FTO promotes gefitinib-resistance by enhancing PELI3 expression and autophagy in non-small cell lung cancer

Pulm Pharmacol Ther. 2024 Dec:87:102317. doi: 10.1016/j.pupt.2024.102317. Epub 2024 Aug 16.

Abstract

The established recognition of N6-methyladenosine (m6A) modification as an indispensable regulatory agent in human cancer is widely accepted. However, the understanding of m6A's role and the mechanisms underlying its contribution to gefitinib resistance is notably limited. Herein, using RT-qPCR, Western blot, Cell proliferation and apoptosis, as well as RNA m6A modification assays, we substantiated that heightened FTO (Fat Mass and Obesity-associated protein) expression substantially underpins the emergence of gefitinib resistance in NSCLC cells. This FTO-driven gefitinib resistance is hinged upon the co-occurrence of PELI3 (Pellino E3 Ubiquitin Protein Ligase Family Member 3) expression and concurrent autophagy activation. Manipulation of PELI3 expression and autophagy activation, including its attenuation, was efficacious in both inducing and overcoming gefitinib resistance within NSCLC cells, as validated in vitro and in vivo. In summary, this study has successfully elucidated the intricate interplay involving FTO-mediated m6A modification, its consequential downstream effect on PELI3, and the concurrent involvement of autophagy in fostering the emergence of gefitinib resistance within the therapeutic context of NSCLC.

Keywords: Autophagy; FTO; Gefitinib-resistance; N6-methyladenosine; Non-small cell lung cancer; PELI3.

MeSH terms

  • Adenosine / analogs & derivatives
  • Adenosine / pharmacology
  • Alpha-Ketoglutarate-Dependent Dioxygenase FTO* / genetics
  • Alpha-Ketoglutarate-Dependent Dioxygenase FTO* / metabolism
  • Animals
  • Antineoplastic Agents* / pharmacology
  • Apoptosis / drug effects
  • Autophagy* / drug effects
  • Carcinoma, Non-Small-Cell Lung* / drug therapy
  • Carcinoma, Non-Small-Cell Lung* / genetics
  • Carcinoma, Non-Small-Cell Lung* / metabolism
  • Carcinoma, Non-Small-Cell Lung* / pathology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Drug Resistance, Neoplasm* / genetics
  • Gefitinib* / pharmacology
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Lung Neoplasms* / drug therapy
  • Lung Neoplasms* / genetics
  • Lung Neoplasms* / pathology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Ubiquitin-Protein Ligases* / genetics
  • Ubiquitin-Protein Ligases* / metabolism

Substances

  • Gefitinib
  • Alpha-Ketoglutarate-Dependent Dioxygenase FTO
  • FTO protein, human
  • Ubiquitin-Protein Ligases
  • Antineoplastic Agents
  • N-methyladenosine
  • Nuclear Proteins
  • Adenosine