Directed RNase H Cleavage of Nascent Transcripts Causes Transcription Termination

Mol Cell. 2020 Mar 5;77(5):1032-1043.e4. doi: 10.1016/j.molcel.2019.12.029. Epub 2020 Jan 7.

Abstract

An attractive approach to reduce gene expression is via the use of antisense oligonucleotides (ASOs) that harness the RNase H1 mechanism. Here we show that RNase H ASOs targeted to introns or exons robustly reduce the level of spliced RNA associated with chromatin. Surprisingly, intron-targeted ASOs reduce the level of pre-mRNA associated with chromatin to a greater extent than exon-targeted ASOs. This indicates that exon-targeted ASOs achieve full activity after the pre-mRNA has undergone splicing, but before the mRNA is released from chromatin. Even though RNase H ASOs can reduce the level of RNA associated with chromatin, the effect of ASO-directed RNA degradation on transcription has never been documented. Here we show that intron-targeted ASOs and, to a lesser extent, exon-targeted ASOs cause RNA polymerase II (Pol II) transcription termination in cultured cells and mice. Furthermore, ASO-directed transcription termination is mediated by the nuclear exonuclease XRN2.

Keywords: ASO; RNase H; XRN2; chromatin; torpedo.

MeSH terms

  • Animals
  • Chromatin / genetics
  • Chromatin / metabolism*
  • Exons
  • Exoribonucleases / genetics
  • Exoribonucleases / metabolism
  • Female
  • HCT116 Cells
  • Humans
  • Introns
  • Mice, Inbred C57BL
  • Models, Genetic
  • Nedd4 Ubiquitin Protein Ligases / genetics
  • Nedd4 Ubiquitin Protein Ligases / metabolism
  • Oligonucleotides, Antisense / genetics
  • Oligonucleotides, Antisense / metabolism*
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism
  • RNA Precursors / genetics
  • RNA Precursors / metabolism*
  • RNA Stability*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism*
  • Ribonuclease H / genetics
  • Ribonuclease H / metabolism*
  • Time Factors
  • Transcription Termination, Genetic*

Substances

  • Chromatin
  • Oligonucleotides, Antisense
  • RNA Precursors
  • RNA, Messenger
  • Nedd4 Ubiquitin Protein Ligases
  • Nedd4 protein, human
  • Nedd4 protein, mouse
  • RNA Polymerase II
  • Exoribonucleases
  • Xrn2 protein, mouse
  • XRN2 protein, human
  • Ribonuclease H