Ca2+-induced Ca2+ release activates K+ currents by a cyclic GMP-dependent mechanism in single gastric smooth muscle cells

doi:10.1016/0014-2999(95)00763-6

European Journal of Pharmacology

Volume 298, Issue 2, 7 March 1996, Pages 159-163

https://doi.org/10.1016/0014-2999(95)00763-6 Get rights and content

Abstract

The participation of sarcoplasmic reticulum Ca²⁺ release channels in the activation of Ca²⁺-sensitive K⁺ currents (I_K(Ca)) by cyclic dibutyryl GMP was investigated in smooth muscle cells from the circular layer of guinea-pig gastric fundus. All experiments were performed in the presence of 3 μM nicardipine into the bath and low Ca²⁺ buffering capacity of the pipette-filling solution (pCa 7.4). Ruthenium red (10 μM) as well as its combination with 10 μM heparin abolished the cyclic GMP-induced activation of I_K(Ca), while 10 μM heparin remained ineffective. Ryanodine (10 μM) and the subsequently added 1 μM thapsigargin induced a relatively small increase in I_K(Ca) amplitudes. The addition of 10 μM ryanodine to 1 μM thapsigargin-containing bath solution caused a vast increase in I_K(Ca). It is hypothesyzed that protein kinase G-induced vectorial Ca²⁺ flux from the cell bulk and sarcoplasmic reticulum Ca²⁺ stores toward the plasma membrane is realized by a spontaneous Ca²⁺-induced Ca²⁺ release from a superficially situated Ca²⁺ store.

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The rebound contraction induced by electrical field stimulation (EFS) and nitric oxide (NO) donor, S-nitroso-L-cysteine (cysNO), were investigated in the longitudinal muscle of porcine gastric fundus (LM-PGF). Under the presence of atropine and guanethidine, cysNO and EFS produced sequential relaxation-contraction in LM-PGF. Tetrodotoxin abolished the EFS-induced response, while leaving the cysNO-induced one unaffected. A soluble guanylate cyclase inhibitor, lH-[1,2,4]-oxadiazolo-[4,3-α]-quinoxalin-1-one, inhibited both cysNO and EFS-induced biphasic response. A cGMP analogue only relaxed LM-PGF. A phosphodiesterase V inhibitor, zaprinast, prolonged the cysNO and the EFS-induced relaxation and inhibited the rebound contraction. The rebound contraction was inhibited by verapamil, an L-type Ca²⁺ channel blocker. The cysNO and the EFS-induced biphasic response were inhibited by ryanodine plus cyclopiazonic acid or by ruthenium red, a ryanodine-receptor blocker. LM-PGF was relaxed on exposure to caffeine and then produced a verapamil-sensitive rebound contraction during the washout period. CysNO and EFS did not induce the rebound contraction in the presence of caffeine. These results suggest that the NO-induced rebound contraction involves both Ca²⁺-release from the ryanodine-sensitive store and Ca²⁺-influx through L-type channels. Although the NO-induced biphasic response is dependent on cGMP, rapid removal of cGMP seems necessary for the rebound contraction.
Control of the phasic and tonic contractions of guinea pig stomach by a ryanodine-sensitive Ca<sup>2+</sup> store
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In some smooth muscle cells, the rise in intracellular Ca²⁺ as a result of a Ca²⁺ influx via plasma membrane Ca²⁺ channels can activate a further increase in intracellular Ca²⁺ as a result of Ca²⁺ release from intracellular stores. This study examined the role of the Ca²⁺-induced Ca²⁺ release from the ryanodine-sensitive intracellular Ca²⁺ stores in shaping the smooth muscle contractions of guinea pig stomach. The contractile activity of isolated muscle strips of the fundus, corpus and antrum region of the stomach was recorded under isometric conditions. Ryanodine, an activator of Ca²⁺-induced Ca²⁺ release, concentration dependently (10⁻⁷–3.10⁻⁵ M) increased the tone of fundus and corpus strips. Ryanodine had a dual action on the phasic contractions of the antrum and corpus: increase by the low concentrations (up to 10⁻⁶ M) and inhibition by the high concentrations (10⁻⁶–3.10⁻⁵ M). Nifedipine (10⁻⁵ M) completely inhibited the ryanodine (10⁻⁶ M)-induced phasic contractions and only partly the ryanodine (3.10⁻⁵ M)-induced tonic contractions. In the presence of 10⁻⁵ M cyclopiazonic acid, a specific inhibitor of sarcoplasmic reticulum Ca²⁺-ATPase, ryanodine (3.10⁻⁵ M) further increased the tone of the corpus and fundus strips. Ryanodine (3.10⁻⁵ M) induced tonic contractions in the fundus and corpus precontracted by acetylcholine (10⁻⁵ M), and inhibited the acetylcholine (10⁻⁶ M)-induced phasic contractions in the antrum and corpus. Ruthenium red, an inhibitor of Ca²⁺-induced Ca²⁺ release, concentration dependently (10⁻⁶–10⁻⁴ M) decreased the tone and amplitude of the phasic contractions. The data obtained provide evidence for the participation of a sarcoplasmic reticulum Ca²⁺-induced Ca²⁺ release mechanism in shaping the tonic and phasic contractions of guinea pig stomach, and highlight important tissue differences.
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The effect of the cationic dye, ruthenium red (RR), on ionic fluxes, Ca²⁺ signal generation, and stimulation of aldosterone production was studied in isolated rat adrenal glomerulosa cells. In these cells, increased extracellular [K⁺] as well as angiotensin II (Ang II) elevate cytoplasmic Ca²⁺ concentration and thereupon activate steroidogenesis. However, the mode of action of the two stimuli are different: while a dihidropyridine-sensitive mechanism contributes to the response to both agonists, Ang II induces Ca²⁺ release from intracellular stores and causes capacitative Ca²⁺ influx, whereas K⁺ was recently shown to activate a plasma membrane Ca²⁺ current (I_gl) independently of membrane depolarization. The difference is reflected in the sensitivity of the response of the cells to RR. The Ang II-induced Ca²⁺ signal and aldosterone production were not inhibited, but rather slightly potentiated by the dye. This potentiation was probably the consequence of the membrane-depolarizing effect of RR, due to the observed inhibition of the resting K⁺ conductance. Conversely, Ca²⁺ signal and aldosterone production were significantly reduced by RR when the cells were stimulated by moderately elevated [K⁺] (6–8 mM). Our patch clamp studies suggest that this effect was related to the inhibition of different voltage-dependent and -independent inward Ca²⁺ currents and indicates the functional importance of the latter in the signal transduction of the potassium-stimulated glomerulosa cell.
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2004, Journal of Physiology

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Ca2+-induced Ca2+ release activates K+ currents by a cyclic GMP-dependent mechanism in single gastric smooth muscle cells

Abstract

Eur. J. Pharmacol.

J. Biol. Chem.

J. Biol. Chem.

Nitric oxide and cGMP cause vasorelaxation by activation of a charibdotoxin-sensitive K+ channel by cGMP-dependent protein kinase

Two kinds of spatially separated caffeine-sensitive Ca2+ stores in smooth muscle cells from guinea-pig mesenteric artery

Function of smooth muscle sarcoplasmic reticulum

Modulation of Ca2+ movements by nitroprusside in isolated vascular smooth muscle cells

Pflüg. Arch.

Regulation of intracellular Ca2+ levels in cultured vascular smooth muscle cells

J. Biol. Chem.

Cyclic GMP activation of K+ currents by sarcoplasmic reticulum Ca2+ pump-dependent mechanism

Gen. Physiol. Biophys.

Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells

J. Physiol. (Paris)

Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches

Pflüg. Arch.

Ca²⁺-induced Ca²⁺ release activates K⁺ currents by a cyclic GMP-dependent mechanism in single gastric smooth muscle cells

Nitric oxide and cGMP cause vasorelaxation by activation of a charibdotoxin-sensitive K⁺ channel by cGMP-dependent protein kinase

Two kinds of spatially separated caffeine-sensitive Ca²⁺ stores in smooth muscle cells from guinea-pig mesenteric artery

Modulation of Ca²⁺ movements by nitroprusside in isolated vascular smooth muscle cells

Regulation of intracellular Ca²⁺ levels in cultured vascular smooth muscle cells

Cyclic GMP activation of K⁺ currents by sarcoplasmic reticulum Ca²⁺ pump-dependent mechanism