Nucleosome dynamics. VI. Histone tail regulation of tetrasome chiral transition. A relaxation study of tetrasomes on DNA minicircles - PubMed (original) (raw)
. 2000 Jan 7;295(1):55-69.
doi: 10.1006/jmbi.1999.3302.
Affiliations
- PMID: 10623508
- DOI: 10.1006/jmbi.1999.3302
Nucleosome dynamics. VI. Histone tail regulation of tetrasome chiral transition. A relaxation study of tetrasomes on DNA minicircles
A Sivolob et al. J Mol Biol. 2000.
Abstract
We have recently described the relaxation of mononucleosomes on an homologous series of 351-366 bp DNA minicircles, as a tool to study nucleosome structure and dynamics in vitro. Nucleosomes were found to have a tail-regulated access to three distinct DNA conformations, depending on the crossing between the entering and exiting DNAs, and its polarity. This approach was now used to explore tetrasome chiral transition, and the influence of the histone tails. The data confirmed the existence of two states, with linking number differences DeltaLk(t)=-0.74(+/-0.01) and +0.51(+/-0.06). As expected, the particle free energy is higher in the right-handed state (DeltaG(t)=1.9(+/-0.I) kT), but it decreased (to 1.3(+/-0.1) kT) upon histone acetylation and the addition of phosphate, a potent tail destabilizer. Removal of the tails with trypsin further decreased DeltaG(t) (to 0.6 kT), and also induced a loss of supercoiling in both states, to DeltaLk(t)=-0.64(+/-0.03) and +0. 35(+/-0.05). The loop end-conditions, and hence the parameters of the DNA superhelix, were then calculated for both states using the explicit solutions to the equations of the mechanical equilibrium in the theory of elastic rod model for DNA. Whereas the pitch of the DNA superhelix may be approximately equal and opposite in the two conformations, its radius (r) was 20% larger in the right-handed conformation, confirming previous observations by electron microscopy of a tetrasome lateral opening in that conformation. The above supercoiling losses were found to reflect a further 3 % increase in r (to 23 %) upon removal of the tails in the right-handed conformation, and a 14 % increase in the left-handed conformation. The use of composite tetramers with one histone tail intact and the other removed showed these effects to be essentially due to the H3 tails. Altogether, these results show that the H3 tails oppose the tetrasome opening which is expected to be required to relieve the clash between the entering and exiting DNAs in the course of the transition, but which also appears to be intrinsic to the protein reorientation mechanism. We propose that the block against opening results from the H3 tails intercalating into the small groove of the double helix at +/-10 bp from the dyad, and acting as wedges against local DNA straightening. The tails (especially H3) may therefore regulate tetrasome chiral transition in vivo.
Copyright 2000 Academic Press.
Similar articles
- Nucleosome dynamics. Protein and DNA contributions in the chiral transition of the tetrasome, the histone (H3-H4)2 tetramer-DNA particle.
Alilat M, Sivolob A, Révet B, Prunell A. Alilat M, et al. J Mol Biol. 1999 Aug 27;291(4):815-41. doi: 10.1006/jmbi.1999.2988. J Mol Biol. 1999. PMID: 10452891 - Characterization of specific nucleosomal states by use of selective substitution reagents in model octamer and tetramer structures.
Hamiche A, Richard-Foy H. Hamiche A, et al. Methods. 1999 Nov;19(3):457-64. doi: 10.1006/meth.1999.0882. Methods. 1999. PMID: 10579941 Review. - [Nucleosome structural dynamics and super spiral linking number paradox].
Sivolob AV. Sivolob AV. Mol Biol (Mosk). 2002 May-Jun;36(3):391-6. Mol Biol (Mosk). 2002. PMID: 12068622 Review. Russian.
Cited by
- Nucleosomes play a dual role in regulating transcription dynamics.
Brahmachari S, Tripathi S, Onuchic JN, Levine H. Brahmachari S, et al. Proc Natl Acad Sci U S A. 2024 Jul 9;121(28):e2319772121. doi: 10.1073/pnas.2319772121. Epub 2024 Jul 5. Proc Natl Acad Sci U S A. 2024. PMID: 38968124 - DNA Sequence Is a Major Determinant of Tetrasome Dynamics.
Ordu O, Lusser A, Dekker NH. Ordu O, et al. Biophys J. 2019 Dec 3;117(11):2217-2227. doi: 10.1016/j.bpj.2019.07.055. Epub 2019 Aug 21. Biophys J. 2019. PMID: 31521330 Free PMC article. - Use of double-stranded DNA mini-circles to characterize the covalent topoisomerase-DNA complex.
Millet A, Strauss F, Delagoutte E. Millet A, et al. Sci Rep. 2015 Aug 24;5:13154. doi: 10.1038/srep13154. Sci Rep. 2015. PMID: 26300432 Free PMC article. - A brief review of nucleosome structure.
Cutter AR, Hayes JJ. Cutter AR, et al. FEBS Lett. 2015 Oct 7;589(20 Pt A):2914-22. doi: 10.1016/j.febslet.2015.05.016. Epub 2015 May 14. FEBS Lett. 2015. PMID: 25980611 Free PMC article. Review. - Histone N-terminal tails interfere with nucleosome traversal by RNA polymerase II.
Ujvári A, Hsieh FK, Luse SW, Studitsky VM, Luse DS. Ujvári A, et al. J Biol Chem. 2008 Nov 21;283(47):32236-43. doi: 10.1074/jbc.M806636200. Epub 2008 Sep 23. J Biol Chem. 2008. PMID: 18815126 Free PMC article.
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Research Materials