α1-adrenoceptors regulate only the caveolae-located subpopulation of cardiac K(V)4 channels

Channels (Austin). 2010 May-Jun;4(3):168-78. doi: 10.4161/chan.4.3.11479.

Abstract

In ventricular myocytes, α1-AR stimulates Gαs proteins and reduces the transient outward K(+) current (I(to)) via a cAMP/PKA-mediated pathway and thus regulates cardiac contraction and excitability. This I(to) reduction is compartmentalized and limited to discrete membrane regions since PKA-dependent phosphorylation of the I(to) channels after α1-AR stimulation requires the integrity of both the sarcoplasmic membrane and the cytoskeleton. The aim of this work was to investigate the mechanisms involved in the compartmentalization of the PKA-dependent modulation of I(to) in response to α1-AR activation. I(to) current recordings were performed by the Patch-Clamp technique. Membrane rafts from isolated ventricular myocytes were extracted by centrifugation in a sucrose density gradient. The different proteins were visualized by western blot and protein-protein interactions determined by coimmunoprecipitation experiments. Localization of I(to) channel in caveolae, particular subtypes of membrane rafts, was achieved by electron microscopy. Patch-Clamp recordings show that a functional supramolecular complex, kept together by the Akinase anchoring protein AKAP100, exist in caveolae in living myocytes. Density gradients and immunoprecipitation experiments show that the components of the α1-AR/I(to) pathway localize in caveolae, forming two different groups of proteins. The K(V)4.2/K(V)4.3 channel forms a supramolecular complex with PKA through AKAP100 and is attached to caveolae by interacting with caveolin-3. On the other hand, α1-AR, Gαs and adenylate cyclase gather in a second group also connected to caveolin-3. Therefore, both groups of preassembled proteins are maintained in close proximity by caveolin-3. A different I(to) channel population localizes in non-caveolar membrane rafts and is not sensitive to α1-adrenergic regulation.

Publication types

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

MeSH terms

  • Animals
  • Caveolae
  • Caveolin 3 / metabolism*
  • Cell Compartmentation*
  • Heart Ventricles / cytology
  • Membrane Microdomains
  • Multiprotein Complexes / metabolism*
  • Muscle Cells / chemistry
  • Muscle Cells / metabolism
  • Myocardium / chemistry
  • Patch-Clamp Techniques
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Adrenergic / physiology*
  • Receptors, Adrenergic, alpha-1 / physiology*
  • Shal Potassium Channels / metabolism*

Substances

  • Adra1a protein, rat
  • Caveolin 3
  • Multiprotein Complexes
  • Receptors, Adrenergic
  • Receptors, Adrenergic, alpha-1
  • Shal Potassium Channels