Nopp140-chaperoned 2'-O-methylation of small nuclear RNAs in Cajal bodies ensures splicing fidelity

Genes Dev. 2021 Aug 1;35(15-16):1123-1141. doi: 10.1101/gad.348660.121. Epub 2021 Jul 22.

Abstract

Spliceosomal small nuclear RNAs (snRNAs) are modified by small Cajal body (CB)-specific ribonucleoproteins (scaRNPs) to ensure snRNP biogenesis and pre-mRNA splicing. However, the function and subcellular site of snRNA modification are largely unknown. We show that CB localization of the protein Nopp140 is essential for concentration of scaRNPs in that nuclear condensate; and that phosphorylation by casein kinase 2 (CK2) at ∼80 serines targets Nopp140 to CBs. Transiting through CBs, snRNAs are apparently modified by scaRNPs. Indeed, Nopp140 knockdown-mediated release of scaRNPs from CBs severely compromises 2'-O-methylation of spliceosomal snRNAs, identifying CBs as the site of scaRNP catalysis. Additionally, alternative splicing patterns change indicating that these modifications in U1, U2, U5, and U12 snRNAs safeguard splicing fidelity. Given the importance of CK2 in this pathway, compromised splicing could underlie the mode of action of small molecule CK2 inhibitors currently considered for therapy in cholangiocarcinoma, hematological malignancies, and COVID-19.

Keywords: Cajal bodies; RNA modification; casein kinase 2; nuclear organization; phosphorylation; pre-mRNA splicing; scaRNPs; snRNA; snoRNPs.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • COVID-19 Drug Treatment
  • Casein Kinase II / antagonists & inhibitors
  • Casein Kinase II / metabolism
  • Cholangiocarcinoma / drug therapy
  • Hematologic Neoplasms / drug therapy
  • Humans
  • Interstitial Cells of Cajal / metabolism*
  • Methylation*
  • Nuclear Proteins / metabolism*
  • Phosphoproteins / metabolism*
  • Phosphorylation
  • RNA Splicing*
  • RNA, Small Nuclear / chemistry
  • RNA, Small Nuclear / metabolism*
  • Ribonucleoproteins / metabolism
  • Spliceosomes / genetics

Substances

  • NOLC1 protein, human
  • Nuclear Proteins
  • Phosphoproteins
  • RNA, Small Nuclear
  • Ribonucleoproteins
  • Casein Kinase II