High-resolution Structure of the Native Histone Octamer

Overview

Journal Acta Crystallogr Sect F Struct Biol Cryst Commun

Date 2006 Mar 3

PMID 16511091

Citations 16

Authors

Christopher M Wood

James M Nicholson

Stanley J Lambert

Laurent Chantalat

Colin D Reynolds

John P Baldwin

Affiliations

Soon will be listed here.

Abstract

Crystals of native histone octamers (H2A-H2B)-(H4-H3)-(H3'-H4')-(H2B'-H2A') from chick erythrocytes in 2 M KCl, 1.35 M potassium phosphate pH 6.9 diffract X-rays to 1.90 A resolution, yielding a structure with an R(work) value of 18.7% and an Rfree of 22.2%. The crystal space group is P6(5), the asymmetric unit of which contains one complete octamer. This high-resolution model of the histone-core octamer allows further insight into intermolecular interactions, including water molecules, that dock the histone dimers to the tetramer in the nucleosome-core particle and have relevance to nucleosome remodelling. The three key areas analysed are the H2A'-H3-H4 molecular cluster (also H2A-H3'-H4'), the H4-H2B' interaction (also H4'-H2B) and the H2A'-H4 beta-sheet interaction (also H2A-H4'). The latter of these three regions is important to nucleosome remodelling by RNA polymerase II, as it is shown to be a likely core-histone binding site, and its disruption creates an instability in the nucleosome-core particle. A majority of the water molecules in the high-resolution octamer have positions that correlate to similar positions in the high-resolution nucleosome-core particle structure, suggesting that the high-resolution octamer model can be used for comparative studies with the high-resolution nucleosome-core particle.

Citing Articles

Genetic interaction mapping informs integrative structure determination of protein complexes.

Braberg H, Echeverria I, Bohn S, Cimermancic P, Shiver A, Alexander R Science. 2020; 370(6522).

PMID: 33303586 PMC: 7946025. DOI: 10.1126/science.aaz4910.

Structural insights into the ability of nucleoplasmin to assemble and chaperone histone octamers for DNA deposition.

Franco A, Arranz R, Fernandez-Rivero N, Velazquez-Campoy A, Martin-Benito J, Segura J Sci Rep. 2019; 9(1):9487.

PMID: 31263230 PMC: 6602930. DOI: 10.1038/s41598-019-45726-7.

The Oligomerization Landscape of Histones.

Zhao H, Winogradoff D, Dalal Y, Papoian G Biophys J. 2019; 116(10):1845-1855.

PMID: 31005236 PMC: 6531916. DOI: 10.1016/j.bpj.2019.03.021.

The histone chaperone Vps75 forms multiple oligomeric assemblies capable of mediating exchange between histone H3-H4 tetramers and Asf1-H3-H4 complexes.

Hammond C, Sundaramoorthy R, Larance M, Lamond A, Stevens M, El-Mkami H Nucleic Acids Res. 2016; 44(13):6157-72.

PMID: 27036862 PMC: 5291247. DOI: 10.1093/nar/gkw209.

Integrated molecular mechanism directing nucleosome reorganization by human FACT.

Tsunaka Y, Fujiwara Y, Oyama T, Hirose S, Morikawa K Genes Dev. 2016; 30(6):673-86.

PMID: 26966247 PMC: 4803053. DOI: 10.1101/gad.274183.115.

References

Verreault A, Kaufman P, Kobayashi R, Stillman B . Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr Biol. 1998; 8(2):96-108. DOI: 10.1016/s0960-9822(98)70040-5. View

Guex N, Peitsch M . SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 1998; 18(15):2714-23. DOI: 10.1002/elps.1150181505. View

Suto R, Clarkson M, Tremethick D, Luger K . Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat Struct Biol. 2000; 7(12):1121-4. DOI: 10.1038/81971. View

Lambert S, Nicholson J, Chantalat L, Reid A, Donovan M, Baldwin J . Purification of histone core octamers and 2.15 A X-ray analysis of crystals in KCl/phosphate. Acta Crystallogr D Biol Crystallogr. 1999; 55(Pt 5):1048-51. DOI: 10.1107/s0907444999001912. View

Park Y, Chodaparambil J, Bao Y, McBryant S, Luger K . Nucleosome assembly protein 1 exchanges histone H2A-H2B dimers and assists nucleosome sliding. J Biol Chem. 2004; 280(3):1817-25. DOI: 10.1074/jbc.M411347200. View

Merritt E, Bacon D . Raster3D: photorealistic molecular graphics. Methods Enzymol. 1997; 277:505-24. DOI: 10.1016/s0076-6879(97)77028-9. View

Jones T, Zou J, Cowan S, Kjeldgaard M . Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A. 1991; 47 ( Pt 2):110-9. DOI: 10.1107/s0108767390010224. View

Wittmeyer J, Joss L, Formosa T . Spt16 and Pob3 of Saccharomyces cerevisiae form an essential, abundant heterodimer that is nuclear, chromatin-associated, and copurifies with DNA polymerase alpha. Biochemistry. 1999; 38(28):8961-71. DOI: 10.1021/bi982851d. View

Emsley P, Cowtan K . Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004; 60(Pt 12 Pt 1):2126-32. DOI: 10.1107/S0907444904019158. View

10.

Kireeva M, Walter W, Tchernajenko V, Bondarenko V, Kashlev M, Studitsky V . Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol Cell. 2002; 9(3):541-52. DOI: 10.1016/s1097-2765(02)00472-0. View

11.

Santisteban M, Arents G, Moudrianakis E, Smith M . Histone octamer function in vivo: mutations in the dimer-tetramer interfaces disrupt both gene activation and repression. EMBO J. 1997; 16(9):2493-506. PMC: 1169849. DOI: 10.1093/emboj/16.9.2493. View

12.

Orphanides G, Leroy G, Chang C, Luse D, Reinberg D . FACT, a factor that facilitates transcript elongation through nucleosomes. Cell. 1998; 92(1):105-16. DOI: 10.1016/s0092-8674(00)80903-4. View

13.

Murshudov G, Vagin A, Dodson E . Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr. 1997; 53(Pt 3):240-55. DOI: 10.1107/S0907444996012255. View

14.

Harp J, Hanson B, Timm D, Bunick G . Asymmetries in the nucleosome core particle at 2.5 A resolution. Acta Crystallogr D Biol Crystallogr. 2000; 56(Pt 12):1513-34. DOI: 10.1107/s0907444900011847. View

15.

Belotserkovskaya R, Reinberg D . Facts about FACT and transcript elongation through chromatin. Curr Opin Genet Dev. 2004; 14(2):139-46. DOI: 10.1016/j.gde.2004.02.004. View

16.

Lamzin V, Wilson K . Automated refinement of protein models. Acta Crystallogr D Biol Crystallogr. 1993; 49(Pt 1):129-47. DOI: 10.1107/S0907444992008886. View

17.

Brady Jr G, Stouten P . Fast prediction and visualization of protein binding pockets with PASS. J Comput Aided Mol Des. 2000; 14(4):383-401. DOI: 10.1023/a:1008124202956. View

18.

Otwinowski Z, Minor W . Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997; 276:307-26. DOI: 10.1016/S0076-6879(97)76066-X. View

19.

Baer B, Rhodes D . Eukaryotic RNA polymerase II binds to nucleosome cores from transcribed genes. Nature. 1983; 301(5900):482-8. DOI: 10.1038/301482a0. View

20.

Ramachandran G, Ramakrishnan C, Sasisekharan V . Stereochemistry of polypeptide chain configurations. J Mol Biol. 1963; 7:95-9. DOI: 10.1016/s0022-2836(63)80023-6. View