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1 Departments of Physiology and Biophysics and Medicine, University of Southern California, Los Angeles, CA, USA
* To whom correspondence should be addressed. E-mail: petipete{at}usc.edu.
ATP release from macula densa (MD) cells into the interstitium of the juxtaglomerular apparatus (JGA) is an integral component of the tubuloglomerular feedback (TGF) mechanism that controls glomerular filtration rate. Since the cells of the JGA express a number of calcium-coupled purinergic receptors, these studies tested the hypothesis that TGF activation triggers a calcium wave which spreads from the MD towards distant cells of the JGA and glomerulus. Ratiometric calcium imaging of the in vitro microperfused isolated JGA-glomerulus complex dissected from rabbits was performed using Fluo-4/Fura-Red and confocal fluorescence microscopy. Activation of TGF by increasing tubular flow rate at the MD rapidly produced a significant elevation in intracellular [Ca2+] ([Ca2+]i) in extraglomerular mesangial cells (by 187.6 ± 45.1 nM) and JG renin granular cells (by 281.4 ± 66.6 nM). Subsequently, cell-to-cell propagation of the calcium signal at a rate of 12.6 ± 1.1 Fm/s was observed upstream towards proximal segments of the afferent arteriole and adjacent glomeruli, as well as towards intraglomerular elements including the most distant podocytes (5.9 ± 0.4 Fm/s). The same calcium wave was observed in non-perfusing glomeruli, causing vasoconstriction and contractions of the glomerular tuft. Gap junction uncoupling, an ATP scavenger enzyme cocktail and pharmacological inhibition of P2 purinergic receptors, but not adenosine A1 receptor blockade, abolished the changes in [Ca2+]i and propagation of the calcium wave. These studies provided evidence that both gap junctional communication and extracellular ATP are integral components of the TGF calcium wave.
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