Loss of cone photoreceptors caused by chromophore depletion is partially prevented by the artificial chromophore pro-drug, 9-cis-retinyl acetate

Hum Mol Genet. 2009 Jun 15;18(12):2277-87. doi: 10.1093/hmg/ddp163. Epub 2009 Apr 1.

Abstract

Inactivating mutations in the retinoid isomerase (RPE65) or lecithin:retinol acyltransferase (LRAT) genes cause Leber congenital amaurosis (LCA), a severe visual impairment in humans. Both enzymes participate in the retinoid (visual) cycle, the enzymatic pathway that continuously generates 11-cis-retinal, the chromophore of visual pigments in rod and cone photoreceptor cells needed for vision. We investigated human RPE65-LCA patients and mice with visual cycle abnormalities to determine the impact of chronic chromophore deprivation on cones. Young patients with RPE65 mutations showed foveal cone loss along with shortened inner and outer segments of remaining cones; cone cell loss also was dramatic in young mice lacking Rpe65 or Lrat gene function. To selectively evaluate cone pathophysiology, we eliminated the rod contribution to electroretinographic (ERG) responses by generating double knockout mice lacking Lrat or Rpe65 together with an inactivated rod-specific G protein transducin gene (Gnat1-/-). Cone ERG responses were absent in Gnat1-/-Lrat-/- mice which also showed progressive degeneration of cones. Cone ERG responses in Gnat1-/-Rpe65-/- mice were markedly reduced and declined over weeks. Treatment of these mice with the artificial chromophore pro-drug, 9-cis-retinyl acetate, partially protected inferior retinal cones as evidenced by improved ERGs and retinal histochemistry. Gnat1-/- mice chronically treated with retinylamine, a selective inhibitor of RPE65, also showed a decline in the number of cones that was ameliorated by 9-cis-retinyl acetate. These results suggest that chronic lack of chromophore leads to progressive loss of cones in mice and humans. Therapy for LCA patients should be geared toward early adequate delivery of chromophore to cone photoreceptors.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Diterpenes
  • Eye Proteins / genetics
  • Eye Proteins / metabolism
  • GTP-Binding Protein alpha Subunits / genetics
  • GTP-Binding Protein alpha Subunits / metabolism
  • Humans
  • Mice
  • Mice, Knockout
  • Optic Atrophy, Hereditary, Leber / drug therapy*
  • Optic Atrophy, Hereditary, Leber / genetics
  • Prodrugs / therapeutic use*
  • Retinal Cone Photoreceptor Cells / drug effects
  • Retinal Cone Photoreceptor Cells / metabolism*
  • Retinaldehyde / deficiency*
  • Retinyl Esters
  • Transducin / genetics
  • Transducin / metabolism
  • Vitamin A / analogs & derivatives*
  • Vitamin A / therapeutic use
  • cis-trans-Isomerases

Substances

  • Adaptor Proteins, Signal Transducing
  • Carrier Proteins
  • Diterpenes
  • Eye Proteins
  • GTP-Binding Protein alpha Subunits
  • Gnat1 protein, mouse
  • Prodrugs
  • Retinyl Esters
  • Vitamin A
  • retinol acetate
  • Lrba protein, mouse
  • retinoid isomerohydrolase
  • Transducin
  • cis-trans-Isomerases
  • Retinaldehyde