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1 Department of Cell and Molecular Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
* To whom correspondence should be addressed. E-mail: sfellner{at}med.unc.edu.
In afferent arteriolar vascular smooth muscle cells (VSMC), angiotensin II (Ang II) induces a rise in cytosolic Ca2+ ([Ca2+]i) via inositol trisphosphate receptor (IP3R) stimulation and by activation of the adenine diphosphate ribose (ADPR) cyclase to form cyclic ADPR, which sensitizes the ryanodine receptor (RyR) to Ca2+. We hypothesize that Ang II stimulation of NAD(P)H oxidases leads to the formation of superoxide anion (.O2 -), which, in turn, activates ADPR cyclase. Afferent arterioles were isolated from rat kidney with the magnetized microsphere and sieving technique and loaded with fura-2 to measure [Ca2+]i . Ang II rapidly increased [Ca2+]i by 124 ± 12 nM. In the presence of apocynin, a specific inhibitor of NAD(P)H oxidase assembly, the [Ca2+]i response was reduced to 35 ± 5 nM (P < 0.01). Tempol, a superoxide dismutase (SOD) mimetic, did not alter the [Ca2+]i response to Ang II at a concentration of 10-4 M (99 ± 12 nM), but 10- 3 M tempol reduced the response to 32 ± 3 nM (P < 0.01). Addition of nicotinamide, an inhibitor of ADPR cyclase, to apocynin or tempol (10-3 M) resulted in no further inhibition. Measurement of superoxide production with the fluorescent probe tempo 9- AC showed that Ang II caused an increase of 48 ± 20 arbitrary units; apocynin or diphenyl iodonium (an inhibitor of flavoprotein oxidases) inhibited the response by 94%. Hydrogen peroxide (H2O2) was studied at physiologic (10-7 M) and higher concentrations. In the presence of H2O2 (10-7 M) neither baseline [Ca2+]i nor the response to Ang II were altered (125 ± 15 nM), whereas H2O2 (10-6 and 10-5 M) inhibited the [Ca2+]i response to Ang II by 35 and 46%, respectively. We conclude that Ang II rapidly activates NAD(P)H oxidases of afferent arterioles, leading to the formation of .O2 -, which then stimulates ADPR cyclase to form cADPR. cADPR, by sensitizing the RyR to Ca2+, augments the Ca2+ response (calcium- induced calcium release) initiated by activation of the IP3R.
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