Multi-Omics Exploration of the Mechanism of Curcumol to Reduce Invasion and Metastasis of Nasopharyngeal Carcinoma by Inhibiting NCL/EBNA1-Mediated UBE2C Upregulation

Biomolecules. 2024 Sep 9;14(9):1142. doi: 10.3390/biom14091142.

Abstract

Nasopharyngeal carcinoma (NPC) is closely linked to Epstein-Barr virus (EBV) infection. Curcumae Rhizoma, a traditional Chinese herb, has shown antitumor effects, primarily through its component curcumol (Cur), which has been shown to reduce NPC cell invasion and migration by targeting nucleolin (NCL) and Epstein-Barr Virus Nuclear Antigen 1 (EBNA1). We constructed an EBV-positive NPC cell model using C666-1 cells and performed transcriptomics studies after treatment with curcumol, which revealed a significant enrichment of ubiquitin-mediated proteolysis, the PI3K-AKT and mTOR signaling pathways, cell cycle and apoptosis involved in tumor invasion and migration. To investigate the importance of NCL and EBNA1 in curcumol-resistant EBV-positive NPC, we performed a multi-omics study using short hairpin NCL (shNCL) and shEBNA1 EBV-positive NPC cells, and the proteomics results showed enrichment in complement and coagulation cascades and ubiquitin-mediated proteolysis signaling pathways. Here, we focused on ubiquitin-conjugating enzyme E2C (UBE2C), which plays an important role in the ubiquitin-mediated proteolysis signaling pathway. In addition, metabolomics revealed that UBE2C is highly associated with 4-Aminobutanoic acid (GABA). In vitro studies further validated the function of the key targets, suggesting that UBE2C plays an important role in NCL and EBNA1-mediated curcumol resistance to nasopharyngeal carcinoma invasion and metastasis.

Keywords: EBNA1; NCL; UBE2C; curcumol; metabolomics; nasopharyngeal carcinoma; proteomics; transcriptomics.

MeSH terms

  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Epstein-Barr Virus Nuclear Antigens* / genetics
  • Epstein-Barr Virus Nuclear Antigens* / metabolism
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Multiomics
  • Nasopharyngeal Carcinoma* / drug therapy
  • Nasopharyngeal Carcinoma* / genetics
  • Nasopharyngeal Carcinoma* / metabolism
  • Nasopharyngeal Carcinoma* / pathology
  • Nasopharyngeal Carcinoma* / virology
  • Nasopharyngeal Neoplasms* / drug therapy
  • Nasopharyngeal Neoplasms* / genetics
  • Nasopharyngeal Neoplasms* / metabolism
  • Nasopharyngeal Neoplasms* / pathology
  • Neoplasm Invasiveness
  • Neoplasm Metastasis / prevention & control
  • Nucleolin*
  • Phosphoproteins* / metabolism
  • Proteomics
  • RNA-Binding Proteins / metabolism
  • Sesquiterpenes* / chemistry
  • Sesquiterpenes* / pharmacology
  • Signal Transduction / drug effects
  • Ubiquitin-Conjugating Enzymes* / genetics
  • Ubiquitin-Conjugating Enzymes* / metabolism
  • Up-Regulation / drug effects

Substances

  • curcumol
  • Epstein-Barr Virus Nuclear Antigens
  • EBV-encoded nuclear antigen 1
  • Sesquiterpenes
  • Ubiquitin-Conjugating Enzymes
  • Nucleolin
  • Phosphoproteins
  • RNA-Binding Proteins