Role of extracellular Na+, Ca2+-activated Cl- channels and BK channels in the contraction of Ca2+ store-depleted tracheal smooth muscle

Clin Exp Pharmacol Physiol. 2009 Jul;36(7):619-25. doi: 10.1111/j.1440-1681.2008.05115.x.

Abstract

1. In the present study, we investigated the series of events involved in the contraction of tracheal smooth muscle induced by the re-addition of Ca(2+) in an in vitro experimental model in which Ca(2+) stores had been depleted and their refilling had been blocked by thapsigargin. 2. Mean (+/-SEM) contraction was diminished by: (i) inhibitors of store-operated calcium channels (SOCC), namely 100 micromol/L SKF-96365 and 100 micromol/L 1-(2-trifluoromethylphenyl) imidazole (to 66.3 +/- 4.4 and 41.3 +/- 5.2% of control, respectively); (ii) inhibitors of voltage-gated Ca(2+) channels Ca(V)1.2 channels, namely 1 micromol/L nifedipine and 10 micromol/L verapamil (to 86.2 +/- 3.4 and 76.9 +/- 5.9% of control, respectively); and (iii) 20 micromol/L niflumic acid, a non-selective inhibitor of Ca(2+)-dependent Cl(-) channels (to 41.1 +/- 9.8% of control). In contrast, contraction was increased 2.3-fold by 100 nmol/L iberiotoxin, a blocker of the large-conductance Ca(2+)-activated K(+) (BK) channels. 3. Furthermore, contraction was significantly inhibited when Na(+) in the bathing solution was replaced by N-methyl-D-glucamine (NMDG(+)) to 39.9 +/- 7.2% of control, but not when it was replaced by Li(+) (114.5 +/- 24.4% of control). In addition, when Na(+) had been replaced by NMDG(+), contractions were further inhibited by both nifedipine and niflumic acid (to 3.0 +/- 1.8 and 24.4 +/- 8.1% of control, respectively). Nifedipine also reduced contractions when Na(+) had been replaced by Li(+) (to 10.7 +/- 3.4% to control), the niflumic acid had no effect (116.0 +/- 4.5% of control). 4. In conclusion, the data of the present study demonstrate the roles of SOCC, BK channels and Ca(V)1.2 channels in the contractions induced by the re-addition of Ca(2+) to the solution bathing guinea-pig tracheal rings under conditions of Ca(2+)-depleted sarcoplasmic reticulum and inhibition of sarcoplasmic/endoplasmic reticulum calcium ATPase. The contractions were highly dependent on extracellular Na(+), suggesting a role for SOCC in mediating the Na(+) influx.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium / pharmacology
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels, L-Type / physiology
  • Chloride Channels / physiology*
  • Extracellular Fluid / drug effects
  • Extracellular Fluid / physiology
  • Guinea Pigs
  • Large-Conductance Calcium-Activated Potassium Channels / physiology*
  • Male
  • Muscle Contraction / drug effects
  • Muscle Contraction / physiology*
  • Muscle, Smooth / drug effects
  • Muscle, Smooth / physiology
  • Sodium / pharmacology
  • Sodium / physiology*
  • Trachea / drug effects
  • Trachea / physiology*

Substances

  • Calcium Channel Blockers
  • Calcium Channels, L-Type
  • Chloride Channels
  • L-type calcium channel alpha(1C)
  • Large-Conductance Calcium-Activated Potassium Channels
  • Sodium
  • Calcium