CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection

Cell Rep. 2024 Jul 23;43(7):114405. doi: 10.1016/j.celrep.2024.114405. Epub 2024 Jun 25.

Abstract

The RNA cap methyltransferase CMTR1 methylates the first transcribed nucleotide of RNA polymerase II transcripts, impacting gene expression mechanisms, including during innate immune responses. Using mass spectrometry, we identify a multiply phosphorylated region of CMTR1 (phospho-patch [P-Patch]), which is a substrate for the kinase CK2 (casein kinase II). CMTR1 phosphorylation alters intramolecular interactions, increases recruitment to RNA polymerase II, and promotes RNA cap methylation. P-Patch phosphorylation occurs during the G1 phase of the cell cycle, recruiting CMTR1 to RNA polymerase II during a period of rapid transcription and RNA cap formation. CMTR1 phosphorylation is required for the expression of specific RNAs, including ribosomal protein gene transcripts, and promotes cell proliferation. CMTR1 phosphorylation is also required for interferon-stimulated gene expression. The cap-snatching virus, influenza A, utilizes host CMTR1 phosphorylation to produce the caps required for virus production and infection. We present an RNA cap methylation control mechanism whereby CK2 controls CMTR1, enhancing co-transcriptional capping.

Keywords: CMTR1; CP: Microbiology; CP: Molecular biology; RNA; RNA cap; cell proliferation; influenza virus; innate immunity; ribosomes; transcription; translation.

MeSH terms

  • Animals
  • Casein Kinase II* / genetics
  • Casein Kinase II* / metabolism
  • HEK293 Cells
  • Humans
  • Influenza A virus
  • Influenza, Human / genetics
  • Influenza, Human / metabolism
  • Influenza, Human / virology
  • Methylation
  • Methyltransferases* / metabolism
  • Phosphorylation
  • RNA Caps* / metabolism
  • RNA Polymerase II / metabolism

Substances

  • Casein Kinase II
  • Methyltransferases
  • RNA Caps
  • RNA Polymerase II
  • CMTR1 protein, human