Extracellular Citrate Affects Critical Elements of Cancer Cell Metabolism and Supports Cancer Development In Vivo

Cancer Res. 2018 May 15;78(10):2513-2523. doi: 10.1158/0008-5472.CAN-17-2959. Epub 2018 Mar 6.

Abstract

Glycolysis and fatty acid synthesis are highly active in cancer cells through cytosolic citrate metabolism, with intracellular citrate primarily derived from either glucose or glutamine via the tricarboxylic acid cycle. We show here that extracellular citrate is supplied to cancer cells through a plasma membrane-specific variant of the mitochondrial citrate transporter (pmCiC). Metabolomic analysis revealed that citrate uptake broadly affected cancer cell metabolism through citrate-dependent metabolic pathways. Treatment with gluconate specifically blocked pmCiC and decreased tumor growth in murine xenografts of human pancreatic cancer. This treatment altered metabolism within tumors, including fatty acid metabolism. High expression of pmCiC was associated with invasion and advanced tumor stage across many human cancers. These findings support the exploration of extracellular citrate transport as a novel potential target for cancer therapy.Significance: Uptake of extracellular citrate through pmCiC can be blocked with gluconate to reduce tumor growth and to alter metabolic characteristics of tumor tissue. Cancer Res; 78(10); 2513-23. ©2018 AACR.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anion Transport Proteins / antagonists & inhibitors*
  • Anion Transport Proteins / metabolism*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects*
  • Citric Acid / metabolism*
  • Epithelial Cells / metabolism
  • Fatty Acids / biosynthesis
  • Gluconates / pharmacology*
  • Glycolysis / physiology
  • Humans
  • Male
  • Mice
  • Mitochondrial Proteins / antagonists & inhibitors*
  • Mitochondrial Proteins / metabolism*
  • Organic Anion Transporters
  • Pancreatic Neoplasms / pathology*
  • Prostate / cytology
  • Prostate / metabolism
  • Prostatic Neoplasms / pathology*
  • RNA Interference
  • RNA, Small Interfering / genetics

Substances

  • Anion Transport Proteins
  • Fatty Acids
  • Gluconates
  • Mitochondrial Proteins
  • Organic Anion Transporters
  • RNA, Small Interfering
  • Slc25a1 protein, human
  • Citric Acid
  • gluconic acid