The makings of TERRA R-loops at chromosome ends

Cell Cycle. 2021 Sep;20(18):1745-1759. doi: 10.1080/15384101.2021.1962638. Epub 2021 Aug 25.

Abstract

Telomeres protect chromosome ends from nucleolytic degradation, uncontrolled recombination by DNA repair enzymes and checkpoint signaling, and they provide mechanisms for their maintenance by semiconservative DNA replication, telomerase and homologous recombination. The telomeric long noncoding RNA TERRA is transcribed from a large number of chromosome ends. TERRA has been implicated in modulating telomeric chromatin structure and checkpoint signaling, and in telomere maintenance by homology directed repair, and telomerase - when telomeres are damaged or very short. Recent work indicates that TERRA association with telomeres involves the formation of DNA:RNA hybrid structures that can be formed post transcription by the RAD51 DNA recombinase, which in turn may trigger homologous recombination between telomeric repeats and telomere elongation. In this review, we describe the mechanisms of TERRA recruitment to telomeres, R-loop formation and its regulation by shelterin proteins. We discuss the consequences of R-loop formation, with regard to telomere maintenance by DNA recombination and how this may impinge on telomere replication while counteracting telomere shortening in normal cells and in ALT cancer cells, which maintain telomeres in the absence of telomerase.

Keywords: R-loops; RAD51; TERRA; Telomeres; homologous recombination; shelterin proteins.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Animals
  • Cell Cycle
  • DNA / metabolism
  • Humans
  • Neoplasms / metabolism*
  • R-Loop Structures*
  • RNA, Long Noncoding / metabolism*
  • Rad51 Recombinase / metabolism
  • Recombinational DNA Repair
  • Repetitive Sequences, Nucleic Acid*
  • Shelterin Complex / metabolism*
  • Signal Transduction*
  • Telomerase / metabolism
  • Telomere Homeostasis*
  • Telomere Shortening
  • Transcription, Genetic*

Substances

  • RNA, Long Noncoding
  • Shelterin Complex
  • DNA
  • Rad51 Recombinase
  • Telomerase

Grants and funding

The laboratory was supported by the Swiss National Science Foundation (SNFS grant 310030_184718), the SNFS-funded National Center of Competence in Research (NCCR) RNA and disease network (grant 182880) and the European Union’s Horizon 2020 research and innovation programme under grant agreement 812829.