Targeting the mevalonate pathway enhances the efficacy of 5-fluorouracil by regulating pyroptosis

Med Oncol. 2024 Nov 20;42(1):9. doi: 10.1007/s12032-024-02557-5.

Abstract

The 5-fluorouracil (5-FU)-based chemotherapy regimen is a primary strategy for treating pancreatic cancer (PC). However, challenges related to 5-FU resistance persist. Investigating the mechanisms of 5-FU resistance and identifying a clinically viable therapeutic strategy are crucial for improving the prognosis of PC. Here, through clinical samples analysis, we found that the expression of 3-hydroxy-3-methylglutaryl coenzyme A reductase (HMGCR), the rate-limiting enzyme in mevalonate metabolism, is negatively correlated with the efficacy of 5-FU treatment. There is a significant correlation between HMGCR and the pyroptosis marker gasdermin D (GSDMD), and the HMGCR inhibitor simvastatin can significantly inhibit the activation of pyroptosis signaling. The exogenous addition of geranylgeranyl pyrophosphate (GGPP), a key metabolite of the mevalonate pathway, can significantly reduce sensitivity to 5-FU, and simvastatin combined with 5-FU demonstrates a strong synergistic effect. Furthermore, in organoid models and genetically engineered mice with spontaneous PC, the combination of simvastatin and 5-FU significantly inhibits tumor growth. In conclusion, our study reveals the critical role of the mevalonate pathway in 5-FU resistance and proposes a clinically feasible combination therapy strategy.

Keywords: 5-Fluorouracil; Chemoresistance; Mevalonate pathway; Pancreatic cancer; Pyroptosis.

MeSH terms

  • Animals
  • Antimetabolites, Antineoplastic / pharmacology
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm / drug effects
  • Drug Synergism
  • Female
  • Fluorouracil* / pharmacology
  • Humans
  • Hydroxymethylglutaryl CoA Reductases / metabolism
  • Hydroxymethylglutaryl-CoA Reductase Inhibitors / pharmacology
  • Male
  • Mevalonic Acid* / metabolism
  • Mice
  • Pancreatic Neoplasms* / drug therapy
  • Pancreatic Neoplasms* / metabolism
  • Pancreatic Neoplasms* / pathology
  • Polyisoprenyl Phosphates / metabolism
  • Polyisoprenyl Phosphates / pharmacology
  • Pyroptosis* / drug effects
  • Simvastatin / pharmacology

Substances

  • Fluorouracil
  • Mevalonic Acid
  • Simvastatin
  • geranylgeranyl pyrophosphate
  • Hydroxymethylglutaryl CoA Reductases
  • Polyisoprenyl Phosphates
  • Antimetabolites, Antineoplastic
  • HMGCR protein, human
  • Hydroxymethylglutaryl-CoA Reductase Inhibitors