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Voltage-gated Ca²⁺ entry and ryanodine receptor Ca²⁺-induced Ca²⁺ release in preglomerular arterioles

Department of Cell and Molecular Physiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina

Submitted 17 November 2006 ; accepted in final form 19 December 2006

We have previously shown that in afferent arterioles, angiotensin II (ANG II) involves activation of the inositol trisphosphate receptor (IP₃R), activation of adenine diphosphoribose (ADPR) cyclase, and amplification of the initial IP₃R-stimulated release of cytosolic Ca²⁺ ([Ca²⁺]_i) from the sarcoplasmic reticulum (SR) (Fellner SK, Arendshorst WJ. Am J Physiol Renal Physiol 288: F785–F791, 2004). The response of the ryanodine receptor (RyR) to local increases in [Ca²⁺]_i is defined as calcium-induced calcium release (CICR). To investigate whether Ca²⁺ entry via voltage-gated channels (VGCC) can stimulate CICR, we treated fura 2-loaded, freshly isolated afferent arterioles with KCl (40 mM; high KCl). In control arterioles, peak [Ca²⁺]_i increased by 165 ± 10 nM. Locking the RyR in the closed position with ryanodine (100 µM) inhibited the [Ca²⁺]_i response by 59% (P < 0.01). 8-Br cADPR, a specific blocker of the ability of cyclic ADPR (cADPR) to sensitize the RyR to Ca²⁺, caused a 43% inhibition. We suggest that the lower inhibition by 8-Br cADPR (P = 0.02, ryanodine vs. 8-Br cADPR) represents endogenously active ADPR cyclase. Depletion of SR Ca²⁺ stores by inhibiting the SR Ca²⁺-ATPase with cyclopiazonic acid or thapsigargin blocked the [Ca²⁺]_i responses to KCl by 51% (P not significant vs. ryanodine or 8-Br cADPR). These data suggest that about half of the increase in [Ca²⁺]_i induced by high KCl is accomplished by activation of CICR through the ability of entered Ca²⁺ to expose the RyR to high local concentrations of Ca²⁺ and that endogenous cADPR contributes to the process.

renal microcirculation; cyclic adenine diphosphoribose; afferent arteriole

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