Dimeric G-quadruplex motifs-induced NFRs determine strong replication origins in vertebrates

Jérémy Poulet-Benedetti, Caroline Tonnerre-Doncarli, Anne-Laure Valton, Marc Laurent, Marie Gérard, Natalja Barinova, Nikolaos Parisis, Florian Massip, Franck Picard () and Marie-Noëlle Prioleau ()
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Jérémy Poulet-Benedetti: Université Paris Cité, CNRS, Institut Jacques Monod
Caroline Tonnerre-Doncarli: Université Paris Cité, CNRS, Institut Jacques Monod
Anne-Laure Valton: Université Paris Cité, CNRS, Institut Jacques Monod
Marc Laurent: Université Paris Cité, CNRS, Institut Jacques Monod
Marie Gérard: Université Paris Cité, CNRS, Institut Jacques Monod
Natalja Barinova: Université Paris Cité, CNRS, Institut Jacques Monod
Nikolaos Parisis: Université Paris Cité, CNRS, Institut Jacques Monod
Florian Massip: MINES ParisTech, PSL-Research University, CBIO-Centre for Computational Biology
Franck Picard: Université de Lyon, Ecole Normale Supérieure de Lyon, CNRS, UMR5239, Université Claude Bernard Lyon 1
Marie-Noëlle Prioleau: Université Paris Cité, CNRS, Institut Jacques Monod

Nature Communications, 2023, vol. 14, issue 1, 1-17

Abstract: Abstract Replication of vertebrate genomes is tightly regulated to ensure accurate duplication, but our understanding of the interplay between genetic and epigenetic factors in this regulation remains incomplete. Here, we investigated the involvement of three elements enriched at gene promoters and replication origins: guanine-rich motifs potentially forming G-quadruplexes (pG4s), nucleosome-free regions (NFRs), and the histone variant H2A.Z, in the firing of origins of replication in vertebrates. We show that two pG4s on the same DNA strand (dimeric pG4s) are sufficient to induce the assembly of an efficient minimal replication origin without inducing transcription in avian DT40 cells. Dimeric pG4s in replication origins are associated with formation of an NFR next to precisely-positioned nucleosomes enriched in H2A.Z on this minimal origin and genome-wide. Thus, our data suggest that dimeric pG4s are important for the organization and duplication of vertebrate genomes. It supports the hypothesis that a nucleosome close to an NFR is a shared signal for the formation of replication origins in eukaryotes.

Date: 2023
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DOI: 10.1038/s41467-023-40441-4

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