Rapid degeneration of rod photoreceptors expressing self-association-deficient arrestin-1 mutant

Cell Signal. 2013 Dec;25(12):2613-24. doi: 10.1016/j.cellsig.2013.08.022. Epub 2013 Sep 3.

Abstract

Arrestin-1 binds light-activated phosphorhodopsin and ensures timely signal shutoff. We show that high transgenic expression of an arrestin-1 mutant with enhanced rhodopsin binding and impaired oligomerization causes apoptotic rod death in mice. Dark rearing does not prevent mutant-induced cell death, ruling out the role of arrestin complexes with light-activated rhodopsin. Similar expression of WT arrestin-1 that robustly oligomerizes, which leads to only modest increase in the monomer concentration, does not affect rod survival. Moreover, WT arrestin-1 co-expressed with the mutant delays retinal degeneration. Thus, arrestin-1 mutant directly affects cell survival via binding partner(s) other than light-activated rhodopsin. Due to impaired self-association of the mutant its high expression dramatically increases the concentration of the monomer. The data suggest that monomeric arrestin-1 is cytotoxic and WT arrestin-1 protects rods by forming mixed oligomers with the mutant and/or competing with it for the binding to non-receptor partners. Thus, arrestin-1 self-association likely serves to keep low concentration of the toxic monomer. The reduction of the concentration of harmful monomer is an earlier unappreciated biological function of protein oligomerization.

Keywords: Arrestin; Cell death; G protein-coupled receptor; G protein-coupled receptor kinase; GPCR; GRK; Monomer; P-Ops; P-Rh; P-Rh*; Retina; Rh; Rh*; Rhodopsin; Self-association; WT; dark phosphorylated rhodopsin; dark unphosphorylated rhodopsin; light-activated phosphorylated rhodopsin; light-activated unphosphorylated rhodopsin; phospho-opsin; wild type.

Publication types

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

MeSH terms

  • Animals
  • Arrestin / chemistry
  • Arrestin / genetics*
  • Arrestin / metabolism*
  • Cell Death
  • MAP Kinase Kinase 4 / metabolism
  • Mice
  • Mutation*
  • Protein Multimerization
  • Retinal Rod Photoreceptor Cells / cytology
  • Retinal Rod Photoreceptor Cells / metabolism*
  • Retinal Rod Photoreceptor Cells / pathology*
  • Rhodopsin / metabolism

Substances

  • Arrestin
  • Rhodopsin
  • MAP Kinase Kinase 4