Evidence for rRNA 2′-O-methylation plasticity: Control of intrinsic translational capabilities of human ribosomes

Author:

Erales Jenny,Marchand Virginie,Panthu Baptiste,Gillot Sandra,Belin Stéphane,Ghayad Sandra E.,Garcia Maxime,Laforêts Florian,Marcel Virginie,Baudin-Baillieu Agnès,Bertin Pierre,Couté Yohann,Adrait Annie,Meyer Mélanie,Therizols Gabriel,Yusupov Marat,Namy OlivierORCID,Ohlmann Théophile,Motorin Yuri,Catez FrédéricORCID,Diaz Jean-Jacques

Abstract

Ribosomal RNAs (rRNAs) are main effectors of messenger RNA (mRNA) decoding, peptide-bond formation, and ribosome dynamics during translation. Ribose 2′-O-methylation (2′-O-Me) is the most abundant rRNA chemical modification, and displays a complex pattern in rRNA. 2′-O-Me was shown to be essential for accurate and efficient protein synthesis in eukaryotic cells. However, whether rRNA 2′-O-Me is an adjustable feature of the human ribosome and a means of regulating ribosome function remains to be determined. Here we challenged rRNA 2′-O-Me globally by inhibiting the rRNA methyl-transferase fibrillarin in human cells. Using RiboMethSeq, a nonbiased quantitative mapping of 2′-O-Me, we identified a repertoire of 2′-O-Me sites subjected to variation and demonstrate that functional domains of ribosomes are targets of 2′-O-Me plasticity. Using the cricket paralysis virus internal ribosome entry site element, coupled to in vitro translation, we show that the intrinsic capability of ribosomes to translate mRNAs is modulated through a 2′-O-Me pattern and not by nonribosomal actors of the translational machinery. Our data establish rRNA 2′-O-Me plasticity as a mechanism providing functional specificity to human ribosomes.

Funder

Agence Nationale de la Recherche

Ligue Contre le Cancer

Fondation ARC pour la Recherche sur le Cancer

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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