YY1 downregulation underlies therapeutic response to molecular targeted agents

Cell Death Dis. 2024 Nov 27;15(11):862. doi: 10.1038/s41419-024-07239-8.

Abstract

During targeted treatment, oncogene-addicted tumor cells often evolve from an initial drug-sensitive state through a drug-tolerant persister bottleneck toward the ultimate emergence of drug-resistant clones. The molecular basis underlying this therapy-induced evolutionary trajectory has not yet been completely elucidated. Here, we employed a multifaceted approach and implicated the convergent role of transcription factor Yin Yang 1 (YY1) in the course of diverse targeted kinase inhibitors. Specifically, pharmacological perturbation of the receptor tyrosine kinase (RTK)/mitogen-activated protein kinase (MAPK) pathway resulted in the downregulation of YY1 transcription, which subsequently resumed upon therapeutic escape. Failure to decrease YY1 subverted cytotoxic effects, whereas elimination of residual YY1 maximized anticancer efficacy and forestalled the emergence of drug resistance. Mechanistically, YY1 was uncovered to dictate cell cycle and autophagic programs. Immunohistochemical analysis on a wide spectrum of clinical specimens revealed that YY1 was ubiquitously expressed across lung adenocarcinomas and exhibited anticipated fluctuation in response to corresponding RTK/MAPK inhibition. These findings advance our understanding of targeted cancer management by highlighting YY1 as a determinant node in the context of genotype-directed agents.

MeSH terms

  • Adenocarcinoma of Lung / drug therapy
  • Adenocarcinoma of Lung / genetics
  • Adenocarcinoma of Lung / metabolism
  • Adenocarcinoma of Lung / pathology
  • Animals
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use
  • Autophagy / drug effects
  • Cell Line, Tumor
  • Down-Regulation* / drug effects
  • Down-Regulation* / genetics
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / genetics
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / pathology
  • Mice
  • Molecular Targeted Therapy
  • Protein Kinase Inhibitors / pharmacology
  • Protein Kinase Inhibitors / therapeutic use
  • YY1 Transcription Factor* / genetics
  • YY1 Transcription Factor* / metabolism

Substances

  • YY1 Transcription Factor
  • YY1 protein, human
  • Protein Kinase Inhibitors
  • Antineoplastic Agents