Ca(2+) movement from leaky sarcoplasmic reticulum during contraction of rat arterial smooth muscles.

To examine the Ca(2+) buffering function of the sarcoplasmic reticulum during arterial contraction, we studied Ca(2+) movement during stimulation with K(+) or norepinephrine in arteries with a leaky sarcoplasmic reticulum. Responses were compared in endothelium-denuded strips of femoral, mesenteric and carotid arteries of the rat. To make the sarcoplasmic reticulum leaky to Ca(2+), Ca(2+)-induced Ca(2+) release channels of the sarcoplasmic reticulum were locked open by treatment with ryanodine plus caffeine. After ryanodine treatment, the contractile responses to K(+) (3-20 mM) were augmented when compared with control responses in femoral and mesenteric arteries, but were inhibited in the carotid artery. Similar results were obtained when the contractile responses to norepinephrine were determined. The inhibition by ryanodine of the K(+)- or norepinephrine-contractions seen in the carotid artery was reversed by pretreatment with cyclopiazonic acid (10 microM), an inhibitor of the sarcoplasmic reticulum Ca(2+)-ATPase, but was not by charybdotoxin (100 nM), a blocker of Ca(2+)-activated K(+) channels. We conclude that (1) after ryanodine treatment, Ca(2+) entering from the extracellular space during stimulation with K(+) or norepinephrine is first taken up into the leaky sarcoplasmic reticulum and then reaches the myofilaments in femoral and mesenteric arteries, while in the carotid artery, Ca(2+) leaked from the sarcoplasmic reticulum reaches mainly the plasma membrane from where it is extruded into the extracellular space, and (2) the different movement of Ca(2+) may be due to the relative location of the sarcoplasmic reticulum in the smooth muscle cell of each artery.