Interphotoreceptor retinoid-binding protein removes all- trans-retinol and retinal from rod outer segments, preventing lipofuscin precursor formation

J Biol Chem. 2017 Nov 24;292(47):19356-19365. doi: 10.1074/jbc.M117.795187. Epub 2017 Sep 28.

Abstract

Interphotoreceptor retinoid-binding protein (IRBP) is a specialized lipophilic carrier that binds the all-trans and 11-cis isomers of retinal and retinol, and this facilitates their transport between photoreceptors and cells in the retina. One of these retinoids, all-trans-retinal, is released in the rod outer segment by photoactivated rhodopsin after light excitation. Following its release, all-trans-retinal is reduced by the retinol dehydrogenase RDH8 to all-trans-retinol in an NADPH-dependent reaction. However, all-trans-retinal can also react with outer segment components, sometimes forming lipofuscin precursors, which after conversion to lipofuscin accumulate in the lysosomes of the retinal pigment epithelium and display cytotoxic effects. Here, we have imaged the fluorescence of all-trans-retinol, all-trans-retinal, and lipofuscin precursors in real time in single isolated mouse rod photoreceptors. We found that IRBP removes all-trans-retinol from individual rod photoreceptors in a concentration-dependent manner. The rate constant for retinol removal increased linearly with IRBP concentration with a slope of 0.012 min-1 μm-1 IRBP also removed all-trans-retinal, but with much less efficacy, indicating that the reduction of retinal to retinol promotes faster clearance of the photoisomerized rhodopsin chromophore. The presence of physiological IRBP concentrations in the extracellular medium resulted in lower levels of all-trans-retinal and retinol in rod outer segments following light exposure. It also prevented light-induced lipofuscin precursor formation, but it did not remove precursors that were already present. These findings reveal an important and previously unappreciated role of IRBP in protecting the photoreceptor cells against the cytotoxic effects of accumulated all-trans-retinal.

Keywords: fluorescence; photoreceptor; retina; retinoid-binding protein; retinol.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cattle
  • Eye Proteins / physiology*
  • Light
  • Lipofuscin / metabolism*
  • Mice
  • Mice, Knockout
  • Retinaldehyde / metabolism*
  • Retinol-Binding Proteins / physiology*
  • Rod Cell Outer Segment / metabolism*
  • Vitamin A / metabolism*

Substances

  • Eye Proteins
  • Lipofuscin
  • Retinol-Binding Proteins
  • interstitial retinol-binding protein
  • Vitamin A
  • Retinaldehyde