RNA G-quadruplexes control mitochondria-localized mRNA translation and energy metabolism

Abstract Cancer cells rely on mitochondria for their bioenergetic supply and macromolecule synthesis. Central to mitochondrial function is the regulation of mitochondrial protein synthesis, which primarily depends on the cytoplasmic translation of nuclear-encoded mitochondrial mRNAs whose protein pr...

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Main Authors: Leïla Dumas, Sauyeun Shin, Quentin Rigaud, Marie Cargnello, Beatriz Hernández-Suárez, Pauline Herviou, Nathalie Saint-Laurent, Marjorie Leduc, Morgane Le Gall, David Monchaud, Erik Dassi, Anne Cammas, Stefania Millevoi
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-58118-5
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author Leïla Dumas
Sauyeun Shin
Quentin Rigaud
Marie Cargnello
Beatriz Hernández-Suárez
Pauline Herviou
Nathalie Saint-Laurent
Marjorie Leduc
Morgane Le Gall
David Monchaud
Erik Dassi
Anne Cammas
Stefania Millevoi
author_facet Leïla Dumas
Sauyeun Shin
Quentin Rigaud
Marie Cargnello
Beatriz Hernández-Suárez
Pauline Herviou
Nathalie Saint-Laurent
Marjorie Leduc
Morgane Le Gall
David Monchaud
Erik Dassi
Anne Cammas
Stefania Millevoi
author_sort Leïla Dumas
collection DOAJ
description Abstract Cancer cells rely on mitochondria for their bioenergetic supply and macromolecule synthesis. Central to mitochondrial function is the regulation of mitochondrial protein synthesis, which primarily depends on the cytoplasmic translation of nuclear-encoded mitochondrial mRNAs whose protein products are imported into mitochondria. Despite the growing evidence that mitochondrial protein synthesis contributes to the onset and progression of cancer, and can thus offer new opportunities for cancer therapy, knowledge of the underlying molecular mechanisms remains limited. Here, we show that RNA G-quadruplexes (RG4s) regulate mitochondrial function by modulating cytoplasmic mRNA translation of nuclear-encoded mitochondrial proteins. Our data support a model whereby the RG4 folding dynamics, under the control of oncogenic signaling and modulated by small molecule ligands or RG4-binding proteins, modifies mitochondria-localized cytoplasmic protein synthesis. Ultimately, this impairs mitochondrial functions, affecting energy metabolism and consequently cancer cell proliferation.
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spelling doaj-art-a2996d78a2ac47da93bcfc4632a208c22025-08-20T03:06:57ZengNature PortfolioNature Communications2041-17232025-04-0116112210.1038/s41467-025-58118-5RNA G-quadruplexes control mitochondria-localized mRNA translation and energy metabolismLeïla Dumas0Sauyeun Shin1Quentin Rigaud2Marie Cargnello3Beatriz Hernández-Suárez4Pauline Herviou5Nathalie Saint-Laurent6Marjorie Leduc7Morgane Le Gall8David Monchaud9Erik Dassi10Anne Cammas11Stefania Millevoi12Centre de Recherches en Cancérologie de Toulouse (CRCT), Université de Toulouse, Equipe Labellisée Fondation ARC, Université de Toulouse, Inserm, CNRS, Université Toulouse III-Paul SabatierCentre de Recherches en Cancérologie de Toulouse (CRCT), Université de Toulouse, Equipe Labellisée Fondation ARC, Université de Toulouse, Inserm, CNRS, Université Toulouse III-Paul SabatierCentre de Recherches en Cancérologie de Toulouse (CRCT), Université de Toulouse, Equipe Labellisée Fondation ARC, Université de Toulouse, Inserm, CNRS, Université Toulouse III-Paul SabatierCentre de Recherches en Cancérologie de Toulouse (CRCT), Université de Toulouse, Equipe Labellisée Fondation ARC, Université de Toulouse, Inserm, CNRS, Université Toulouse III-Paul SabatierCentre de Recherches en Cancérologie de Toulouse (CRCT), Université de Toulouse, Equipe Labellisée Fondation ARC, Université de Toulouse, Inserm, CNRS, Université Toulouse III-Paul SabatierCentre de Recherches en Cancérologie de Toulouse (CRCT), Université de Toulouse, Equipe Labellisée Fondation ARC, Université de Toulouse, Inserm, CNRS, Université Toulouse III-Paul SabatierCentre de Recherches en Cancérologie de Toulouse (CRCT), Université de Toulouse, Equipe Labellisée Fondation ARC, Université de Toulouse, Inserm, CNRS, Université Toulouse III-Paul SabatierProteom’IC facility, Université Paris Cité, CNRS, INSERM Institut CochinProteom’IC facility, Université Paris Cité, CNRS, INSERM Institut CochinInstitut de Chimie Moléculaire (ICMUB), UBFC Dijon CNRS UMR6302Laboratory of RNA Regulatory Networks, Department of Cellular, Computational and Integrative Biology (CIBIO), University of TrentoCentre de Recherches en Cancérologie de Toulouse (CRCT), Université de Toulouse, Equipe Labellisée Fondation ARC, Université de Toulouse, Inserm, CNRS, Université Toulouse III-Paul SabatierCentre de Recherches en Cancérologie de Toulouse (CRCT), Université de Toulouse, Equipe Labellisée Fondation ARC, Université de Toulouse, Inserm, CNRS, Université Toulouse III-Paul SabatierAbstract Cancer cells rely on mitochondria for their bioenergetic supply and macromolecule synthesis. Central to mitochondrial function is the regulation of mitochondrial protein synthesis, which primarily depends on the cytoplasmic translation of nuclear-encoded mitochondrial mRNAs whose protein products are imported into mitochondria. Despite the growing evidence that mitochondrial protein synthesis contributes to the onset and progression of cancer, and can thus offer new opportunities for cancer therapy, knowledge of the underlying molecular mechanisms remains limited. Here, we show that RNA G-quadruplexes (RG4s) regulate mitochondrial function by modulating cytoplasmic mRNA translation of nuclear-encoded mitochondrial proteins. Our data support a model whereby the RG4 folding dynamics, under the control of oncogenic signaling and modulated by small molecule ligands or RG4-binding proteins, modifies mitochondria-localized cytoplasmic protein synthesis. Ultimately, this impairs mitochondrial functions, affecting energy metabolism and consequently cancer cell proliferation.https://doi.org/10.1038/s41467-025-58118-5
spellingShingle Leïla Dumas
Sauyeun Shin
Quentin Rigaud
Marie Cargnello
Beatriz Hernández-Suárez
Pauline Herviou
Nathalie Saint-Laurent
Marjorie Leduc
Morgane Le Gall
David Monchaud
Erik Dassi
Anne Cammas
Stefania Millevoi
RNA G-quadruplexes control mitochondria-localized mRNA translation and energy metabolism
Nature Communications
title RNA G-quadruplexes control mitochondria-localized mRNA translation and energy metabolism
title_full RNA G-quadruplexes control mitochondria-localized mRNA translation and energy metabolism
title_fullStr RNA G-quadruplexes control mitochondria-localized mRNA translation and energy metabolism
title_full_unstemmed RNA G-quadruplexes control mitochondria-localized mRNA translation and energy metabolism
title_short RNA G-quadruplexes control mitochondria-localized mRNA translation and energy metabolism
title_sort rna g quadruplexes control mitochondria localized mrna translation and energy metabolism
url https://doi.org/10.1038/s41467-025-58118-5
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