A conserved tryptophan at the membrane-water interface acts as a gatekeeper for Kir6.2/SUR1 channels and causes neonatal diabetes when mutated

J Physiol. 2011 Jul 1;589(Pt 13):3071-83. doi: 10.1113/jphysiol.2011.209700. Epub 2011 May 3.

Abstract

We identified a novel heterozygous mutation, W68R, in the Kir6.2 subunit of the ATP-sensitive potassium (KATP) channel, in a patient with transient neonatal diabetes. This tryptophan is absolutely conserved in mammalian Kir channels. The functional effects of mutations at residue 68 of Kir6.2 were studied by heterologous expression in Xenopus oocytes, and by homology modelling. We found the Kir6.2-W68R mutation causes a small reduction in ATP inhibition in the heterozygous state and an increase in the whole-cell KATP current. This can explain the clinical phenotype of the patient. The effect of the mutation was not charge or size dependent, the order of potency for ATP inhibition being W<M∼L<R∼E∼K∼A<C∼F<Y. Replacement with tyrosine (Y) rendered the KATP channel almost completely insensitive to ATP block, dramatically increased the channel open probability, and affected the interaction of Kir6.2 with SUR1. In different Kir crystal structures the residue corresponding to W68 adopts two distinct positions. In one state, the tryptophan lies in a position that would impede movement of transmembrane domain 2 (TM2) and opening of the gate. In the other state, it is flipped out, enabling movement of TM2. We therefore hypothesise that W68 may act as a molecular'gatekeeper' for Kir channels.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP-Binding Cassette Transporters / genetics*
  • ATP-Binding Cassette Transporters / metabolism
  • Amino Acid Sequence
  • Animals
  • Cell Membrane / genetics*
  • Cell Membrane / metabolism
  • Child
  • Conserved Sequence / genetics
  • Diabetes Mellitus / genetics*
  • Diabetes Mellitus / metabolism
  • Female
  • Genetic Carrier Screening
  • Humans
  • Infant, Newborn
  • Infant, Newborn, Diseases / genetics*
  • Infant, Newborn, Diseases / metabolism
  • Molecular Sequence Data
  • Mutation / genetics*
  • Oocytes / metabolism
  • Phenotype
  • Potassium Channels, Inwardly Rectifying / genetics*
  • Potassium Channels, Inwardly Rectifying / metabolism
  • Rats
  • Receptors, Drug / genetics*
  • Receptors, Drug / metabolism
  • Sulfonylurea Receptors
  • Tryptophan / genetics*
  • Xenopus laevis

Substances

  • ABCC8 protein, human
  • ATP-Binding Cassette Transporters
  • Abcc8 protein, rat
  • Kir6.2 channel
  • Potassium Channels, Inwardly Rectifying
  • Receptors, Drug
  • Sulfonylurea Receptors
  • Tryptophan