Targeting and degradation of OTUB1 by Erianin for antimetastasis in esophageal squamous cell carcinoma

Phytomedicine. 2024 Dec:135:155969. doi: 10.1016/j.phymed.2024.155969. Epub 2024 Aug 19.

Abstract

Background: Metastasis is a major contributor to mortality in patients with esophageal squamous cell carcinoma (ESCC); effective treatment is currently lacking. Erianin, a bioactive ingredient of traditional Chinese medicine, Dendrobium chrysotoxum, has anti-tumor activity against multiple human tumors. However, the effect and associated underlying mechanism of Erianin on ESCC antimetastasis remain unclear.

Purpose: To investigate the anti-metastatic properties of Erianin in ESCC both in vitro and in vivo and associated molecular mechanisms.

Methods: Wound healing assay, Transwell assay, CCK-8 assay, immunohistochemistry, and lung metastasis mouse model were carried out to examine ESCC cell migration and viability in vitro and in vivo. Drug affinity responsive target stability (DARTS), cellular thermal migration assay (CETSA), molecular docking, and Surface plasmon resonance (SPR) assay were used to confirm Erianin binding to ovarian tumor ubiquitin aldehyde-binding protein 1 (OTUB1) protein. Protein stability assay, cell transfection, and western blotting were used to confirm Erianin-mediated degradation of OTUB1 and Snail via the ubiquitin-proteasome pathway. qRT-PCR and western blotting were used to assess OTUB1expression in ESCC tissues.

Results: Erianin suppressed the migration/invasion of ESCC cells without modulating cell viability in vitro and in vivo, bound to OTUB1 through DARTS, CETSA, and molecular docking, and SPR assay, and enhanced OTUB1 degradation via the ubiquitin-proteasome system. Moreover, Erianin inhibited the ESCC epithelial-mesenchymal transition by enhancing the ubiquitination and degradation of Snail via targeting OTUB1.

Conclusion: Erianin inhibited ESCC metastasis through ubiquitination and degradation of Snail via targeting OTUB1. Our findings suggest Erianin as a novel OTUB1 inhibitor for preventing ESCC metastasis.

Keywords: Erianin; Esophageal squamous cell carcinoma; Metastasis; Ovarian tumor ubiquitin aldehyde-binding protein 1; Snail.

MeSH terms

  • Animals
  • Antineoplastic Agents, Phytogenic / pharmacology
  • Bibenzyls / pharmacology
  • Cell Line, Tumor
  • Cell Movement* / drug effects
  • Deubiquitinating Enzymes* / metabolism
  • Epithelial-Mesenchymal Transition / drug effects
  • Esophageal Neoplasms* / drug therapy
  • Esophageal Neoplasms* / metabolism
  • Esophageal Neoplasms* / pathology
  • Esophageal Squamous Cell Carcinoma* / drug therapy
  • Esophageal Squamous Cell Carcinoma* / metabolism
  • Esophageal Squamous Cell Carcinoma* / pathology
  • Female
  • Humans
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / secondary
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Molecular Docking Simulation
  • Phenol / pharmacology
  • Snail Family Transcription Factors / metabolism

Substances

  • Erianin
  • Deubiquitinating Enzymes
  • OTUB1 protein, human
  • Bibenzyls
  • Snail Family Transcription Factors
  • Phenol
  • Antineoplastic Agents, Phytogenic