Constitutively active phosphodiesterase activity regulates urinary bladder smooth muscle function: critical role of KCa1.1 channel

Am J Physiol Renal Physiol. 2012 Nov 1;303(9):F1300-6. doi: 10.1152/ajprenal.00351.2012. Epub 2012 Aug 15.

Abstract

Pharmacological blockade of cyclic nucleotide phosphodiesterase (PDE) can relax human urinary bladder smooth muscle (UBSM); however, the underlying cellular mechanism is unknown. In this study, we investigated the effects of PDE pharmacological blockade on human UBSM excitability, spontaneous and nerve-evoked contractility, and determined the underlying cellular mechanism mediating these effects. Patch-clamp electrophysiological experiments showed that 3-isobutyl-1-methylxanthine (10 μM), a nonselective PDE inhibitor, caused ∼3.6-fold increase in the transient K(Ca)1.1 channel current frequency and ∼2.5-fold increase in the spontaneous transient hyperpolarization frequency in UBSM-isolated cells. PDE blockade also caused ∼5.6-mV hyperpolarization of the UBSM cell membrane potential. Blocking the K(Ca)1.1 channels with paxilline abolished the spontaneous transient hyperpolarization and the hyperpolarization effect of PDE blockade on the UBSM cell membrane potential. Live cell Ca(2+)-imaging experiments showed that PDE blockade significantly decreased the global intracellular Ca(2+) levels. Attenuation of PDE activity significantly reduced spontaneous phasic contraction amplitude, muscle force integral, duration, frequency, and muscle tone of human UBSM isolated strips. Blockade of PDE also significantly reduced the contraction amplitude, muscle force integral, and duration of the nerve-evoked contractions induced by 20-Hz electrical field stimulation. Pharmacological inhibition of K(Ca)1.1 channels abolished the relaxation effects of PDE blockade on both spontaneous and nerve-evoked contractions in human UBSM-isolated strips. Our data provide strong evidence that in human UBSM PDE is constitutively active, thus maintaining spontaneous UBSM contractility. PDE blockade causes relaxation of human UBSM by increasing transient K(Ca)1.1 channel current activity, hyperpolarizing cell membrane potential, and decreasing the global intracellular Ca(2+).

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • 1-Methyl-3-isobutylxanthine / pharmacology
  • Aged
  • Female
  • Humans
  • In Vitro Techniques
  • Indoles / pharmacology
  • Large-Conductance Calcium-Activated Potassium Channel alpha Subunits / antagonists & inhibitors
  • Large-Conductance Calcium-Activated Potassium Channel alpha Subunits / drug effects
  • Large-Conductance Calcium-Activated Potassium Channel alpha Subunits / physiology*
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Middle Aged
  • Muscle Contraction / drug effects
  • Muscle Contraction / physiology
  • Muscle, Smooth / drug effects
  • Muscle, Smooth / physiology*
  • Patch-Clamp Techniques
  • Phosphodiesterase Inhibitors / pharmacology
  • Phosphoric Diester Hydrolases / drug effects
  • Phosphoric Diester Hydrolases / physiology*
  • Potassium Channel Blockers / pharmacology
  • Urinary Bladder / drug effects
  • Urinary Bladder / physiology*

Substances

  • Indoles
  • KCNMA1 protein, human
  • Large-Conductance Calcium-Activated Potassium Channel alpha Subunits
  • Phosphodiesterase Inhibitors
  • Potassium Channel Blockers
  • paxilline
  • Phosphoric Diester Hydrolases
  • 1-Methyl-3-isobutylxanthine