Single-molecule FRET reveals multiscale chromatin dynamics modulated by HP1α

Sinan Kilic, Suren Felekyan, Olga Doroshenko, Iuliia Boichenko, Mykola Dimura, Hayk Vardanyan, Louise C. Bryan, Gaurav Arya, Claus A. M. Seidel () and Beat Fierz ()
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Sinan Kilic: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Suren Felekyan: Heinrich-Heine-Universität
Olga Doroshenko: Heinrich-Heine-Universität
Iuliia Boichenko: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Mykola Dimura: Heinrich-Heine-Universität
Hayk Vardanyan: Heinrich-Heine-Universität
Louise C. Bryan: Ecole Polytechnique Fédérale de Lausanne (EPFL)
Gaurav Arya: Duke University
Claus A. M. Seidel: Heinrich-Heine-Universität
Beat Fierz: Ecole Polytechnique Fédérale de Lausanne (EPFL)

Nature Communications, 2018, vol. 9, issue 1, 1-14

Abstract: Abstract The dynamic architecture of chromatin fibers, a key determinant of genome regulation, is poorly understood. Here, we employ multimodal single-molecule Förster resonance energy transfer studies to reveal structural states and their interconversion kinetics in chromatin fibers. We show that nucleosomes engage in short-lived (micro- to milliseconds) stacking interactions with one of their neighbors. This results in discrete tetranucleosome units with distinct interaction registers that interconvert within hundreds of milliseconds. Additionally, we find that dynamic chromatin architecture is modulated by the multivalent architectural protein heterochromatin protein 1α (HP1α), which engages methylated histone tails and thereby transiently stabilizes stacked nucleosomes. This compacted state nevertheless remains dynamic, exhibiting fluctuations on the timescale of HP1α residence times. Overall, this study reveals that exposure of internal DNA sites and nucleosome surfaces in chromatin fibers is governed by an intrinsic dynamic hierarchy from micro- to milliseconds, allowing the gene regulation machinery to access compact chromatin.

Date: 2018
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DOI: 10.1038/s41467-017-02619-5

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