The silent codon change I507-ATC->ATT contributes to the severity of the ΔF508 CFTR channel dysfunction

FASEB J. 2013 Nov;27(11):4630-45. doi: 10.1096/fj.13-227330. Epub 2013 Aug 1.

Abstract

The most common disease-causing mutation in the cystic fibrosis transmembrane conductance regulator (CFTR) gene is the out-of-frame deletion of 3 nucleotides (CTT). This mutation leads to the loss of phenylalanine-508 (ΔF508) and a silent codon change (SCC) for isoleucine-507 (I507-ATC→ATT). ΔF508 CFTR is misfolded and degraded by endoplasmic reticulum-associated degradation (ERAD). We have demonstrated that the I507-ATC→ATT SCC alters ΔF508 CFTR mRNA structure and translation dynamics. By comparing the biochemical and functional properties of the I507-ATT and I507-ATC ΔF508 CFTR, we establish that the I507-ATC→ATT SCC contributes to the cotranslational misfolding, ERAD, and to the functional defects associated with ΔF508 CFTR. We demonstrate that the I507-ATC ΔF508 CFTR is less susceptible to the ER quality-control machinery during translation than the I507-ATT, although 27°C correction is necessary for sufficient cell-surface expression. Whole-cell patch-clamp recordings indicate sustained, thermally stable cAMP-activated Cl(-) transport through I507-ATC and unstable function of the I507-ATT ΔF508 CFTR. Single-channel recordings reveal improved gating properties of the I507-ATC compared to I507-ATT ΔF508 CFTR (NPo=0.45±0.037 vs. NPo=0.09±0.002; P<0.001). Our results signify the role of the I507-ATC→ATT SCC in the ΔF508 CFTR defects and support the importance of synonymous codon choices in determining the function of gene products.

Keywords: ABC protein; channel gating; cotranslational folding; patch-clamp; sSNP; single-nucleotide polymorphism.

Publication types

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

MeSH terms

  • Action Potentials
  • Cell Membrane / metabolism
  • Chlorides / metabolism
  • Codon*
  • Cystic Fibrosis Transmembrane Conductance Regulator / biosynthesis
  • Cystic Fibrosis Transmembrane Conductance Regulator / genetics*
  • Cystic Fibrosis Transmembrane Conductance Regulator / metabolism*
  • Endoplasmic Reticulum-Associated Degradation
  • HEK293 Cells
  • Humans
  • Ion Channel Gating
  • Mutation, Missense*
  • Polymorphism, Single Nucleotide
  • Protein Biosynthesis
  • Protein Transport
  • RNA Folding
  • RNA Stability
  • RNA, Messenger / chemistry
  • RNA, Messenger / metabolism

Substances

  • Chlorides
  • Codon
  • RNA, Messenger
  • Cystic Fibrosis Transmembrane Conductance Regulator