Trafficking-deficient hERG K⁺ channels linked to long QT syndrome are regulated by a microtubule-dependent quality control compartment in the ER

Am J Physiol Cell Physiol. 2011 Jul;301(1):C75-85. doi: 10.1152/ajpcell.00494.2010. Epub 2011 Apr 13.

Abstract

The human ether-a-go-go related gene (hERG) encodes the voltage-gated K(+) channel that underlies the rapidly activating delayed-rectifier current in cardiac myocytes. hERG is synthesized in the endoplasmic reticulum (ER) as an "immature" N-linked glycoprotein and is terminally glycosylated in the Golgi apparatus. Most hERG missense mutations linked to long QT syndrome type 2 (LQT2) reduce the terminal glycosylation and functional expression. We tested the hypothesis that a distinct pre-Golgi compartment negatively regulates the trafficking of some LQT2 mutations to the Golgi apparatus. We found that treating cells in nocodazole, a microtubule depolymerizing agent, altered the subcellular localization, functional expression, and glycosylation of the LQT2 mutation G601S-hERG differently from wild-type hERG (WT-hERG). G601S-hERG quickly redistributed to peripheral compartments that partially colocalized with KDEL (Lys-Asp-Glu-Leu) chaperones but not calnexin, Sec31, or the ER golgi intermediate compartment (ERGIC). Treating cells in E-4031, a drug that increases the functional expression of G601S-hERG, prevented the accumulation of G601S-hERG to the peripheral compartments and increased G601S-hERG colocalization with the ERGIC. Coexpressing the temperature-sensitive mutant G protein from vesicular stomatitis virus, a mutant N-linked glycoprotein that is retained in the ER, showed it was not restricted to the same peripheral compartments as G601S-hERG at nonpermissive temperatures. We conclude that the trafficking of G601S-hERG is negatively regulated by a microtubule-dependent compartment within the ER. Identifying mechanisms that prevent the sorting or promote the release of LQT2 channels from this compartment may represent a novel therapeutic strategy for LQT2.

Publication types

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

MeSH terms

  • Anti-Arrhythmia Agents / pharmacology
  • Blotting, Western
  • Endoplasmic Reticulum / metabolism*
  • Ether-A-Go-Go Potassium Channels / biosynthesis
  • Ether-A-Go-Go Potassium Channels / genetics
  • Ether-A-Go-Go Potassium Channels / metabolism*
  • Fluorescent Antibody Technique
  • Glycosylation
  • Golgi Apparatus / metabolism
  • Green Fluorescent Proteins
  • HEK293 Cells
  • Humans
  • Long QT Syndrome / genetics*
  • Long QT Syndrome / metabolism
  • Microtubules / drug effects
  • Microtubules / metabolism*
  • Mutation
  • Myocytes, Cardiac / metabolism
  • Nocodazole / pharmacology
  • Patch-Clamp Techniques
  • Piperidines / pharmacology
  • Protein Transport
  • Pyridines / pharmacology
  • Tubulin Modulators / pharmacology

Substances

  • Anti-Arrhythmia Agents
  • Ether-A-Go-Go Potassium Channels
  • Piperidines
  • Pyridines
  • Tubulin Modulators
  • E 4031
  • Green Fluorescent Proteins
  • Nocodazole