Epigenetically silenced lncRNA SNAI3-AS1 promotes ferroptosis in glioma via perturbing the m6A-dependent recognition of Nrf2 mRNA mediated by SND1

J Exp Clin Cancer Res. 2023 May 19;42(1):127. doi: 10.1186/s13046-023-02684-3.

Abstract

Background: Ferroptosis has been linked to tumor progression and resistance to antineoplastic therapy. Long noncoding RNA (lncRNA) exerts a regulatory role in various biological processes of tumor cells, while the function and molecular mechanism of lncRNA in ferroptosis are yet to be clarified in glioma.

Methods: Both gain-of-function and loss-of-function experiments were employed to investigate the effects of SNAI3-AS1 on the tumorigenesis and ferroptosis susceptibility of glioma in vitro and in vivo. Bioinformatics analysis, Bisulfite sequencing PCR, RNA pull-down, RIP, MeRIP and dual-luciferase reporter assay were performed to explore the low expression mechanism of SNAI3-AS1 and the downstream mechanism of SNAI3-AS1 in ferroptosis susceptibility of glioma.

Results: We found that ferroptosis inducer erastin downregulates SNAI3-AS1 expression in glioma by increasing the DNA methylation level of SNAI3-AS1 promoter. SNAI3-AS1 functions as a tumor suppressor in glioma. Importantly, SNAI3-AS1 enhances the anti-tumor activity of erastin by promoting ferroptosis both in vitro and in vivo. Mechanistically, SNAI3-AS1 competitively binds to SND1 and perturbs the m6A-dependent recognition of Nrf2 mRNA 3'UTR by SND1, thereby reducing the mRNA stability of Nrf2. Rescue experiments confirmed that SND1 overexpression and silence can rescue the gain- and loss-of-function ferroptotic phenotypes of SNAI3-AS1, respectively.

Conclusions: Our findings elucidate the effect and detailed mechanism of SNAI3-AS1/SND1/Nrf2 signalling axis in ferroptosis, and provide a theoretical support for inducing ferroptosis to improve glioma treatment.

Keywords: Ferroptosis; Glioma; LncRNA; Nrf2; m6A.

MeSH terms

  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Endonucleases / metabolism
  • Ferroptosis* / genetics
  • Gene Expression Regulation, Neoplastic
  • Glioma* / pathology
  • Humans
  • MicroRNAs* / genetics
  • NF-E2-Related Factor 2 / genetics
  • NF-E2-Related Factor 2 / metabolism
  • RNA, Long Noncoding* / genetics
  • RNA, Long Noncoding* / metabolism
  • RNA, Messenger
  • Snail Family Transcription Factors / genetics
  • Snail Family Transcription Factors / metabolism

Substances

  • Endonucleases
  • MicroRNAs
  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • RNA, Long Noncoding
  • RNA, Messenger
  • Snail Family Transcription Factors
  • SND1 protein, human
  • SNAI3 protein, human