Combinatorial targeting of glutamine metabolism and lysosomal-based lipid metabolism effectively suppresses glioblastoma

Cell Rep Med. 2024 Sep 17;5(9):101706. doi: 10.1016/j.xcrm.2024.101706. Epub 2024 Sep 4.

Abstract

Antipsychotic drugs have been shown to have antitumor effects but have had limited potency in the clinic. Here, we unveil that pimozide inhibits lysosome hydrolytic function to suppress fatty acid and cholesterol release in glioblastoma (GBM), the most lethal brain tumor. Unexpectedly, GBM develops resistance to pimozide by boosting glutamine consumption and lipogenesis. These elevations are driven by SREBP-1, which we find upregulates the expression of ASCT2, a key glutamine transporter. Glutamine, in turn, intensifies SREBP-1 activation through the release of ammonia, creating a feedforward loop that amplifies both glutamine metabolism and lipid synthesis, leading to drug resistance. Disrupting this loop via pharmacological targeting of ASCT2 or glutaminase, in combination with pimozide, induces remarkable mitochondrial damage and oxidative stress, leading to GBM cell death in vitro and in vivo. Our findings underscore the promising therapeutic potential of effectively targeting GBM by combining glutamine metabolism inhibition with lysosome suppression.

Keywords: ASCT2; GLS; SREBP-1; cholesterol; fatty acids; glioblastoma; glutamine; lipid droplets; lysosome; pimozide.

MeSH terms

  • Amino Acid Transport System ASC / genetics
  • Amino Acid Transport System ASC / metabolism
  • Animals
  • Brain Neoplasms / drug therapy
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology
  • Cell Line, Tumor
  • Glioblastoma* / drug therapy
  • Glioblastoma* / genetics
  • Glioblastoma* / metabolism
  • Glioblastoma* / pathology
  • Glutaminase / antagonists & inhibitors
  • Glutaminase / genetics
  • Glutaminase / metabolism
  • Glutamine* / metabolism
  • Humans
  • Lipid Metabolism* / drug effects
  • Lipogenesis / drug effects
  • Lysosomes* / drug effects
  • Lysosomes* / metabolism
  • Mice
  • Minor Histocompatibility Antigens
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Oxidative Stress / drug effects
  • Sterol Regulatory Element Binding Protein 1 / genetics
  • Sterol Regulatory Element Binding Protein 1 / metabolism

Substances

  • Glutamine
  • Amino Acid Transport System ASC
  • Sterol Regulatory Element Binding Protein 1
  • SLC1A5 protein, human
  • Glutaminase
  • SREBF1 protein, human
  • Minor Histocompatibility Antigens