IDH1 Reprograms Nucleotide Metabolism by Inducing Chromatin Remodeling and DHODH Transcription to Drive Chemoresistance in Nasopharyngeal Carcinoma

Cancer Res. 2026 Apr 15;86(8):2004-2023. doi: 10.1158/0008-5472.CAN-25-2313.

Abstract

Metabolic reprogramming under therapeutic stress may represent a targetable vulnerability for cancer treatment. Elucidation of the metabolic alterations linked to chemotherapy in nasopharyngeal carcinoma (NPC) could uncover potential therapeutic strategies. Using proteomics and transcriptomic profiles, we identified wild-type (WT) isocitrate dehydrogenase 1 (IDH1) as a crucial metabolic enzyme upregulated in gemcitabine plus cisplatin (GP) chemotherapy-resistant NPC. IDH1 reprogrammed nucleotide metabolism in response to chemotherapy, linking DNA damage repair (DDR) to ferroptosis resistance via dihydroorotate dehydrogenase (DHODH), thereby contributing to chemoresistance in NPC. Mechanistically, α-ketoglutarate (αKG), a metabolite of IDH1, enhanced chromatin accessibility to promote DHODH transcription via αKG-dependent dioxygenase AlkB homolog 5 (ALKBH5)-recruited heterogeneous nuclear ribonucleoprotein C (HNRNPC). The DHODH inhibitor BAY2402234 markedly sensitized NPC cells to chemotherapy. Clinically, a prognostic model based on DDR and ferroptosis signatures effectively predicted disease relapse risk following chemotherapy in NPC. This study links DDR to ferroptosis defense via the IDH1/αKG/ALKBH5/DHODH axis, suggesting DHODH inhibition as a promising therapeutic strategy to overcome chemoresistance in tumors harboring WT IDH1.

Significance: DHODH-mediated nucleotide metabolic reprogramming represents a targetable vulnerability to counteract chemoresistance in nasopharyngeal carcinoma with wild-type IDH1 overexpression.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Chromatin Assembly and Disassembly*
  • Cisplatin / pharmacology
  • DNA Repair
  • Deoxycytidine / analogs & derivatives
  • Deoxycytidine / pharmacology
  • Dihydroorotate Dehydrogenase
  • Drug Resistance, Neoplasm* / genetics
  • Ferroptosis / drug effects
  • Gemcitabine
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Isocitrate Dehydrogenase* / genetics
  • Isocitrate Dehydrogenase* / metabolism
  • Mice
  • Mice, Nude
  • Nasopharyngeal Carcinoma* / drug therapy
  • Nasopharyngeal Carcinoma* / genetics
  • Nasopharyngeal Carcinoma* / metabolism
  • Nasopharyngeal Carcinoma* / pathology
  • Nasopharyngeal Neoplasms* / drug therapy
  • Nasopharyngeal Neoplasms* / genetics
  • Nasopharyngeal Neoplasms* / metabolism
  • Nasopharyngeal Neoplasms* / pathology
  • Oxidoreductases Acting on CH-CH Group Donors* / genetics
  • Oxidoreductases Acting on CH-CH Group Donors* / metabolism
  • Prognosis
  • Xenograft Model Antitumor Assays

Substances

  • Isocitrate Dehydrogenase
  • Dihydroorotate Dehydrogenase
  • IDH1 protein, human
  • Cisplatin
  • Oxidoreductases Acting on CH-CH Group Donors
  • Deoxycytidine
  • Gemcitabine