Control of noncoding RNA production and histone levels by a 5' tRNA fragment

Genes Dev. 2020 Jan 1;34(1-2):118-131. doi: 10.1101/gad.332783.119. Epub 2019 Dec 12.

Abstract

Small RNAs derived from mature tRNAs, referred to as tRNA fragments or "tRFs," are an emerging class of regulatory RNAs with poorly understood functions. We recently identified a role for one specific tRF-5' tRF-Gly-GCC, or tRF-GG-as a repressor of genes associated with the endogenous retroelement MERVL, but the mechanistic basis for this regulation was unknown. Here, we show that tRF-GG plays a role in production of a wide variety of noncoding RNAs-snoRNAs, scaRNAs, and snRNAs-that are dependent on Cajal bodies for stability and activity. Among these noncoding RNAs, regulation of the U7 snRNA by tRF-GG modulates heterochromatin-mediated transcriptional repression of MERVL elements by supporting an adequate supply of histone proteins. Importantly, the effects of inhibiting tRF-GG on histone mRNA levels, on activity of a histone 3' UTR reporter, and ultimately on MERVL regulation could all be suppressed by manipulating U7 RNA levels. We additionally show that the related RNA-binding proteins hnRNPF and hnRNPH bind directly to tRF-GG, and are required for Cajal body biogenesis, positioning these proteins as strong candidates for effectors of tRF-GG function in vivo. Together, our data reveal a conserved mechanism for 5' tRNA fragment control of noncoding RNA biogenesis and, consequently, global chromatin organization.

Keywords: epigenetics; histones; tRNA fragment.

Publication types

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

MeSH terms

  • Animals
  • Cell Line
  • Coiled Bodies / metabolism
  • Gene Expression Regulation*
  • Histones / genetics*
  • Histones / metabolism*
  • Human Embryonic Stem Cells
  • Humans
  • Mice
  • Protein Binding
  • RNA, Small Nuclear / genetics
  • RNA, Transfer / metabolism*
  • RNA, Untranslated / genetics*
  • RNA, Untranslated / metabolism*
  • Retroelements / genetics

Substances

  • Histones
  • RNA, Small Nuclear
  • RNA, Untranslated
  • Retroelements
  • U7 small nuclear RNA
  • RNA, Transfer