Mechanistic basis for the pathogenesis of long QT syndrome associated with a common splicing mutation in KCNQ1 gene

J Mol Cell Cardiol. 2007 Mar;42(3):662-9. doi: 10.1016/j.yjmcc.2006.12.015. Epub 2007 Jan 5.

Abstract

Mutations in KCNQ1, the gene encoding the delayed rectifier K(+) channel in cardiac muscle, cause long QT syndrome (LQTS). We studied 3 families with LQTS, in whom a guanine to adenine change in the last base of exon 7 (c.1032G>A), previously reported as a common splice-site mutation, was identified. We performed quantitative measurements of exon-skipping KCNQ1 mRNAs caused by this mutation using real-time reverse transcription polymerase chain reaction. Compared with normal individuals who have minor fractions of splicing variants (Delta7-8: 0.1%, Delta8: 6.9%, of total KCNQ1 transcripts), the affected individuals showed remarkable increases of exon-skipping mRNAs (Delta7: 23.5%, Delta7-8: 16.8%, Delta8: 4.5%). Current recordings from Xenopus laevis oocytes heterologously expressing channels of wild-type (WT) or exon-skipping KCNQ1 (Delta7, Delta7-8, or Delta8) revealed that none of the mutants produced any measurable currents, and moreover they displayed mutant-specific degree of dominant-negative effects on WT currents, when co-expressed with WT. Confocal microscopy analysis showed that fluorescent protein-tagged WT was predominantly expressed on the plasma membrane, whereas the mutants showed intracellular distribution. When WT was co-expressed with mutants, the majority of WT co-localized with the mutants in the intracellular space. Finally, we provide evidence showing direct protein-protein interactions between WT and the mutants, by using fluorescence resonance energy transfer. Thus, the mutants may exert their dominant-negative effects by trapping WT intracellularly and thereby interfering its translocation to the plasma membrane. In conclusion, our data provide a mechanistic basis for the pathogenesis of LQTS caused by a splicing mutation in KCNQ1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Biophysical Phenomena
  • Biophysics
  • COS Cells
  • Chlorocebus aethiops
  • Electrophysiology
  • Exons / genetics
  • KCNQ1 Potassium Channel / genetics*
  • KCNQ1 Potassium Channel / metabolism*
  • Long QT Syndrome / genetics
  • Long QT Syndrome / metabolism*
  • Mutation / genetics
  • Patch-Clamp Techniques
  • RNA Splicing / genetics*
  • RNA, Messenger / genetics
  • Xenopus laevis

Substances

  • KCNQ1 Potassium Channel
  • RNA, Messenger