photochemical reactivity upon protein binding are interpreted as being mainly induced by alterations in individual base pair roll angles. The results strengthen the importance of the role of an initial (H3/H4)2 histone tetramer-DNA interaction and highlight the modulation of this early event by the DNA sequence. (H3/H4)2 binding precedes and dictates subsequent H2A/H2B-DNA interactions, which are less affected by the DNA sequence, leading to the final octameric nucleosome. Overall, our results provide a novel, exciting way to investigate those biophysical properties of DNA that constitute a crucial component in nucleosome formation and stabilization.

Citing Articles

Nucleosome assembly and disassembly pathways in vitro.

Hatakeyama A, Shymko Y, Hartmann B, Retureau R, Nogues C, Pasi M PLoS One. 2022; 17(7):e0267382.

PMID: 35830437 PMC: 9278766. DOI: 10.1371/journal.pone.0267382.

Slow motions in A·T rich DNA sequence.

Ben Imeddourene A, Zargarian L, Buckle M, Hartmann B, Mauffret O Sci Rep. 2020; 10(1):19005.

PMID: 33149183 PMC: 7642443. DOI: 10.1038/s41598-020-75645-x.

Histone deposition promotes recombination-dependent replication at arrested forks.

Hardy J, Dai D, Ait Saada A, Teixeira-Silva A, Dupoiron L, Mojallali F PLoS Genet. 2019; 15(10):e1008441.

PMID: 31584934 PMC: 6795475. DOI: 10.1371/journal.pgen.1008441.

Photochemical analysis of structural transitions in DNA liquid crystals reveals differences in spatial structure of DNA molecules organized in liquid crystalline form.

Brach K, Hatakeyama A, Nogues C, Olesiak-Banska J, Buckle M, Matczyszyn K Sci Rep. 2018; 8(1):4528.

PMID: 29540820 PMC: 5852169. DOI: 10.1038/s41598-018-22863-z.

Yeast HMO1: Linker Histone Reinvented.

Panday A, Grove A Microbiol Mol Biol Rev. 2016; 81(1).

PMID: 27903656 PMC: 5312240. DOI: 10.1128/MMBR.00037-16.

References

Wu B, Mohideen K, Vasudevan D, Davey C . Structural insight into the sequence dependence of nucleosome positioning. Structure. 2010; 18(4):528-36. DOI: 10.1016/j.str.2010.01.015. View

Jackson S, Brooks W, Jackson V . Dynamics of the interactions of histones H2A,H2B and H3,H4 with torsionally stressed DNA. Biochemistry. 1994; 33(18):5392-403. DOI: 10.1021/bi00184a006. View

Luger K, Mader A, Richmond R, Sargent D, Richmond T . Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997; 389(6648):251-60. DOI: 10.1038/38444. View

Makde R, England J, Yennawar H, Tan S . Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature. 2010; 467(7315):562-6. PMC: 3168546. DOI: 10.1038/nature09321. View

Olson W, Zhurkin V . Working the kinks out of nucleosomal DNA. Curr Opin Struct Biol. 2011; 21(3):348-57. PMC: 3112303. DOI: 10.1016/j.sbi.2011.03.006. View

Fernandez A, Anderson J . Nucleosome positioning determinants. J Mol Biol. 2007; 371(3):649-68. DOI: 10.1016/j.jmb.2007.05.090. View

Xu F, Olson W . DNA architecture, deformability, and nucleosome positioning. J Biomol Struct Dyn. 2010; 27(6):725-39. PMC: 3000044. DOI: 10.1080/073911010010524943. View

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

GODFREY J, Eickbush T, Moudrianakis E . Reversible association of calf thymus histones to form the symmetrical octamer (H2AH2BH3H4)2: a case of a mixed-associating system. Biochemistry. 1980; 19(7):1339-46. DOI: 10.1021/bi00548a012. View

10.

Widom J . Role of DNA sequence in nucleosome stability and dynamics. Q Rev Biophys. 2002; 34(3):269-324. DOI: 10.1017/s0033583501003699. View

11.

Satchwell S, Drew H, Travers A . Sequence periodicities in chicken nucleosome core DNA. J Mol Biol. 1986; 191(4):659-75. DOI: 10.1016/0022-2836(86)90452-3. View

12.

Buttinelli M, Minnock A, Panetta G, Waring M, Travers A . The exocyclic groups of DNA modulate the affinity and positioning of the histone octamer. Proc Natl Acad Sci U S A. 1998; 95(15):8544-9. PMC: 21112. DOI: 10.1073/pnas.95.15.8544. View

13.

Berman H . Crystal studies of B-DNA: the answers and the questions. Biopolymers. 1997; 44(1):23-44. DOI: 10.1002/(SICI)1097-0282(1997)44:1<23::AID-BIP3>3.0.CO;2-1. View

14.

Pehrson J . Thymine dimer formation as a probe of the path of DNA in and between nucleosomes in intact chromatin. Proc Natl Acad Sci U S A. 1989; 86(23):9149-53. PMC: 298451. DOI: 10.1073/pnas.86.23.9149. View

15.

Cui F, Zhurkin V . Structure-based analysis of DNA sequence patterns guiding nucleosome positioning in vitro. J Biomol Struct Dyn. 2010; 27(6):821-41. PMC: 2993692. DOI: 10.1080/073911010010524947. View

16.

Heddi B, Oguey C, Lavelle C, Foloppe N, Hartmann B . Intrinsic flexibility of B-DNA: the experimental TRX scale. Nucleic Acids Res. 2009; 38(3):1034-47. PMC: 2817485. DOI: 10.1093/nar/gkp962. View

17.

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

18.

Gale J, Smerdon M . Photofootprint of nucleosome core DNA in intact chromatin having different structural states. J Mol Biol. 1988; 204(4):949-58. DOI: 10.1016/0022-2836(88)90054-x. View

19.

Norambuena T, Melo F . The Protein-DNA Interface database. BMC Bioinformatics. 2010; 11:262. PMC: 2885377. DOI: 10.1186/1471-2105-11-262. View

20.

Tolstorukov M, Jernigan R, Zhurkin V . Protein-DNA hydrophobic recognition in the minor groove is facilitated by sugar switching. J Mol Biol. 2004; 337(1):65-76. DOI: 10.1016/j.jmb.2004.01.011. View