Folding heterogeneity in the essential human telomerase RNA three-way junction

RNA. 2020 Dec;26(12):1787-1800. doi: 10.1261/rna.077255.120. Epub 2020 Aug 19.

Abstract

Telomeres safeguard the genome by suppressing illicit DNA damage responses at chromosome termini. To compensate for incomplete DNA replication at telomeres, most continually dividing cells, including many cancers, express the telomerase ribonucleoprotein (RNP) complex. Telomerase maintains telomere length by catalyzing de novo synthesis of short DNA repeats using an internal telomerase RNA (TR) template. TRs from diverse species harbor structurally conserved domains that contribute to RNP biogenesis and function. In vertebrate TRs, the conserved regions 4 and 5 (CR4/5) fold into a three-way junction (TWJ) that binds directly to the telomerase catalytic protein subunit and is required for telomerase function. We have analyzed the structural properties of the human TR (hTR) CR4/5 domain using a combination of in vitro chemical mapping, secondary structural modeling, and single-molecule structural analysis. Our data suggest the essential P6.1 stem-loop within CR4/5 is not stably folded in the absence of the telomerase reverse transcriptase in vitro. Rather, the hTR CR4/5 domain adopts a heterogeneous ensemble of conformations. Finally, single-molecule FRET measurements of CR4/5 and a mutant designed to stabilize the P6.1 stem demonstrate that TERT binding selects for a structural conformation of CR4/5 that is not the dominant state of the TERT-free in vitro RNA ensemble.

Keywords: RNA folding; single-molecule FRET; structure modeling; telomerase.

Publication types

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

MeSH terms

  • Binding Sites
  • Humans
  • Models, Molecular
  • Protein Binding
  • RNA / chemistry*
  • RNA / genetics
  • RNA / metabolism
  • RNA Folding*
  • Telomerase / chemistry*
  • Telomerase / genetics
  • Telomerase / metabolism*

Substances

  • telomerase RNA
  • RNA
  • TERT protein, human
  • Telomerase