Differential utilization of ketone bodies by neurons and glioma cell lines: a rationale for ketogenic diet as experimental glioma therapy

BMC Cancer. 2011 Jul 26:11:315. doi: 10.1186/1471-2407-11-315.

Abstract

Background: Even in the presence of oxygen, malignant cells often highly depend on glycolysis for energy generation, a phenomenon known as the Warburg effect. One strategy targeting this metabolic phenotype is glucose restriction by administration of a high-fat, low-carbohydrate (ketogenic) diet. Under these conditions, ketone bodies are generated serving as an important energy source at least for non-transformed cells.

Methods: To investigate whether a ketogenic diet might selectively impair energy metabolism in tumor cells, we characterized in vitro effects of the principle ketone body 3-hydroxybutyrate in rat hippocampal neurons and five glioma cell lines. In vivo, a non-calorie-restricted ketogenic diet was examined in an orthotopic xenograft glioma mouse model.

Results: The ketone body metabolizing enzymes 3-hydroxybutyrate dehydrogenase 1 and 2 (BDH1 and 2), 3-oxoacid-CoA transferase 1 (OXCT1) and acetyl-CoA acetyltransferase 1 (ACAT1) were expressed at the mRNA and protein level in all glioma cell lines. However, no activation of the hypoxia-inducible factor-1α (HIF-1α) pathway was observed in glioma cells, consistent with the absence of substantial 3-hydroxybutyrate metabolism and subsequent accumulation of succinate. Further, 3-hydroxybutyrate rescued hippocampal neurons from glucose withdrawal-induced cell death but did not protect glioma cell lines. In hypoxia, mRNA expression of OXCT1, ACAT1, BDH1 and 2 was downregulated. In vivo, the ketogenic diet led to a robust increase of blood 3-hydroxybutyrate, but did not alter blood glucose levels or improve survival.

Conclusion: In summary, glioma cells are incapable of compensating for glucose restriction by metabolizing ketone bodies in vitro, suggesting a potential disadvantage of tumor cells compared to normal cells under a carbohydrate-restricted ketogenic diet. Further investigations are necessary to identify co-treatment modalities, e.g. glycolysis inhibitors or antiangiogenic agents that efficiently target non-oxidative pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3-Hydroxybutyric Acid / metabolism
  • 3-Hydroxybutyric Acid / pharmacology
  • Acetyl-CoA C-Acetyltransferase / genetics
  • Acetyl-CoA C-Acetyltransferase / metabolism
  • Animals
  • Animals, Newborn
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Cells, Cultured
  • Coenzyme A-Transferases / genetics
  • Coenzyme A-Transferases / metabolism
  • Diet, Ketogenic
  • Female
  • Glioma / diet therapy
  • Glioma / metabolism*
  • Glioma / pathology
  • Glucose / metabolism
  • Glucose / pharmacology
  • Humans
  • Hydroxybutyrate Dehydrogenase / genetics
  • Hydroxybutyrate Dehydrogenase / metabolism
  • Immunoblotting
  • Ketone Bodies / metabolism*
  • Mice
  • Mice, Nude
  • NIH 3T3 Cells
  • Neurons / cytology
  • Neurons / metabolism*
  • Rats
  • Rats, Wistar
  • Reverse Transcriptase Polymerase Chain Reaction
  • Xenograft Model Antitumor Assays

Substances

  • Ketone Bodies
  • Hydroxybutyrate Dehydrogenase
  • ACAT1 protein, human
  • Acetyl-CoA C-Acetyltransferase
  • Coenzyme A-Transferases
  • 3-ketoacid CoA-transferase
  • Glucose
  • 3-Hydroxybutyric Acid