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Structural plasticity of single chromatin fibers revealed by torsional manipulation

Nature Structural & Molecular Biology volume 13, pages 444–450 (2006)Cite this article

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Abstract

Magnetic tweezers were used to study the mechanical response under torsion of single nucleosome arrays reconstituted on tandem repeats of 5S positioning sequences. Regular arrays are extremely resilient and can reversibly accommodate a large amount of supercoiling without much change in length. This behavior is quantitatively described by a molecular model of the chromatin three-dimensional architecture. In this model, we assume the existence of a dynamic equilibrium between three conformations of the nucleosome, corresponding to different crossing statuses of the entry/exit DNAs (positive, null or negative, respectively). Torsional strain displaces that equilibrium, leading to an extensive reorganization of the fiber's architecture. The model explains a number of long-standing topological questions regarding DNA in chromatin and may provide the basis to better understand the dynamic binding of chromatin-associated proteins.

Note: In the supplementary information initially published online to accompany this article, Supplementary Figure 2 was mistakenly replaced by Supplementary Equation 2. The error has been corrected online.

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Figure 1: Schematic of the experiment.
Figure 2: Micromanipulation of single chromatin fibers.
Figure 3: Tension dependence of the fiber behavior.
Figure 4: Salt-dependence of the fiber's mechanical behavior.
Figure 5: Three-state model of the chromatin fiber.
Figure 6: Single-parameter fitting.
Figure 7: Chromatin as a topological buffer.

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  • 30 April 2006

    Figure incorrect and author name incorrect in pubmed

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Acknowledgements

The authors are grateful to G. Almouzni and J.P. Quivy for providing material in preliminary experiments, E. Ben-Haim and C. Bouchiat for discussions and K. Dorfman and A. Sivolob for critical reading. A.B., N.C.eS., G.W., C.L. and J.M. thank the French Ministry of Research for AC-MENRT fellowships. This work was supported by the Centre National de la Recherche Scientifique (A.P.'s and J.M.V.'s laboratories) and by grants from the Centre National de la Recherche Scientifique/Ministère de l'Education Nationale de la Recherche et de la Technologie DRAB programs and the Institut Curie Physics of the Cell cooperative program (J.L.V.'s laboratory).

Author information

Authors and Affiliations

  1. Institut Curie, UMR 168, Paris, 75231, France

    Aurélien Bancaud, Gaudeline Wagner & Jean-Louis Viovy

  2. Institut Jacques Monod (UMR 7592), 2 Place Jussieu, Paris, 75251 cedex 05, France

    Natalia Conde e Silva, Christophe Lavelle & Ariel Prunell

  3. Laboratoire de Physique Théorique de la Matière Condensée (UMR 7600), 4 Place Jussieu, Paris, 75252 cedex 05, France

    Maria Barbi, Julien Mozziconacci, Christophe Lavelle & Jean-Marc Victor

  4. Laboratoire de Physique Statistique (UMR 8549), 24 Rue Lhomond, Paris, 75231 cedex 05, France

    Jean-François Allemand & Vincent Croquette

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Correspondence to Ariel Prunell or Jean-Louis Viovy.

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Supplementary information

Supplementary Fig. 1

Regular and irregular fibers (PDF 227 kb)

Supplementary Fig. 2

The 'single-state' fiber (PDF 288 kb)

Supplementary Fig. 3

'Open-state' and 'positive-state' ideal fibers (PDF 297 kb)

Supplementary Fig. 4

The 'three-state' fiber (PDF 290 kb)

Supplementary Fig. 5

Plectoneme structures (PDF 764 kb)

Supplementary Discussion (PDF 132 kb)

Supplementary Equation 1

Length and topology. (PDF 179 kb)

Supplementary Equation 2

Gibbs free energy of a fiber containing nucleosomes fluctuating between 3 states. (PDF 19 kb)

Supplementary Equation 3

Proportion of nucleosomes in the negative state as a function of the external torque C. (PDF 171 kb)

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Bancaud, A., Conde e Silva, N., Barbi, M. et al. Structural plasticity of single chromatin fibers revealed by torsional manipulation. Nat Struct Mol Biol 13, 444–450 (2006). https://doi.org/10.1038/nsmb1087

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