Pharmacological inhibition of noncanonical EED-EZH2 signaling overcomes chemoresistance in prostate cancer

Theranostics. 2021 May 8;11(14):6873-6890. doi: 10.7150/thno.49235. eCollection 2021.

Abstract

Rationale: Chemoresistance is a major obstacle in prostate cancer (PCa) treatment. We sought to understand the underlying mechanism of PCa chemoresistance and discover new treatments to overcome docetaxel resistance. Methods: We developed a novel phenotypic screening platform for the discovery of specific inhibitors of chemoresistant PCa cells. The mechanism of action of the lead compound was investigated using computational, molecular and cellular approaches. The in vivo toxicity and efficacy of the lead compound were evaluated in clinically-relevant animal models. Results: We identified LG1980 as a lead compound that demonstrates high selectivity and potency against chemoresistant PCa cells. Mechanistically, LG1980 binds embryonic ectoderm development (EED), disrupts the interaction between EED and enhancer of zeste homolog 2 (EZH2), thereby inducing the protein degradation of EZH2 and inhibiting the phosphorylation and activity of EZH2. Consequently, LG1980 targets a survival signaling cascade consisting of signal transducer and activator of transcription 3 (Stat3), S-phase kinase-associated protein 2 (SKP2), ATP binding cassette B 1 (ABCB1) and survivin. As a lead compound, LG1980 is well tolerated in mice and effectively suppresses the in vivo growth of chemoresistant PCa and synergistically enhances the efficacy of docetaxel in xenograft models. Conclusions: These results indicate that pharmacological inhibition of EED-EZH2 interaction is a novel strategy for the treatment of chemoresistant PCa. LG1980 and its analogues have the potential to be integrated into standard of care to improve clinical outcomes in PCa patients.

Keywords: EED inhibitor; EZH2 signaling; chemoresistance; drug discovery; prostate cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily B / metabolism
  • Animals
  • Antineoplastic Agents / chemistry*
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • Bone Neoplasms / drug therapy*
  • Bone Neoplasms / metabolism
  • Bone Neoplasms / secondary
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Docetaxel / pharmacology
  • Docetaxel / therapeutic use
  • Drug Discovery / methods*
  • Drug Resistance, Neoplasm*
  • Drug Synergism
  • Enhancer of Zeste Homolog 2 Protein / metabolism*
  • Humans
  • Inhibitory Concentration 50
  • Male
  • Mice
  • Polycomb Repressive Complex 2 / antagonists & inhibitors*
  • Polycomb Repressive Complex 2 / chemistry
  • Polycomb Repressive Complex 2 / metabolism
  • Prostatic Neoplasms / drug therapy*
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology
  • S-Phase Kinase-Associated Proteins / metabolism
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction / drug effects
  • Survivin / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • ABCB1 protein, human
  • ATP Binding Cassette Transporter, Subfamily B
  • Antineoplastic Agents
  • EED protein, human
  • S-Phase Kinase-Associated Proteins
  • SKP2 protein, human
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Survivin
  • Docetaxel
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • Polycomb Repressive Complex 2