CBX4 counteracts cellular senescence to desensitize gastric cancer cells to chemotherapy by inducing YAP1 SUMOylation

Drug Resist Updat. 2024 Nov:77:101136. doi: 10.1016/j.drup.2024.101136. Epub 2024 Aug 12.

Abstract

Aims: As our comprehension of the intricate relationship between cellular senescence and tumor biology continues to evolve, the therapeutic potential of cellular senescence is gaining increasing recognition. Here, we identify chromobox 4 (CBX4), a Small Ubiquitin-related Modifier (SUMO) E3 ligase, as an antagonist of cellular senescence and elucidate a novel mechanism by which CBX4 promotes drug resistance and malignant progression of gastric cancer (GC).

Methods: In vitro and in vivo models were conducted to investigate the manifestation and impact of CBX4 on cellular senescence and chemoresistance. High-throughput sequencing, chromatin immunoprecipitation, and co-immunoprecipitation techniques were utilized to identify the upstream regulators and downstream effectors associated with CBX4, revealing its intricate regulatory network.

Results: CBX4 diminishes the sensitivity of GC cells to cellular senescence, facilitating chemoresistance and GC development by deactivating the senescence-related Hippo pathway. Mechanistically, low-dose cisplatin transcriptionally downregulates CBX4 through CEBPB. In addition, CBX4 preserves the stability and cytoplasm-nuclear transport of YAP1, the key player of Hippo pathway, by inducing SUMO1 modification at K97 and K280, which competitively inhibits YAP1-S127 phosphorylation.

Conclusions: Our study highlights the anti-senescence role of CBX4 and suggests that CBX4 inhibition in combination with low-dose cisplatin has the potential to overcome chemoresistance and effectively restrict GC progression.

Keywords: CBX4; Cellular senescence; Chemoresistance; Cisplatin; Hippo pathway; SUMOylation; YAP1.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Antineoplastic Agents / pharmacology
  • CCAAT-Enhancer-Binding Protein-beta / metabolism
  • Cell Line, Tumor
  • Cellular Senescence* / drug effects
  • Drug Resistance, Neoplasm* / drug effects
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Ligases
  • Mice
  • Polycomb-Group Proteins / genetics
  • Polycomb-Group Proteins / metabolism
  • Stomach Neoplasms* / drug therapy
  • Stomach Neoplasms* / metabolism
  • Stomach Neoplasms* / pathology
  • Sumoylation* / drug effects
  • Transcription Factors / metabolism
  • Xenograft Model Antitumor Assays
  • YAP-Signaling Proteins* / metabolism

Substances

  • CBX4 protein, human
  • YAP-Signaling Proteins
  • YAP1 protein, human
  • Antineoplastic Agents
  • CEBPB protein, human
  • Polycomb-Group Proteins
  • CCAAT-Enhancer-Binding Protein-beta
  • Adaptor Proteins, Signal Transducing
  • Transcription Factors
  • Ligases