Trinucleotide Repeat Expansion in the Transcription Factor 4 (TCF4) Gene Leads to Widespread mRNA Splicing Changes in Fuchs' Endothelial Corneal Dystrophy

Invest Ophthalmol Vis Sci. 2017 Jan 1;58(1):343-352. doi: 10.1167/iovs.16-20900.

Abstract

Purpose: To identify RNA missplicing events in human corneal endothelial tissue isolated from Fuchs' endothelial corneal dystrophy (FECD).

Methods: Total RNA was isolated and sequenced from corneal endothelial tissue obtained during keratoplasty from 12 patients with FECD and 4 patients undergoing keratoplasty or enucleation for other indications. The length of the trinucleotide repeat (TNR) CTG in the transcription factor 4 (TCF4) gene was determined using leukocyte-derived DNA analyzed by a combination of Southern blotting and Genescan analysis. Commercial statistical software was used to quantify expression of alternatively spliced genes. Validation of selected alternative splicing events was performed by using RT-PCR. Gene sets identified were analyzed for overrepresentation using Web-based analysis system.

Results: Corneal endothelial tissue from FECD patients containing a CTG TNR expansion sequence in the TCF4 gene revealed widespread changes in mRNA splicing, including a novel splicing event involving FGFR2. Differential splicing of NUMA1, PPFIBP1, MBNL1, and MBNL2 transcripts were identified in all FECD samples containing a TNR expansion. The differentially spliced genes were enriched for products that localize to the cell cortex and bind cytoskeletal and cell adhesion proteins.

Conclusions: Corneal endothelium from FECD patients harbors a unique signature of mis-splicing events due to CTG TNR expansion in the TCF4 gene, consistent with the hypothesis that RNA toxicity contributes to the pathogenesis of FECD. Changes to the endothelial barrier function, a known event in the development of FECD, was identified as a key biological process influenced by the missplicing events.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Alleles
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / genetics*
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / metabolism
  • Blotting, Southern
  • Endothelium, Corneal / metabolism
  • Endothelium, Corneal / pathology
  • Female
  • Fuchs' Endothelial Dystrophy / diagnosis
  • Fuchs' Endothelial Dystrophy / genetics*
  • Fuchs' Endothelial Dystrophy / metabolism
  • Gene Expression Regulation*
  • Genetic Predisposition to Disease*
  • Genotype
  • Humans
  • Male
  • Middle Aged
  • Polymerase Chain Reaction
  • RNA Splicing / genetics*
  • RNA, Messenger / genetics*
  • Transcription Factor 4
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Trinucleotide Repeat Expansion

Substances

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • RNA, Messenger
  • TCF4 protein, human
  • Transcription Factor 4
  • Transcription Factors