AKAP150 contributes to enhanced vascular tone by facilitating large-conductance Ca2+-activated K+ channel remodeling in hyperglycemia and diabetes mellitus

Circ Res. 2014 Feb 14;114(4):607-15. doi: 10.1161/CIRCRESAHA.114.302168. Epub 2013 Dec 9.

Abstract

Rationale: Increased contractility of arterial myocytes and enhanced vascular tone during hyperglycemia and diabetes mellitus may arise from impaired large-conductance Ca(2+)-activated K(+) (BKCa) channel function. The scaffolding protein A-kinase anchoring protein 150 (AKAP150) is a key regulator of calcineurin (CaN), a phosphatase known to modulate the expression of the regulatory BKCa β1 subunit. Whether AKAP150 mediates BKCa channel suppression during hyperglycemia and diabetes mellitus is unknown.

Objective: To test the hypothesis that AKAP150-dependent CaN signaling mediates BKCa β1 downregulation and impaired vascular BKCa channel function during hyperglycemia and diabetes mellitus.

Methods and results: We found that AKAP150 is an important determinant of BKCa channel remodeling, CaN/nuclear factor of activated T-cells c3 (NFATc3) activation, and resistance artery constriction in hyperglycemic animals on high-fat diet. Genetic ablation of AKAP150 protected against these alterations, including augmented vasoconstriction. d-glucose-dependent suppression of BKCa channel β1 subunits required Ca(2+) influx via voltage-gated L-type Ca(2+) channels and mobilization of a CaN/NFATc3 signaling pathway. Remarkably, high-fat diet mice expressing a mutant AKAP150 unable to anchor CaN resisted activation of NFATc3 and downregulation of BKCa β1 subunits and attenuated high-fat diet-induced elevation in arterial blood pressure.

Conclusions: Our results support a model whereby subcellular anchoring of CaN by AKAP150 is a key molecular determinant of vascular BKCa channel remodeling, which contributes to vasoconstriction during diabetes mellitus.

Keywords: calcineurin; hyperglycemia; hypertension; ion channels; potassium channels.

Publication types

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

MeSH terms

  • A Kinase Anchor Proteins / genetics
  • A Kinase Anchor Proteins / metabolism*
  • Animals
  • Diabetes Mellitus, Experimental / genetics
  • Diabetes Mellitus, Experimental / metabolism*
  • Diabetes Mellitus, Experimental / physiopathology
  • Dietary Fats / pharmacology
  • Gene Knock-In Techniques
  • Hyperglycemia / genetics
  • Hyperglycemia / metabolism*
  • Hyperglycemia / physiopathology
  • Hypertension / genetics
  • Hypertension / metabolism
  • Hypertension / physiopathology
  • Large-Conductance Calcium-Activated Potassium Channel beta Subunits / genetics
  • Large-Conductance Calcium-Activated Potassium Channel beta Subunits / metabolism*
  • Large-Conductance Calcium-Activated Potassium Channels / genetics
  • Large-Conductance Calcium-Activated Potassium Channels / metabolism*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Muscle, Smooth, Vascular / metabolism
  • Muscle, Smooth, Vascular / physiology
  • NFATC Transcription Factors / metabolism
  • Peptides / pharmacology
  • Signal Transduction / physiology
  • Toxins, Biological / pharmacology
  • Vasoconstriction / drug effects
  • Vasoconstriction / physiology*

Substances

  • A Kinase Anchor Proteins
  • Akap5 protein, mouse
  • Dietary Fats
  • Kcnmb1 protein, mouse
  • Large-Conductance Calcium-Activated Potassium Channel beta Subunits
  • Large-Conductance Calcium-Activated Potassium Channels
  • NFATC Transcription Factors
  • Nfatc3 protein, mouse
  • Peptides
  • Toxins, Biological
  • iberiotoxin