KDM1A/LSD1 inhibition enhances chemotherapy response in ovarian cancer

Mol Carcinog. 2024 Oct;63(10):2026-2039. doi: 10.1002/mc.23792. Epub 2024 Jul 11.

Abstract

Ovarian cancer (OCa) is the deadliest of all gynecological cancers. The standard treatment for OCa is platinum-based chemotherapy, such as carboplatin or cisplatin in combination with paclitaxel. Most patients are initially responsive to these treatments; however, nearly 90% will develop recurrence and inevitably succumb to chemotherapy-resistant disease. Recent studies have revealed that the epigenetic modifier lysine-specific histone demethylase 1A (KDM1A/LSD1) is highly overexpressed in OCa. However, the role of KDM1A in chemoresistance and whether its inhibition enhances chemotherapy response in OCa remains uncertain. Analysis of TCGA datasets revealed that KDM1A expression is high in patients who poorly respond to chemotherapy. Western blot analysis show that treatment with chemotherapy drugs cisplatin, carboplatin, and paclitaxel increased KDM1A expression in OCa cells. KDM1A knockdown (KD) or treatment with KDM1A inhibitors NCD38 and SP2509 sensitized established and patient-derived OCa cells to chemotherapy drugs in reducing cell viability and clonogenic survival and inducing apoptosis. Moreover, knockdown of KDM1A sensitized carboplatin-resistant A2780-CP70 cells to carboplatin treatment and paclitaxel-resistant SKOV3-TR cells to paclitaxel. RNA-seq analysis revealed that a combination of KDM1A-KD and cisplatin treatment resulted in the downregulation of genes related to epithelial-mesenchymal transition (EMT). Interestingly, cisplatin treatment increased a subset of NF-κB pathway genes, and KDM1A-KD or KDM1A inhibition reversed this effect. Importantly, KDM1A-KD, in combination with cisplatin, significantly reduced tumor growth compared to a single treatment in an orthotopic intrabursal OCa xenograft model. Collectively, these findings suggest that combination of KDM1A inhibitors with chemotherapy could be a promising therapeutic approach for the treatment of OCa.

Keywords: KDM1A; LSD1; chemotherapy; ovarian cancer.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • Apoptosis / drug effects
  • Carboplatin* / pharmacology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cisplatin* / pharmacology
  • Drug Resistance, Neoplasm* / drug effects
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Histone Demethylases* / antagonists & inhibitors
  • Histone Demethylases* / genetics
  • Histone Demethylases* / metabolism
  • Humans
  • Hydrazines
  • Mice
  • Mice, Nude
  • Ovarian Neoplasms* / drug therapy
  • Ovarian Neoplasms* / genetics
  • Ovarian Neoplasms* / metabolism
  • Ovarian Neoplasms* / pathology
  • Paclitaxel* / pharmacology
  • Sulfonamides
  • Xenograft Model Antitumor Assays*

Substances

  • Histone Demethylases
  • KDM1A protein, human
  • Paclitaxel
  • Cisplatin
  • Carboplatin
  • SP2509
  • Antineoplastic Agents
  • Hydrazines
  • Sulfonamides