ATP4- mediates closure of pancreatic beta-cell ATP-sensitive potassium channels by interaction with 1 of 4 identical sites

Diabetes. 2000 Sep;49(9):1413-8. doi: 10.2337/diabetes.49.9.1413.

Abstract

In pancreatic beta-cells, cytosolic [ATP(4-)] critically controls insulin secretion via inhibition of ATP-sensitive potassium (KATP) channels. These channels are heteromultimers composed with a 4:4 stoichiometry of an inwardly rectifying K+ channel subunit (Kir6.2) plus a regulatory sulfonylurea receptor. To elucidate stoichiometry of ATP(4-) action, we analyzed ATP(4-) sensitivity of channels coassembled from wild-type Kir6.2 and a loss of ATP(4-) sensitivity mutant (G334D). Concentration-inhibition curves for cDNA ratios of 1:1 or 1:10 resembled those for channel block resulting from interaction with 1 of 4 sites, whereas models for inhibition requiring occupation of 2, 3, or 4 sites were incongruous. Random assembly of wild-type Kir6.2 with the G334D mutant was confirmed by controls, which assessed the effect of an additional mutation that induced strong rectification (N160D). We conclude 4 identical noncooperative ATP(4-) sites to be grouped within 1 KATP channel complex, with occupation of 1 site being sufficient to induce channel closure. This architecture might facilitate coupling of [ATP(4-)] to insulin secretion and may protect against diabetic dysregulation resulting from heterozygous mutations in Kir6.2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / pharmacology*
  • Adenosine Triphosphate / physiology
  • Amino Acid Substitution
  • Animals
  • COS Cells
  • Cricetinae
  • Islets of Langerhans / physiology*
  • Kinetics
  • Macromolecular Substances
  • Membrane Potentials
  • Mice
  • Mutagenesis, Site-Directed
  • Potassium Channels / chemistry
  • Potassium Channels / drug effects
  • Potassium Channels / physiology*
  • Potassium Channels, Inwardly Rectifying*
  • Protein Structure, Quaternary
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Transfection

Substances

  • Macromolecular Substances
  • Potassium Channels
  • Potassium Channels, Inwardly Rectifying
  • Recombinant Proteins
  • Adenosine Triphosphate