A connexin50 mutant, CX50fs, that causes cataracts is unstable, but is rescued by a proteasomal inhibitor

J Biol Chem. 2013 Jul 12;288(28):20427-34. doi: 10.1074/jbc.M113.452847. Epub 2013 May 17.

Abstract

The mechanisms by which mutant connexins lead to disease are diverse, including those of connexin50 (CX50) encoded by the GJA8 gene. We investigated the cellular and functional behavior of CX50fs, a mutant CX50 that has a frameshift after amino acid 255 and causes recessive congenital cataracts. Cellular levels of CX50fs were much lower than those of wild type CX50 in stably transfected HeLa cells. Whereas CX50 localized at distinct gap junction plaques and supported extensive intercellular transfer of Neurobiotin, CX50fs gap junctions were rare, and their support of Neurobiotin transfer was reduced by >90%. After inhibition of new protein synthesis with cycloheximide, CX50fs disappeared much more rapidly than CX50, suggesting increased degradation of the mutant. Treatment of cells with epoxomicin (a proteasomal inhibitor) led to a dramatic increase in CX50fs levels and in the abundance of gap junctions. Epoxomicin treatment also rescued intercellular transfer of Neurobiotin to levels similar to those in cells expressing the wild type protein. Treatment with eeyarestatin I (an inhibitor of p97-dependent protein degradation) resulted in many abundant slowly migrating CX50 and CX50fs bands consistent with polyubiquitination of the proteins. These results demonstrate that the CX50fs mutant is rapidly degraded by endoplasmic reticulum-associated degradation in mammalian cells. This accelerated degradation reduces the abundance of gap junctions and the extent of intercellular communication, potentially explaining the pathogenesis of cataracts linked to this mutant. The efficacy of epoxomicin in restoring function suggests that protease inhibition might have therapeutic value for this and other diseases caused by mutants with similar defects.

Keywords: Cataract; Cell Junctions; Connexin; Gap Junctions; Intercellular Communication; Proteasome.

Publication types

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

MeSH terms

  • Biological Transport / drug effects
  • Biotin / analogs & derivatives
  • Biotin / metabolism
  • Cataract / enzymology*
  • Cataract / genetics
  • Cell Communication / drug effects
  • Connexins / genetics
  • Connexins / metabolism*
  • Cycloheximide / pharmacology
  • Endoplasmic Reticulum-Associated Degradation / drug effects
  • Eye Proteins / genetics
  • Eye Proteins / metabolism*
  • Gap Junctions / drug effects
  • Gap Junctions / metabolism
  • HeLa Cells
  • Humans
  • Hydrazones / pharmacology
  • Hydroxyurea / analogs & derivatives
  • Hydroxyurea / pharmacology
  • Immunoblotting
  • Microscopy, Fluorescence
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism*
  • Mutation
  • Oligopeptides / pharmacology
  • Proteasome Inhibitors / pharmacology*
  • Protein Stability / drug effects
  • Protein Synthesis Inhibitors / pharmacology
  • Proteolysis / drug effects

Substances

  • 1-(4-chlorophenyl)-3-(3-(4-chlorophenyl)-5,5-dimethyl-1-(3-(5-nitrofuran-2-yl)allyldienehydrazinocarbonylmethyl)-2-oxoimidazolidin-4-yl)-1-hydroxyurea
  • Connexins
  • Eye Proteins
  • Hydrazones
  • Mutant Proteins
  • Oligopeptides
  • Proteasome Inhibitors
  • Protein Synthesis Inhibitors
  • connexin 50
  • neurobiotin
  • Biotin
  • Cycloheximide
  • Hydroxyurea
  • epoxomicin