REST-dependent glioma progression occurs independently of the repression of the long non-coding RNA HAR1A

PLoS One. 2024 Nov 27;19(11):e0312237. doi: 10.1371/journal.pone.0312237. eCollection 2024.

Abstract

The long non-coding RNA (lncRNA), HAR1A is emerging as a putative tumour suppressor. In non-neoplastic brain cells, REST suppresses HAR1A expression. In gliomas REST acts as an oncogene and is a potential therapeutic target. It is therefore conceivable that REST promotes glioma progression by down-regulating HAR1A. To test this hypothesis, glioma clinical databases were analysed to study: (I) HAR1A/REST correlation; (II) HAR1A and REST prognostic role; (III) molecular pathways associated with these genes. HAR1A expression and subcellular localization were studied in glioblastoma and paediatric glioma cells. REST function was also studied in these cells, by observing the effects of gene silencing on: (I) HAR1A expression; (II) cancer cell proliferation, apoptosis, migration; (III) expression of neural differentiation genes. The same phenotypes (and cell morphology) were studied in HAR1A overexpressing cells. Our results show that REST and HAR1A are negatively correlated in gliomas. Higher REST expression predicts worse prognosis in low-grade gliomas (the opposite is true for HAR1A). REST-silencing induces HAR1A upregulation. HAR1A is primarily detected in the nucleus. REST-silencing dramatically reduces cell proliferation and induces apoptosis, but HAR1A overexpression has no major effect on investigated cell phenotypes. We also show that REST regulates the expression of neural differentiation genes and that its oncogenic function is primarily HAR1A-independent.

MeSH terms

  • Apoptosis* / genetics
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Movement / genetics
  • Cell Proliferation* / genetics
  • Disease Progression*
  • Gene Expression Regulation, Neoplastic*
  • Gene Silencing
  • Glioma* / genetics
  • Glioma* / metabolism
  • Glioma* / pathology
  • Humans
  • Prognosis
  • RNA, Long Noncoding* / genetics
  • RNA, Long Noncoding* / metabolism
  • Repressor Proteins* / genetics
  • Repressor Proteins* / metabolism

Substances

  • RE1-silencing transcription factor
  • RNA, Long Noncoding
  • Repressor Proteins

Grants and funding

This work was supported by the European Union’s NextGenerationEU (grant number CN00000041). The grant was awarded to Istituto Italiano di Tecnologia (IIT), with Dr. Benedetto Grimaldi as the recipient of the funding.