Inhibition of METTL14 overcomes CDK4/6 inhibitor resistance driven by METTL14-m6A-E2F1-axis in ERα-positive breast cancer

J Nanobiotechnology. 2025 Jan 3;23(1):3. doi: 10.1186/s12951-024-03021-2.

Abstract

CDK4/6i, the first-line drug for treating ERα-positive breast cancer, significantly improves clinical outcomes. However, CDK4/6i resistance often develops and remains a major hurdle, and the underlying mechanisms remain challenging to fully investigate. Here, we used Genome-wide CRISPR/Cas9 library screening combined with single-cell sequencing to screen for molecules mediating CDK4/6i resistance and identified METTL14 as a determinant of CDK4/6i sensitivity. Clinical samples and datasets were analyzed and in vitro and in vivo experiments were performed to confirm the critical function of METTL14 in CDK4/6i resistance. Mechanistically, METTL14 can induce an increase in E2F1 expression in breast cancer cells via an m6A IGF2BP2-dependent mechanism and thus promote CDK4/6i resistance. Furthermore, through a small molecule screen, a novel METTL14 inhibitor named WKYMVM, which can restore sensitivity to CDK4/6i in CDK4/6i-resistant breast cancer cells, was identified. Treatment with folate-conjugated liposomes targeting breast cancer cells that contained both a CDK4/6i and WKYMVM revealed the synergistic effect of METTL14 inhibition with CDK4/6i therapy in a CDK4/6i-resistant PDX model. Together, our findings reveal the mechanism of CDK4/6i resistance and provide a strategy for overcoming CDK4/6i resistance via METTL14 inhibition.

Keywords: Breast cancer; METTL14; RNA modification; m6A.

MeSH terms

  • Animals
  • Breast Neoplasms* / drug therapy
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / metabolism
  • Cell Line, Tumor
  • Cyclin-Dependent Kinase 4* / antagonists & inhibitors
  • Cyclin-Dependent Kinase 4* / metabolism
  • Cyclin-Dependent Kinase 6* / antagonists & inhibitors
  • Cyclin-Dependent Kinase 6* / metabolism
  • Drug Resistance, Neoplasm* / drug effects
  • E2F1 Transcription Factor* / genetics
  • E2F1 Transcription Factor* / metabolism
  • Estrogen Receptor alpha / metabolism
  • Female
  • Humans
  • Methyltransferases* / metabolism
  • Mice
  • Mice, Nude
  • Protein Kinase Inhibitors / pharmacology

Substances

  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6
  • Methyltransferases
  • E2F1 Transcription Factor
  • METTL14 protein, human
  • CDK6 protein, human
  • Estrogen Receptor alpha
  • CDK4 protein, human
  • E2F1 protein, human
  • Protein Kinase Inhibitors
  • ESR1 protein, human