Curcumin derivative C210 induces Epstein-Barr virus lytic cycle and inhibits virion production by disrupting Hsp90 function

Sci Rep. 2024 Nov 4;14(1):26694. doi: 10.1038/s41598-024-77294-w.

Abstract

Lytic induction therapy was devised to selectively combat malignancies associated with Epstein-Barr virus (EBV) by triggering viral reactivation from latency. At present, the major challenges of lytic induction therapy are to maximize reactivating efficiencies and meanwhile minimize infectious virion production. C210, a novel curcumin derivative with potent Hsp90 inhibitory activity, was explored for EBV-reactivating and virion-producing effects in EBV-positive nasopharyngeal carcinoma (NPC) and gastric carcinoma (GC) cell lines. And the molecular mechanisms underlying these effects were determined. Follow C210 treatment, EBV lytic RNAs and proteins were upregulated, but infectious virions were not produced. Knockdown of heat shock protein 90 (Hsp90) induced expression of lytic RNAs and proteins, and diminished C210-driven EBV lytic induction. Pretreatment with an X box binding protein 1 (XBP1) inhibitor reduced C210-induced EBV lytic RNA. Furthermore, we demonstrated that C210 inhibited the binding of Hsp90 with its clients, signal transducer and activator of transcription 3 (STAT3) and xeroderma pigmentosum group B-complementing protein (XPB), which subsequently promoted their proteasomal degradation. Degradation of STAT3 by C210 enhanced the EBV-reactivating and anticancer capacity of suberoylanilide hydroxamic acid (SAHA). Depletion of XPB blocked SAHA-induced expression of late viral genes and production of infectious virions. These results elucidate a novel Hsp90 inhibitor targeting EBV lytic phase and extend the research on lytic induction strategy, which may offer reference value in the treatment of EBV-positive malignancies.

Keywords: Curcumin derivative; Epstein–Barr virus; Gastric carcinoma; Hsp90 inhibitor; Lytic induction therapy; Nasopharyngeal carcinoma.

MeSH terms

  • Cell Line, Tumor
  • Curcumin* / analogs & derivatives
  • Curcumin* / pharmacology
  • Epstein-Barr Virus Infections / drug therapy
  • Epstein-Barr Virus Infections / metabolism
  • Epstein-Barr Virus Infections / virology
  • HSP90 Heat-Shock Proteins* / antagonists & inhibitors
  • HSP90 Heat-Shock Proteins* / metabolism
  • Herpesvirus 4, Human* / drug effects
  • Herpesvirus 4, Human* / physiology
  • Humans
  • Nasopharyngeal Carcinoma / drug therapy
  • Nasopharyngeal Carcinoma / metabolism
  • Nasopharyngeal Carcinoma / virology
  • Nasopharyngeal Neoplasms / drug therapy
  • Nasopharyngeal Neoplasms / metabolism
  • Nasopharyngeal Neoplasms / virology
  • STAT3 Transcription Factor* / metabolism
  • Stomach Neoplasms / drug therapy
  • Stomach Neoplasms / metabolism
  • Stomach Neoplasms / virology
  • Virion* / drug effects
  • Virion* / metabolism
  • Virus Activation* / drug effects
  • Virus Replication / drug effects
  • Vorinostat / pharmacology

Substances

  • HSP90 Heat-Shock Proteins
  • Curcumin
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Vorinostat