SSRI antidepressant citalopram reverses the Warburg effect to inhibit hepatocellular carcinoma by directly targeting GLUT1

Cell Rep. 2024 Oct 22;43(10):114818. doi: 10.1016/j.celrep.2024.114818. Epub 2024 Oct 9.

Abstract

Selective serotonin reuptake inhibitors (SSRIs) have shown promise in cancer therapy, particularly for hepatocellular carcinoma (HCC), but their molecular targets and mechanisms remain unclear. Here, we show that SSRIs exhibit significant anti-HCC effects independent of their classical target, the serotonin reuptake transporter (SERT). Using global inverse gene expression profiling, drug affinity responsive target stability assays, and in silico molecular docking, we demonstrate that citalopram targets glucose transporter 1 (GLUT1), resulting in reduced glycolytic flux. A mutant GLUT1 variant at the citalopram binding site (E380) diminishes the drug's inhibitory effects on the Warburg effect and tumor growth. In preclinical models, citalopram dampens the growth of GLUT1high liver tumors and displays a synergistic effect with anti-PD-1 therapy. Retrospective analysis reveals that SSRI use correlates with a lower risk of metastasis among patients with HCC. Our study describes a role for SSRIs in cancer metabolism, establishing a rationale for their repurposing as potential anti-cancer drugs for HCC.

Keywords: CP: Cancer; SERT; SLC6A4; aerobic glycolysis; drug discovery; drug repurposing.

MeSH terms

  • Animals
  • Antidepressive Agents / pharmacology
  • Carcinoma, Hepatocellular* / drug therapy
  • Carcinoma, Hepatocellular* / metabolism
  • Carcinoma, Hepatocellular* / pathology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Citalopram* / pharmacology
  • Glucose Transporter Type 1* / genetics
  • Glucose Transporter Type 1* / metabolism
  • Humans
  • Liver Neoplasms* / drug therapy
  • Liver Neoplasms* / metabolism
  • Liver Neoplasms* / pathology
  • Male
  • Mice
  • Mice, Nude
  • Selective Serotonin Reuptake Inhibitors* / pharmacology
  • Warburg Effect, Oncologic / drug effects

Substances

  • Selective Serotonin Reuptake Inhibitors
  • Citalopram
  • Glucose Transporter Type 1
  • SLC2A1 protein, human
  • Antidepressive Agents