Single nucleosome imaging reveals principles of transient multiscale chromatin reorganization triggered by histone ADP-ribosylation at DNA lesions

Fabiola García Fernández, Junwoo Park, Catherine Chapuis, Eva Pinto Jurado, Victor Imburchia, Rebecca Smith, Edoardo José Longarini, Angela Taddei, Christian Hubert, Nataliya Sokolovska, Ivan Matić, Sébastien Huet () and Judith Miné-Hattab ()
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Fabiola García Fernández: Sorbonne Université
Junwoo Park: Sorbonne Université
Catherine Chapuis: BIOSIT-UMS 3480
Eva Pinto Jurado: BIOSIT-UMS 3480
Victor Imburchia: BIOSIT-UMS 3480
Rebecca Smith: BIOSIT-UMS 3480
Edoardo José Longarini: University of Szeged
Angela Taddei: Nuclear Dynamics
Christian Hubert: Errol laser
Nataliya Sokolovska: Sorbonne Université
Ivan Matić: Max Planck Institute for Biology of Ageing
Sébastien Huet: BIOSIT-UMS 3480
Judith Miné-Hattab: Sorbonne Université

Nature Communications, 2025, vol. 16, issue 1, 1-14

Abstract: Abstract Timely access to DNA lesions is crucial for genome integrity. This process requires profound remodeling of densely packed chromatin to establish a repair-competent architecture. However, limited resolution has made it impossible to fully understand these remodeling events. Here, combining microirradiation with live-cell multiscale imaging, we report that DNA damage-induced changes in genome packing rely on the conformational behaviour of the chromatin fiber. Immediately after damage, a transient increase in nucleosome mobility switches chromatin from a densely-packed state to a looser conformation, making it accessible to repair. While histone poly-ADP-ribosylation is required to trigger this switch, mono-ADP-ribosylation is sufficient to maintain the open-chromatin state. The removal of these histone marks by the ARH3 hydrolase then leads to chromatin recondensation. Together, our multiscale study of chromatin dynamics establishes a global model: distinct waves of histone ADP-ribosylation control nucleosome mobility, triggering a transient breathing of chromatin, crucial for initiating the DNA damage response.

Date: 2025
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DOI: 10.1038/s41467-025-61834-7

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