Structural basis of control of inward rectifier Kir2 channel gating by bulk anionic phospholipids

J Gen Physiol. 2016 Sep;148(3):227-37. doi: 10.1085/jgp.201611616. Epub 2016 Aug 15.

Abstract

Inward rectifier potassium (Kir) channel activity is controlled by plasma membrane lipids. Phosphatidylinositol-4,5-bisphosphate (PIP2) binding to a primary site is required for opening of classic inward rectifier Kir2.1 and Kir2.2 channels, but interaction of bulk anionic phospholipid (PL(-)) with a distinct second site is required for high PIP2 sensitivity. Here we show that introduction of a lipid-partitioning tryptophan at the second site (K62W) generates high PIP2 sensitivity, even in the absence of PL(-) Furthermore, high-resolution x-ray crystal structures of Kir2.2[K62W], with or without added PIP2 (2.8- and 2.0-Å resolution, respectively), reveal tight tethering of the C-terminal domain (CTD) to the transmembrane domain (TMD) in each condition. Our results suggest a refined model for phospholipid gating in which PL(-) binding at the second site pulls the CTD toward the membrane, inducing the formation of the high-affinity primary PIP2 site and explaining the positive allostery between PL(-) binding and PIP2 sensitivity.

Publication types

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

MeSH terms

  • Animals
  • Anions / metabolism*
  • Cell Membrane / metabolism
  • Chickens
  • Crystallography, X-Ray / methods
  • Ion Channel Gating / physiology*
  • Membrane Proteins / metabolism
  • Phosphatidylinositol 4,5-Diphosphate / metabolism
  • Phospholipids / metabolism*
  • Potassium / metabolism
  • Potassium Channels, Inwardly Rectifying / metabolism*
  • Protein Domains
  • Tryptophan / metabolism

Substances

  • Anions
  • Kir2.2 channel
  • Membrane Proteins
  • Phosphatidylinositol 4,5-Diphosphate
  • Phospholipids
  • Potassium Channels, Inwardly Rectifying
  • Tryptophan
  • Potassium

Associated data

  • PDB/3JYC
  • PDB/3SPC
  • PDB/3SPI
  • PDB/5KUK
  • PDB/5KUM