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Heterogeneity of P2X Receptors in Sympathetic Neurons: Contribution of Neuronal P2X₁ Receptors Revealed Using Knockout Mice

Department of Cell Physiology and Pharmacology, University of Leicester, Leicester, United Kingdom

P2X receptors are highly expressed throughout the nervous system, where ATP has been shown to be a neurotransmitter. The aim of this study was to characterize P2X receptor expression within sympathetic postganglionic neurons from the superior cervical ganglia. Reverse transcription-polymerase chain reaction showed the presence of mRNA for all P2X receptors, raising the possibility of multiple subunit expression within these ganglia. Whole-cell patch-clamp and calcium imaging studies revealed a heterogeneous population of P2X receptors in 70% of neurons. We propose that the heterogeneity in properties could be caused by differential expression and/or subunit composition of the P2X receptor. The dominant phenotype was P2X₂-like; neurons showed slow desensitization, sensitivity to antagonists, and a profile of ionic modulation that is characteristic of P2X₂ receptors: potentiation by acidification and extracellular Zn²⁺ and attenuation by high extracellular Ca²⁺ and pH. A subpopulation of neurons (10-15%) were ,-methylene ATP (,-meATP) sensitive, and in neurons from P2X₁ receptor-deficient mice the ,-meATP response was reduced to 2% of all neurons, demonstrating a direct role for P2X₁ subunits. Control ,-meATP responses were eliminated by high extracellular Ca²⁺ and pH, indicating the presence of heteromeric channels incorporating the properties of P2X₁ and P2X₂ receptors. This study demonstrates that in neurons, the P2X₁ receptor can contribute to the properties of heteromeric P2X receptors. Given the expression of P2X₁ receptors in a range of neurons, it seems likely that regulation of the properties of P2X receptors by this subunit is more widespread.

Address correspondence to: Dr. R. J. Evans, Department of Cell Physiology and Pharmacology, University of Leicester, Leicester, LE1 9HN, UK. E-mail: rje6{at}le.ac.uk

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