Dark noise and retinal degeneration from D190N-rhodopsin

Proc Natl Acad Sci U S A. 2020 Sep 15;117(37):23033-23043. doi: 10.1073/pnas.2010417117. Epub 2020 Sep 1.

Abstract

Numerous rhodopsin mutations have been implicated in night blindness and retinal degeneration, often with unclear etiology. D190N-rhodopsin (D190N-Rho) is a well-known inherited human mutation causing retinitis pigmentosa. Both higher-than-normal spontaneous-isomerization activity and misfolding/mistargeting of the mutant protein have been proposed as causes of the disease, but neither explanation has been thoroughly examined. We replaced wild-type rhodopsin (WT-Rho) in RhoD190N/WT mouse rods with a largely "functionally silenced" rhodopsin mutant to isolate electrical responses triggered by D190N-Rho activity, and found that D190N-Rho at the single-molecule level indeed isomerizes more frequently than WT-Rho by over an order of magnitude. Importantly, however, this higher molecular dark activity does not translate into an overall higher cellular dark noise, owing to diminished D190N-Rho content in the rod outer segment. Separately, we found that much of the degeneration and shortened outer-segment length of RhoD190N/WT mouse rods was not averted by ablating rod transducin in phototransduction-also consistent with D190N-Rho's higher isomerization activity not being the primary cause of disease. Instead, the low pigment content, shortened outer-segment length, and a moderate unfolded protein response implicate protein misfolding as the major pathogenic problem. Finally, D190N-Rho also provided some insight into the mechanism of spontaneous pigment excitation.

Keywords: D190N-rhodopsin; night blindness; protein misfolding; retinitis pigmentosa; spontaneous isomerization.

Publication types

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

MeSH terms

  • Animals
  • Cell Line
  • Disease Models, Animal
  • HEK293 Cells
  • Humans
  • Light Signal Transduction / physiology
  • Mice
  • Mutation / physiology
  • Retinal Degeneration / metabolism*
  • Retinal Rod Photoreceptor Cells / metabolism
  • Retinitis Pigmentosa / metabolism
  • Rhodopsin / metabolism*
  • Rod Cell Outer Segment / metabolism

Substances

  • Rhodopsin