The Alkylating Chemotherapeutic Temozolomide Induces Metabolic Stress in IDH1-Mutant Cancers and Potentiates NAD+ Depletion-Mediated Cytotoxicity

Cancer Res. 2017 Aug 1;77(15):4102-4115. doi: 10.1158/0008-5472.CAN-16-2263. Epub 2017 Jun 16.

Abstract

IDH1-mutant gliomas are dependent upon the canonical coenzyme NAD+ for survival. It is known that PARP activation consumes NAD+ during base excision repair (BER) of chemotherapy-induced DNA damage. We therefore hypothesized that a strategy combining NAD+ biosynthesis inhibitors with the alkylating chemotherapeutic agent temozolomide could potentiate NAD+ depletion-mediated cytotoxicity in mutant IDH1 cancer cells. To investigate the impact of temozolomide on NAD+ metabolism, patient-derived xenografts and engineered mutant IDH1-expressing cell lines were exposed to temozolomide, in vitro and in vivo, both alone and in combination with nicotinamide phosphoribosyltransferase (NAMPT) inhibitors, which block NAD+ biosynthesis. The acute time period (<3 hours) after temozolomide treatment displayed a burst of NAD+ consumption driven by PARP activation. In IDH1-mutant-expressing cells, this consumption reduced further the abnormally lowered basal steady-state levels of NAD+, introducing a window of hypervulnerability to NAD+ biosynthesis inhibitors. This effect was selective for IDH1-mutant cells and independent of methylguanine methyltransferase or mismatch repair status, which are known rate-limiting mediators of adjuvant temozolomide genotoxic sensitivity. Combined temozolomide and NAMPT inhibition in an in vivo IDH1-mutant cancer model exhibited enhanced efficacy compared with each agent alone. Thus, we find IDH1-mutant cancers have distinct metabolic stress responses to chemotherapy-induced DNA damage and that combination regimens targeting nonredundant NAD+ pathways yield potent anticancer efficacy in vivo Such targeting of convergent metabolic pathways in genetically selected cancers could minimize treatment toxicity and improve durability of response to therapy. Cancer Res; 77(15); 4102-15. ©2017 AACR.

MeSH terms

  • Acrylamides / pharmacology
  • Animals
  • Antineoplastic Agents, Alkylating / pharmacology*
  • Cell Line, Tumor
  • Dacarbazine / analogs & derivatives*
  • Dacarbazine / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Female
  • Glioma / genetics
  • Glioma / metabolism*
  • Humans
  • Isocitrate Dehydrogenase / genetics
  • Mice
  • Mice, SCID
  • Mutation
  • NAD
  • Nicotinamide Phosphoribosyltransferase / antagonists & inhibitors
  • Piperidines / pharmacology
  • Random Allocation
  • Stress, Physiological / drug effects*
  • Temozolomide
  • Xenograft Model Antitumor Assays

Substances

  • Acrylamides
  • Antineoplastic Agents, Alkylating
  • Enzyme Inhibitors
  • N-(4-(1-benzoylpiperidin-4-yl)butyl)-3-(pyridin-3-yl)acrylamide
  • Piperidines
  • NAD
  • Dacarbazine
  • Isocitrate Dehydrogenase
  • IDH1 protein, human
  • Nicotinamide Phosphoribosyltransferase
  • Temozolomide