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The Journal of Neuroscience, September 13, 2006, 26(37):9482-9493; doi:10.1523/JNEUROSCI.1672-06.2006

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Cellular/Molecular
Expression of Multiple P2X Receptors by Glossopharyngeal Neurons Projecting to Rat Carotid Body O₂-Chemoreceptors: Role in Nitric Oxide-Mediated Efferent Inhibition

Verónica A. Campanucci, Min Zhang, Cathy Vollmer, and Colin A. Nurse

Department of Biology, McMaster University, Hamilton, Ontario, Canada L8S 4K1

Correspondence should be addressed to Dr. Verónica A. Campanucci at her present address: Department of Physiology, McGill University, McIntyre Medical Science Building, Room 1129, 3655 Promenade Sir William Osler, Montréal, Québec, Canada H3G 1Y6. Email: veronica.campanucci{at}mcgill.ca

In mammals, ventilation is peripherally controlled by the carotid body (CB), which receives afferent innervation from the petrosal ganglion and efferent innervation from neurons located along the glossopharyngeal nerve (GPN). GPN neurons give rise to the "efferent inhibitory" pathway via a plexus of neuronal nitric oxide (NO) synthase-positive fibers, believed to be responsible for CB chemoreceptor inhibition via NO release. Although NO is elevated during natural CB stimulation by hypoxia, the underlying mechanisms are unclear. We hypothesized that ATP, released by rat CB chemoreceptors (type 1 cells) and/or red blood cells during hypoxia, may directly activate GPN neurons and contribute to NO-mediated inhibition. Using combined electrophysiological, molecular, and confocal immunofluorescence techniques, we detected the expression of multiple P2X receptors in GPN neurons. These receptors involve at least four different purinergic subunits: P2X₂ [and the splice variant P2X_2(b)], P2X₃, P2X₄, and P2X₇. Using a novel coculture preparation of CB type I cell clusters and GPN neurons, we tested the role of P2X signaling on CB function. In cocultures, fast application of ATP, or its synthetic analog 2',3'-O-(4 benzoylbenzoyl)-ATP, caused type I cell hyperpolarization that was prevented in the presence of the NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethyl-imidazoline-1-oxyl-3-oxide potassium. These data suggest that ATP released during hypoxic stress from CB chemoreceptors (and/or red blood cells) will cause GPN neuron depolarization mediated by multiple P2X receptors. Activation of this pathway will lead to calcium influx and efferent inhibition of CB chemoreceptors via NO synthesis and consequent release.

Key words: ATP; CB chemoreceptors; efferent inhibition; glossopharyngeal neurons; hypoxia; NO; P2X receptor

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Received April 19, 2006; revised July 11, 2006; accepted Aug. 7, 2006.

Correspondence should be addressed to Dr. Verónica A. Campanucci at her present address: Department of Physiology, McGill University, McIntyre Medical Science Building, Room 1129, 3655 Promenade Sir William Osler, Montréal, Québec, Canada H3G 1Y6. Email: veronica.campanucci{at}mcgill.ca

This article has been cited by other articles:

				M. Zhang, K. Clarke, H. Zhong, C. Vollmer, and C. A. Nurse Postsynaptic action of GABA in modulating sensory transmission in co-cultures of rat carotid body via GABAA receptors J. Physiol., January 15, 2009; 587(2): 329 - 344. [Abstract] [Full Text] [PDF]

				J. Lopez-Barneo, P. Ortega-Saenz, R. Pardal, A. Pascual, and J. I. Piruat Carotid body oxygen sensing Eur. Respir. J., November 1, 2008; 32(5): 1386 - 1398. [Abstract] [Full Text] [PDF]

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