Inhibition of ceramide accumulation in AdipoR1-/- mice increases photoreceptor survival and improves vision

JCI Insight. 2022 Feb 22;7(4):e156301. doi: 10.1172/jci.insight.156301.

Abstract

Adiponectin receptor 1 (ADIPOR1) is a lipid and glucose metabolism regulator that possesses intrinsic ceramidase activity. Mutations of the ADIPOR1 gene have been associated with nonsyndromic and syndromic retinitis pigmentosa. Here, we show that the absence of AdipoR1 in mice leads to progressive photoreceptor degeneration, significant reduction of electroretinogram amplitudes, decreased retinoid content in the retina, and reduced cone opsin expression. Single-cell RNA-Seq results indicate that ADIPOR1 encoded the most abundantly expressed ceramidase in mice and one of the 2 most highly expressed ceramidases in the human retina, next to acid ceramidase ASAH1. We discovered an accumulation of ceramides in the AdipoR1-/- retina, likely due to insufficient ceramidase activity for healthy retina function, resulting in photoreceptor death. Combined treatment with desipramine/L-cycloserine (DC) lowered ceramide levels and exerted a protective effect on photoreceptors in AdipoR1-/- mice. Moreover, we observed improvement in cone-mediated retinal function in the DC-treated animals. Lastly, we found that prolonged DC treatment corrected the electrical responses of the primary visual cortex to visual stimuli, approaching near-normal levels for some parameters. These results highlight the importance of ADIPOR1 ceramidase in the retina and show that pharmacological inhibition of ceramide generation can provide a therapeutic strategy for ADIPOR1-related retinopathy.

Keywords: Drug therapy; Ophthalmology.

Publication types

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

MeSH terms

  • Animals
  • Ceramidases / antagonists & inhibitors*
  • DNA / genetics*
  • DNA Mutational Analysis
  • Disease Models, Animal
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Mutation*
  • Receptors, Adiponectin / genetics*
  • Receptors, Adiponectin / metabolism
  • Retinal Cone Photoreceptor Cells / metabolism*
  • Retinal Cone Photoreceptor Cells / pathology
  • Retinal Diseases / genetics*
  • Retinal Diseases / metabolism
  • Retinal Diseases / pathology

Substances

  • Receptors, Adiponectin
  • adiponectin receptor 1, mouse
  • DNA
  • Ceramidases