The cpk model of recessive PKD shows glutamine dependence associated with the production of the oncometabolite 2-hydroxyglutarate

Am J Physiol Renal Physiol. 2015 Sep 15;309(6):F492-8. doi: 10.1152/ajprenal.00238.2015. Epub 2015 Jul 8.

Abstract

Since polycystic kidney disease (PKD) was first noted over 30 years ago to have neoplastic parallels, there has been a resurgent interest in elucidating neoplasia-relevant pathways in PKD. Taking a nontargeted metabolomics approach in the B6(Cg)-Cys1(cpk/)J (cpk) mouse model of recessive PKD, we have now characterized metabolic reprogramming in these tissues, leading to a glutamine-dependent TCA cycle shunt toward total 2-hydroxyglutarate (2-HG) production in cpk compared with B6 wild-type kidney tissue. After confirmation of increased 2-HG expression in immortalized collecting duct cpk cells as well as in human autosomal recessive PKD tissue using targeted analysis, we show that the increase in 2-HG is likely due to glutamine-sourced α-ketoglutarate. In addition, cpk cells require exogenous glutamine for growth such that inhibition of glutaminase-1 decreases cell viability as well as proliferation. This study is a demonstration of the striking parallels between recessive PKD and cancer metabolism. Our data, once confirmed in other PKD models, suggest that future therapeutic approaches targeting this pathway, such as using glutaminase inhibitors, have the potential to open novel treatment options for renal cystic disease.

Keywords: ARPKD; glutamine; metabolomics; oncometabolite; reprogramming.

Publication types

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

MeSH terms

  • Animals
  • Cells, Cultured
  • Creatine Kinase / genetics*
  • DNA Mutational Analysis
  • Disease Models, Animal
  • Enzyme Inhibitors / pharmacology
  • Female
  • Glutaminase / antagonists & inhibitors
  • Glutamine / metabolism*
  • Glutarates / metabolism*
  • Humans
  • Infant
  • Infant, Newborn
  • Male
  • Metabolomics
  • Mice
  • Models, Genetic
  • Polycystic Kidney Diseases / genetics*
  • Polycystic Kidney Diseases / metabolism*

Substances

  • Enzyme Inhibitors
  • Glutarates
  • Glutamine
  • alpha-hydroxyglutarate
  • Creatine Kinase
  • Glutaminase