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The Journal of Neuroscience, July 6, 2005, 25(27):6286-6295; doi:10.1523/JNEUROSCI.0628-05.2005

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Cellular/Molecular
Dual Presynaptic Control by ATP of Glutamate Release via Facilitatory P2X₁, P2X_2/3, and P2X₃ and Inhibitory P2Y₁, P2Y₂, and/or P2Y₄ Receptors in the Rat Hippocampus

Ricardo J. Rodrigues,¹ Teresa Almeida,¹ Peter J. Richardson,² Catarina R. Oliveira,¹ and Rodrigo A. Cunha¹

¹Centre for Neurosciences of Coimbra, Institute of Biochemistry, Faculty of Medicine, University of Coimbra, 3004-504 Coimbra, Portugal, and ²Department of Pharmacology, University of Cambridge, Cambridge CB2 1PD, United Kingdom

ATP is released in a vesicular manner from nerve terminals mainly at higher stimulation frequencies. There is a robust expression of ATP (P2) receptors in the brain, but their role is primarily unknown. We report that ATP analogs biphasically modulate the evoked release of glutamate from purified nerve terminals of the rat hippocampus, the facilitation being mediated by P2X₁, P2X_2/3, and P2X₃ [antagonized by 8-(benzamido)naphthalene-1,3,5-trisulfonate and 2',3'-O-(2,4,6-trinitrophenyl)-ATP] and the inhibition by P2Y_1, P2Y₂, and/or P2Y₄ [antagonized by reactive blue 2 and 2'deoxy-N⁶-methyladenosine-3',5'-bisphosphate and mimicked by P1-(urinine 5'-),P4-(inosine 5'-) tetraphosphate and 2-methylthio-ADP] receptors. The combination of single-cell PCR analysis of rat hippocampal pyramidal neurons, Western blot analysis of purified presynaptic active zone fraction, and immunocytochemical analysis of hippocampal glutamatergic terminals revealed that the P2 receptors expressed in glutamatergic neurons, located in the active zone and in glutamatergic terminals, were precisely P2X_1, P2X₂, and P2X₃ subunits and P2Y_1, P2Y₂, and P2Y₄ receptors. This provides coincident functional and molecular evidence that P2 receptors are present and act presynaptically as a modulatory system controlling hippocampal glutamate release.

Key words: ATP; P2X receptors; P2Y receptors; glutamate release; nerve terminals; rat hippocampus

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Received Feb 16, 2005; revised April 11, 2005; accepted May 6, 2005.

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