KCNE variants reveal a critical role of the beta subunit carboxyl terminus in PKA-dependent regulation of the IKs potassium channel

Channels (Austin). 2009 Jan-Feb;3(1):16-24. doi: 10.4161/chan.3.1.7387. Epub 2009 Jan 7.

Abstract

Co-assembly of KCNQ1 with different accessory, or beta, subunits that are members of the KCNE family results in potassium (K+) channels that conduct functionally distinct currents. The alpha subunit KCNQ1 conducts a slowly activated delayed rectifier K+ current (IKs), a major contributor to cardiac repolarization, when co-assembled with KCNE1 and channels that favor the open state when co-assembled with either KCNE2 or KCNE3. In the heart, stimulation of the sympathetic nervous system enhances IKs. A macromolecular signaling complex of the IKs channel including the targeting protein Yotiao coordinates up or downregulation of channel activity by protein kinase A (PKA) phosphorylation and dephosphorylation of molecules in the complex. beta-adrenergic receptor mediated IKs upregulation, a functional consequence of PKA phosphorylation of the KCNQ1 amino terminus (N-T), requires co-expression of KCNQ1/Yotiao with KCNE1. Here, we report that co-expression of KCNE2, like KCNE1, confers a functional channel response to KCNQ1 phosphorylation, but co-expression of KCNE3 does not. Amino acid sequence comparison among the KCNE peptides, and KCNE1 truncation experiments, reveal a segment of the predicted intracellular KCNE1 carboxyl terminus (C-T) that is necessary for functional transduction of PKA phosphorylated KCNQ1. Moreover, chimera analysis reveals a region of KCNE1 sufficient to confer cAMP-dependent functional regulation upon the KCNQ1_KCNE3_Yotiao channel. The property of specific beta subunits to transduce post-translational regulation of alpha subunits of ion channels adds another dimension to our understanding molecular mechanisms underlying the diversity of regulation of native K+ channels.

Publication types

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

MeSH terms

  • A Kinase Anchor Proteins / metabolism
  • Amino Acid Sequence
  • Animals
  • CHO Cells
  • Cricetinae
  • Cricetulus
  • Cyclic AMP / metabolism
  • Cyclic AMP-Dependent Protein Kinase Catalytic Subunits / metabolism*
  • Humans
  • KCNQ1 Potassium Channel / drug effects
  • KCNQ1 Potassium Channel / genetics
  • KCNQ1 Potassium Channel / metabolism*
  • Membrane Potentials
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Okadaic Acid / pharmacology
  • Phosphorylation
  • Potassium Channels, Voltage-Gated / drug effects
  • Potassium Channels, Voltage-Gated / genetics
  • Potassium Channels, Voltage-Gated / metabolism*
  • Protein Structure, Tertiary
  • Time Factors
  • Transfection

Substances

  • A Kinase Anchor Proteins
  • KCNE2 protein, human
  • KCNE3 protein, human
  • KCNQ1 Potassium Channel
  • Potassium Channels, Voltage-Gated
  • Okadaic Acid
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinase Catalytic Subunits
  • protein kinase A Calpha