Design, synthesis, and biological evaluation of N1-(2-(adamantan-1-yl)-1H-indol-5-yl)-N2-(substituent)-1,2-dicarboxamides as anticancer agents targeting Nur77-mediated endoplasmic reticulum stress

Bioorg Chem. 2025 Feb:155:108113. doi: 10.1016/j.bioorg.2024.108113. Epub 2024 Dec 30.

Abstract

Targeting endoplasmic reticulum (ER) stress-induced apoptosis has attracted considerable research interest in anti-cancer drug development. Nur77 is a potential therapeutic target in many cancers and several Nur77 modulators have recently been identified as effective anticancer agents by activating ER stress. As an ongoing work, this study reports a new series of novel N1-(2-(adamantan-1-yl)-1H-indol-5-yl)-N2-(substituent)-1,2-dicarboxamides as potent Nur77 modulators that cause ER stress-induced apoptosis. Among this new series, most compounds show improved cytotoxicity against liver cancer (HepG2 and Huh7) and breast cancer (MCF-7 and MDA-MB-231) cell lines. The representative analog 15h dramatically induces Nur77 expression and cell apoptosis, showing excellent growth inhibition of HepG2 and MCF-7 cells (IC50 < 5.0 μM). Mechanistically, 15h binds (KD = 0.477 μM) and activates Nur77-mediated ER stress through the PERK-ATF4 and IRE1 signaling pathways, thereby inducing cell apoptosis. In vivo, 15h treatment strongly suppresses HepG2 xenograft tumor growth (tumor shrink by 54.06 %). In summary, we synthesize a series of novel indole derivatives, among which 15h has significantly improved pharmacological activity against various cancer cells. We further identify 15h as a novel ligand of Nur77, which may serve a therapeutic lead for developing new cancer therapy.

Keywords: Anticancer activity; Apoptosis; Endoplasmic reticulum stress; Indole derivatives; Nur77; Target identification.

MeSH terms

  • Animals
  • Antineoplastic Agents* / chemical synthesis
  • Antineoplastic Agents* / chemistry
  • Antineoplastic Agents* / pharmacology
  • Apoptosis* / drug effects
  • Cell Line, Tumor
  • Cell Proliferation* / drug effects
  • Dose-Response Relationship, Drug
  • Drug Design*
  • Drug Screening Assays, Antitumor*
  • Endoplasmic Reticulum Stress* / drug effects
  • Humans
  • Indoles / chemical synthesis
  • Indoles / chemistry
  • Indoles / pharmacology
  • Mice
  • Mice, Nude
  • Molecular Structure
  • Nuclear Receptor Subfamily 4, Group A, Member 1* / antagonists & inhibitors
  • Nuclear Receptor Subfamily 4, Group A, Member 1* / metabolism
  • Structure-Activity Relationship

Substances

  • Antineoplastic Agents
  • Nuclear Receptor Subfamily 4, Group A, Member 1
  • NR4A1 protein, human
  • Indoles