Identification of natural compound garcinone E as a novel autophagic flux inhibitor with anticancer effect in nasopharyngeal carcinoma cells

Pharm Biol. 2023 Dec;61(1):839-857. doi: 10.1080/13880209.2023.2210187.

Abstract

Context: Current chemotherapeutic drugs cannot meet the treatment needs of patients with nasopharyngeal carcinoma (NPC), so urgent action is needed to discover novel chemotherapeutic agents. Our previous study revealed that garcinone E (GE) inhibited the proliferation and metastasis of NPC, suggesting that the compound might display promising anticancer activity.

Objective: To examine the mechanism underlying the anti-NPC activity of GE for the first time.

Materials and methods: For MTS assay, NPC cells were treated with 2.5-20 μmol/L GE or dimethyl sulfoxide for 24, 48, and 72 h. Colony formation capacity, cell cycle distribution, and in vivo xenograft experiment of GE were assessed. MDC staining, StubRFP-sensGFP-LC3 observation, LysoBrite Blue staining, and immunofluorescence examined the autophagy of NPC cells after GE exposure. Western blotting, RNA-sequencing, and RT-qPCR measured protein and mRNA levels.

Results: GE suppressed cell viability with an IC50 of 7.64, 8.83 and 4.65 μmol/L for HK1, HONE1 and S18 cells. GE inhibited colony formation and cell cycle, increased autophagosome number, and inhibited the autophagic flux partially by blocking lysosome-autophagosome fusion, and repressed S18 xenograft growth. GE dysregulated the expression of autophagy- and cell cycle-related proteins such as Beclin-1, SQSTM1/p62, LC3, CDKs, and Cyclins. Bioinformatics GO and KEGG pathway enrichment analysis of RNA-seq showed that autophagy was enriched in differentially expressed genes upon GE treatment.

Discussion and conclusion: GE acts as an autophagic flux inhibitor, which may have potential chemotherapeutic use for NPC treatment and may have an application in basic research to explore the mechanisms of autophagy.

Keywords: Autophagy; KEGG pathway enrichment; RNA-seq; autophagosome; cell cycle arrest.

MeSH terms

  • Apoptosis*
  • Autophagy
  • Cell Line, Tumor
  • Cell Proliferation
  • Humans
  • Nasopharyngeal Carcinoma / drug therapy
  • Nasopharyngeal Carcinoma / metabolism
  • Nasopharyngeal Neoplasms* / drug therapy
  • Nasopharyngeal Neoplasms* / metabolism
  • Nasopharyngeal Neoplasms* / pathology

Substances

  • garcinone E

Grants and funding

This work was supported by the National Natural Science Foundation of China (Grant No. 82260721, 81903644, 81660606 and 81860458), Guangxi Natural Science Foundation (Grant No. 2018GXNSFAA281227 and 2021GXNSFAA075002), Advanced Innovation Teams and Xinghu Scholars Program of Guangxi Medical University (No. 24/02304001018X), and Innovation Project of Guangxi Graduate Education (No. YCSW2022215).