Mitochondrial DNA alterations underlie an irreversible shift to aerobic glycolysis in fumarate hydratase-deficient renal cancer

Sci Signal. 2021 Jan 5;14(664):eabc4436. doi: 10.1126/scisignal.abc4436.

Abstract

Understanding the mechanisms of the Warburg shift to aerobic glycolysis is critical to defining the metabolic basis of cancer. Hereditary leiomyomatosis and renal cell carcinoma (HLRCC) is an aggressive cancer characterized by biallelic inactivation of the gene encoding the Krebs cycle enzyme fumarate hydratase, an early shift to aerobic glycolysis, and rapid metastasis. We observed impairment of the mitochondrial respiratory chain in tumors from patients with HLRCC. Biochemical and transcriptomic analyses revealed that respiratory chain dysfunction in the tumors was due to loss of expression of mitochondrial DNA (mtDNA)-encoded subunits of respiratory chain complexes, caused by a marked decrease in mtDNA content and increased mtDNA mutations. We demonstrated that accumulation of fumarate in HLRCC tumors inactivated the core factors responsible for replication and proofreading of mtDNA, leading to loss of respiratory chain components, thereby promoting the shift to aerobic glycolysis and disease progression in this prototypic model of glucose-dependent human cancer.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Carcinoma, Renal Cell / etiology
  • Carcinoma, Renal Cell / genetics*
  • Carcinoma, Renal Cell / metabolism
  • Citric Acid Cycle*
  • DNA Damage*
  • DNA Repair
  • DNA Replication
  • DNA, Mitochondrial / metabolism*
  • Female
  • Fumarate Hydratase / deficiency
  • Fumarate Hydratase / genetics*
  • Gene Expression Profiling
  • Humans
  • Kidney Neoplasms / etiology
  • Kidney Neoplasms / genetics*
  • Kidney Neoplasms / metabolism
  • Leiomyomatosis / complications
  • Leiomyomatosis / enzymology*
  • Male
  • Middle Aged
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Mutation
  • Neoplastic Syndromes, Hereditary / complications
  • Neoplastic Syndromes, Hereditary / enzymology*
  • Skin Neoplasms / complications
  • Skin Neoplasms / enzymology*
  • Uterine Neoplasms / complications
  • Uterine Neoplasms / enzymology*
  • Young Adult

Substances

  • DNA, Mitochondrial
  • Fumarate Hydratase

Supplementary concepts

  • Hereditary leiomyomatosis and renal cell cancer