Loss of 5-methylcytosine alters the biogenesis of vault-derived small RNAs to coordinate epidermal differentiation.

Sajini, Abdulrahim A; Choudhury, Nila Roy; Wagner, Rebecca E; Bornelöv, Susanne; Selmi, Tommaso; Spanos, Christos; Dietmann, Sabine; Rappsilber, Juri et al. · Nat Commun · 2019

basic_science · Level V

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Abstract

The presence and absence of RNA modifications regulates RNA metabolism by modulating the binding of writer, reader, and eraser proteins. For 5-methylcytosine (m<sup>5</sup>C) however, it is largely unknown how it recruits or repels RNA-binding proteins. Here, we decipher the consequences of m<sup>5</sup>C deposition into the abundant non-coding vault RNA VTRNA1.1. Methylation of cytosine 69 in VTRNA1.1 occurs frequently in human cells, is exclusively mediated by NSUN2, and determines the processing of VTRNA1.1 into small-vault RNAs (svRNAs). We identify the serine/arginine rich splicing factor 2 (SRSF2) as a novel VTRNA1.1-binding protein that counteracts VTRNA1.1 processing by binding the non-methylated form with higher affinity. Both NSUN2 and SRSF2 orchestrate the production of distinct svRNAs. Finally, we discover a functional role of svRNAs in regulating the epidermal differentiation programme. Thus, our data reveal a direct role for m<sup>5</sup>C in the processing of VTRNA1.1 that involves SRSF2 and is crucial for efficient cellular differentiation.

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