Reductions in the Cardiac Transient Outward K+ Current Ito Caused by Chronic β-Adrenergic Receptor Stimulation Are Partly Rescued by Inhibition of Nuclear Factor κB

J Biol Chem. 2016 Feb 19;291(8):4156-65. doi: 10.1074/jbc.M115.694984. Epub 2016 Jan 7.

Abstract

The fast transient outward potassium current (Ito,f) plays a critical role in the electrical and contractile properties of the myocardium. Ito,f channels are formed by the co-assembly of the pore-forming α-subunits, Kv4.2 and Kv4.3, together with the accessory β-subunit KChIP2. Reductions of Ito,f are common in the diseased heart, which is also associated with enhanced stimulation of β-adrenergic receptors (β-ARs). We used cultured neonatal rat ventricular myocytes to examine how chronic β-AR stimulation decreases Ito,f. To determine which downstream pathways mediate these Ito,f changes, adenoviral infections were used to inhibit CaMKIIδc, CaMKIIδb, calcineurin, or nuclear factor κB (NF-κB). We observed that chronic β-AR stimulation with isoproterenol (ISO) for 48 h reduced Ito,f along with mRNA expression of all three of its subunits (Kv4.2, Kv4.3, and KChIP2). Inhibiting either CaMKIIδc nor CaMKIIδb did not prevent the ISO-mediated Ito,f reductions, even though CaMKIIδc and CaMKIIδb clearly regulated Ito,f and the mRNA expression of its subunits. Likewise, calcineurin inhibition did not prevent the Ito,f reductions induced by β-AR stimulation despite strongly modulating Ito,f and subunit mRNA expression. In contrast, NF-κB inhibition partly rescued the ISO-mediated Ito,f reductions in association with restoration of KChIP2 mRNA expression. Consistent with these observations, KChIP2 promoter activity was reduced by p65 as well as β-AR stimulation. In conclusion, NF-κB, and not CaMKIIδ or calcineurin, partly mediates the Ito,f reductions induced by chronic β-AR stimulation. Both mRNA and KChIP2 promoter data suggest that the ISO-induced Ito,f reductions are, in part, mediated through reduced KChIP2 transcription caused by NF-κB activation.

Keywords: Ca2+/calmodulin-dependent protein kinase (CaMK); adrenergic receptor; cardiomyocyte; potassium channel; transcription.

Publication types

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

MeSH terms

  • Adrenergic beta-Agonists / pharmacology*
  • Animals
  • Calcineurin / genetics
  • Calcineurin / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / genetics
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism
  • Gene Expression Regulation / drug effects
  • Isoproterenol / pharmacology*
  • Kv Channel-Interacting Proteins / genetics
  • Kv Channel-Interacting Proteins / metabolism*
  • Myocytes, Cardiac / metabolism*
  • NF-kappa B / genetics
  • NF-kappa B / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Adrenergic / genetics
  • Receptors, Adrenergic / metabolism
  • Shal Potassium Channels / genetics
  • Shal Potassium Channels / metabolism
  • Transcription, Genetic / drug effects*

Substances

  • Adrenergic beta-Agonists
  • Kcnip2 protein, rat
  • Kv Channel-Interacting Proteins
  • NF-kappa B
  • Receptors, Adrenergic
  • Shal Potassium Channels
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcineurin
  • Isoproterenol