U6 snRNA m6A modification is required for accurate and efficient splicing of C. elegans and human pre-mRNAs

Nucleic Acids Res. 2024 Aug 27;52(15):9139-9160. doi: 10.1093/nar/gkae447.

Abstract

pre-mRNA splicing is a critical feature of eukaryotic gene expression. Both cis- and trans-splicing rely on accurately recognising splice site sequences by spliceosomal U snRNAs and associated proteins. Spliceosomal snRNAs carry multiple RNA modifications with the potential to affect different stages of pre-mRNA splicing. Here, we show that the conserved U6 snRNA m6A methyltransferase METT-10 is required for accurate and efficient cis- and trans-splicing of C. elegans pre-mRNAs. The absence of METT-10 in C. elegans and METTL16 in humans primarily leads to alternative splicing at 5' splice sites with an adenosine at +4 position. In addition, METT-10 is required for splicing of weak 3' cis- and trans-splice sites. We identified a significant overlap between METT-10 and the conserved splicing factor SNRNP27K in regulating 5' splice sites with +4A. Finally, we show that editing endogenous 5' splice site +4A positions to +4U restores splicing to wild-type positions in a mett-10 mutant background, supporting a direct role for U6 snRNA m6A modification in 5' splice site recognition. We conclude that the U6 snRNA m6A modification is important for accurate and efficient pre-mRNA splicing.

MeSH terms

  • Adenosine / analogs & derivatives
  • Adenosine / genetics
  • Adenosine / metabolism
  • Alternative Splicing
  • Animals
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Caenorhabditis elegans* / genetics
  • Caenorhabditis elegans* / metabolism
  • Humans
  • Methyltransferases* / genetics
  • Methyltransferases* / metabolism
  • RNA Precursors* / genetics
  • RNA Precursors* / metabolism
  • RNA Splice Sites*
  • RNA Splicing*
  • RNA, Small Nuclear* / genetics
  • RNA, Small Nuclear* / metabolism
  • Spliceosomes / genetics
  • Spliceosomes / metabolism

Substances

  • RNA, Small Nuclear
  • U6 small nuclear RNA
  • RNA Precursors
  • Methyltransferases
  • Caenorhabditis elegans Proteins
  • RNA Splice Sites
  • Adenosine
  • METTL16 protein, human