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Nucleosomes can invade DNA territories occupied by their neighbors

Nature Structural & Molecular Biology volume 16, pages 151–158 (2009)Cite this article

Abstract

Nucleosomes are the fundamental subunits of eukaryotic chromatin. They are not static entities, but can undergo a number of dynamic transitions, including spontaneous repositioning along DNA. As nucleosomes are spaced close together within genomes, it is likely that on occasion they approach each other and may even collide. Here we have used a dinucleosomal model system to show that the 147-base-pair (bp) DNA territories of two nucleosomes can overlap extensively. In the situation of an overlap by 44 bp or 54 bp, one histone dimer is lost and the resulting complex can condense to form a compact single particle. We propose a pathway in which adjacent nucleosomes promote DNA unraveling as they approach each other and that this permits their 147-bp territories to overlap, and we suggest that these events may represent early steps in a pathway for nucleosome removal via collision.

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Figure 1: Chromatin assembly on defined dinucleosomal templates.
Figure 2: Measuring the histone content of dimeric chromatin particles.
Figure 3: AFM imaging of dinucleosomes.
Figure 4: Helical phasing is required for the condensation of overlapping dinucleosomes.
Figure 5: Formation of overlapping nucleosomes as a result of repositioning.

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Acknowledgements

We would like to thank D. Lamont and K. Beattie for assistance with MS and D. Norman for assistance with modeling. We thank members of the T.O.-H. laboratory for valuable suggestions. M.d.J. and J.v.N. were financially supported by the 'Netherlands Organisation for Scientific Research' (NWO) and the European Science Foundation (ESF). M.E. (Studentship), A.F. and T.O.-H. were funded by the Wellcome Trust (Senior Fellowship 064414).

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  1. Andrew Flaus

    Present address: Present address: Department of Biochemistry, NUI Galway, Ireland.,

Authors and Affiliations

  1. Wellcome Trust Centre for Gene Regulation and Expression, University of Dundee, Dundee, DD1 5EH, UK.,

    Maik Engeholm, Andrew Flaus & Tom Owen-Hughes

  2. Physics of Life Processes, Leiden Institute of Physics, Leiden University, Niels Bohrweg 2, CA, 2333, Leiden, The Netherlands

    Martijn de Jager & John van Noort

  3. Division of Biological Chemistry and Drug Discovery, College of Life Sciences, University of Dundee, Dundee, 5EH, DD1, UK

    Ruth Brenk

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Contributions

M.E. carried out most of the experimental work and data analysis; M.d.J. and J.v.N. carried out AFM and associated data analysis; A.F. performed the assays in Figure 5; R.B. assisted with the modeling of the dinucleosome structure; M.E. and T.O.-H. designed the experiments and wrote the manuscript.

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Correspondence to Tom Owen-Hughes.

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Engeholm, M., de Jager, M., Flaus, A. et al. Nucleosomes can invade DNA territories occupied by their neighbors. Nat Struct Mol Biol 16, 151–158 (2009). https://doi.org/10.1038/nsmb.1551

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