Domain organization of the ATP-sensitive potassium channel complex examined by fluorescence resonance energy transfer

J Biol Chem. 2013 Feb 8;288(6):4378-88. doi: 10.1074/jbc.M112.388629. Epub 2012 Dec 6.

Abstract

K(ATP) channels link cell metabolism to excitability in many cells. They are formed as tetramers of Kir6.2 subunits, each associated with a SUR1 subunit. We used mutant GFP-based FRET to assess domain organization in channel complexes. Full-length Kir6.2 subunits were linked to YFP or cyan fluorescent protein (CFP) at N or C termini, and all such constructs, including double-tagged YFP-Kir6.2-CFP (Y6.2C), formed functional K(ATP) channels. In intact COSm6 cells, background emission of YFP excited by 430-nm light was ∼6%, but the Y6.2C construct expressed alone exhibited an apparent FRET efficiency of ∼25%, confirmed by trypsin digestion, with or without SUR1 co-expression. Similar FRET efficiency was detected in mixtures of CFP- and YFP-tagged full-length Kir6.2 subunits and transmembrane domain only constructs, when tagged at the C termini but not at the N termini. The FRET-reported Kir6.2 tetramer domain organization was qualitatively consistent with Kir channel crystal structures: C termini and M2 domains are centrally located relative to N termini and M1 domains, respectively. Additional FRET analyses were performed on cells in which tagged full-length Kir6.2 and tagged SUR1 constructs were co-expressed. These analyses further revealed that 1) NBD1 of SUR1 is closer to the C terminus of Kir6.2 than to the N terminus; 2) the Kir6.2 cytoplasmic domain is not essential for complexation with SUR1; and 3) the N-terminal half of SUR1 can complex with itself in the absence of either the C-terminal half or Kir6.2.

Publication types

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

MeSH terms

  • ATP-Binding Cassette Transporters / genetics
  • ATP-Binding Cassette Transporters / metabolism*
  • Animals
  • COS Cells
  • Chlorocebus aethiops
  • Cricetinae
  • Fluorescence Resonance Energy Transfer
  • KATP Channels / genetics
  • KATP Channels / metabolism*
  • Mice
  • Potassium Channels, Inwardly Rectifying / genetics
  • Potassium Channels, Inwardly Rectifying / metabolism*
  • Protein Structure, Tertiary
  • Receptors, Drug / genetics
  • Receptors, Drug / metabolism*
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Sulfonylurea Receptors

Substances

  • ATP-Binding Cassette Transporters
  • Abcc8 protein, mouse
  • KATP Channels
  • Potassium Channels, Inwardly Rectifying
  • Receptors, Drug
  • Recombinant Fusion Proteins
  • Sulfonylurea Receptors
  • uK-ATP-1 potassium channel