Glutaminolysis is Essential for Energy Production and Ion Transport in Human Corneal Endothelium

EBioMedicine. 2017 Feb:16:292-301. doi: 10.1016/j.ebiom.2017.01.004. Epub 2017 Jan 13.

Abstract

Corneal endothelium (CE) is among the most metabolically active tissues in the body. This elevated metabolic rate helps the CE maintain corneal transparency by its ion and fluid transport properties, which when disrupted, leads to visual impairment. Here we demonstrate that glutamine catabolism (glutaminolysis) through TCA cycle generates a large fraction of the ATP needed to maintain CE function, and this glutaminolysis is severely disrupted in cells deficient in NH3:H+ cotransporter Solute Carrier Family 4 Member 11 (SLC4A11). Considering SLC4A11 mutations leads to corneal endothelial dystrophy and sensorineural deafness, our results indicate that SLC4A11-associated developmental and degenerative disorders result from altered glutamine catabolism. Overall, our results describe an important metabolic mechanism that provides CE cells with the energy required to maintain high level transport activity, reveal a direct link between glutamine metabolism and developmental and degenerative neuronal diseases, and suggest an approach for protecting the CE during ophthalmic surgeries.

Keywords: Congenital hereditary endothelial dystrophy (CHED); Corneal endothelium; Energy metabolism; Fuchs' endothelial corneal dystrophy (FECD); Glutaminolysis; SLC4A11 ammonia transporter.

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Amino Acid Transport System X-AG / genetics
  • Amino Acid Transport System X-AG / metabolism
  • Animals
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Line
  • Cells, Cultured
  • Citric Acid Cycle
  • Corneal Dystrophies, Hereditary / genetics
  • Corneal Dystrophies, Hereditary / metabolism
  • Corneal Dystrophies, Hereditary / pathology
  • Endothelium, Corneal / metabolism*
  • Energy Metabolism*
  • Epithelium, Corneal / cytology
  • Epithelium, Corneal / metabolism
  • Fuchs' Endothelial Dystrophy / genetics
  • Fuchs' Endothelial Dystrophy / metabolism
  • Fuchs' Endothelial Dystrophy / pathology
  • Gene Expression
  • Glutamine / metabolism*
  • Humans
  • Ion Transport
  • Mice, Knockout
  • Microscopy, Fluorescence
  • Mutation
  • Rabbits
  • Reverse Transcriptase Polymerase Chain Reaction
  • SLC4A Proteins / genetics
  • SLC4A Proteins / metabolism

Substances

  • Amino Acid Transport System X-AG
  • Carrier Proteins
  • SLC4A Proteins
  • glutamine transport proteins
  • Glutamine
  • Adenosine Triphosphate