RBMX involves in telomere stability maintenance by regulating TERRA expression

PLoS Genet. 2023 Sep 27;19(9):e1010937. doi: 10.1371/journal.pgen.1010937. eCollection 2023 Sep.

Abstract

Telomeric repeat-containing RNA (TERRA) is a class of long noncoding RNAs (lncRNAs) that are transcribed from subtelomeric to telomeric region of chromosome ends. TERRA is prone to form R-loop structures at telomeres by invading into telomeric DNA. Excessive telomere R-loops result in telomere instability, so the TERRA level needs to be delicately modulated. However, the molecular mechanisms and factors controlling TERRA level are still largely unknown. In this study, we report that the RNA binding protein RBMX is a novel regulator of TERRA level and telomere integrity. The expression level of TERRA is significantly elevated in RBMX depleted cells, leading to enhanced telomere R-loop formation, replication stress, and telomere instability. We also found that RBMX binds to TERRA and the nuclear exosome targeting protein ZCCHC8 simultaneously, and that TERRA degradation slows down upon RBMX depletion, implying that RBMX promotes TERRA degradation by regulating its transportation to the nuclear exosome, which decays nuclear RNAs. Altogether, these findings uncover a new role of RBMX in TERRA expression regulation and telomere integrity maintenance, and raising RBMX as a potential target of cancer therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Exosomes* / genetics
  • Heterochromatin
  • Humans
  • Nuclear Proteins
  • RNA, Long Noncoding* / genetics
  • Telomere / genetics

Substances

  • Heterochromatin
  • Nuclear Proteins
  • RNA, Long Noncoding

Grants and funding

This work was supported by the National Natural Science Foundation of China [82171549 (HL), 31970683 (HL), 32170757 (WM), 92249304 (WM)]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.