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J Neurophysiol 86: 304-311, 2001;
0022-3077/01 $5.00
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The Journal of Neurophysiology Vol. 86 No. 1 July 2001, pp. 304-311
Copyright ©2001 by the American Physiological Society

Nitric Oxide Modulates Ca2+ Channels in Dorsal Root Ganglion Neurons Innervating Rat Urinary Bladder

Naoki Yoshimura, Satoshi Seki, and William C. de Groat

Department of Pharmacology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261

Yoshimura, Naoki, Satoshi Seki, and William C. de Groat. Nitric Oxide Modulates Ca2+ Channels in Dorsal Root Ganglion Neurons Innervating Rat Urinary Bladder. J. Neurophysiol. 86: 304-311, 2001. The effect of a nitric oxide (NO) donor on high-voltage-activated Ca2+ channel currents (ICa) was examined using the whole cell patch-clamp technique in L6-S1 dorsal root ganglion (DRG) neurons innervating the urinary bladder. The neurons were labeled by axonal transport of a fluorescent dye, Fast Blue, injected into the bladder wall. Approximately 70% of bladder afferent neurons exhibited tetrodotoxin (TTX)-resistant action potentials (APs), and 93% of these neurons were sensitive to capsaicin, while the remaining neurons had TTX-sensitive spikes and were insensitive to capsaicin. The peak current density of nimodipine-sensitive L-type Ca2+ channels activated by depolarizing pulses (0 mV) from a holding potential of -60 mV was greater in bladder afferent neurons with TTX-resistant APs (39.2 pA/pF) than in bladder afferent neurons with TTX-sensitive APs (28.9 pA/pF), while the current density of omega -conotoxin GVIA-sensitive N-type Ca2+ channels was similar (43-45 pA/pF) in both types of neurons. In both types of neurons, the NO donor, S-nitroso-N-acetylpenicillamine (SNAP) (500 µM), reversibly reduced (23.4-26.6%) the amplitude of ICa elicited by depolarizing pulses to 0 mV from a holding potential of -60 mV. SNAP-induced inhibition of ICa was reduced by 90% in the presence of omega -conotoxin GVIA but was unaffected in the presence of nimodipine, indicating that NO-induced inhibition of ICa is mainly confined to N-type Ca2+ channels. Exposure of the neurons for 30 min to 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ, 10 µM), an inhibitor of NO-stimulated guanylyl cyclase, prevented the SNAP-induced reduction in ICa. Extracellular application of 8-bromo-cGMP (1 mM) mimicked the effects of NO donors by reducing the peak amplitude of ICa (28.6% of reduction). Action potential configuration and firing frequency during depolarizing current pulses were not altered by the application of SNAP (500 µM) in bladder afferent neurons with TTX-resistant and -sensitive APs. These results indicate that NO acting via a cGMP signaling pathway can modulate N-type Ca2+ channels in DRG neurons innervating the urinary bladder.




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