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Research ArticleNEUROPHARMACOLOGY

P2X Receptor Activation Elicits Transporter-Mediated Noradrenaline Release from Rat Hippocampal Slices

Lilla Papp, Tamás Balázsa, Attila Köfalvi, Ferenc Erdélyi, Gábor Szabó, E. Sylvester Vizi and Beáta Sperlágh
Journal of Pharmacology and Experimental Therapeutics September 2004, 310 (3) 973-980; DOI: https://doi.org/10.1124/jpet.104.066712
Lilla Papp
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Tamás Balázsa
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Attila Köfalvi
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Ferenc Erdélyi
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Gábor Szabó
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E. Sylvester Vizi
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Beáta Sperlágh
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Abstract

This study was designed to test the hypothesis of whether activation of presynaptic P2X receptor-gated ion channels elicits noradrenaline release from central catecholaminergic terminals. ATP, α,β-methylene-adenosine 5′-triphosphate (α,β-methyleneATP), and ADP elicited concentration-dependent [3H]noradrenaline outflow from superfused rat hippocampal slices with the following rank order of agonist potency: α,β-methyleneATP > ATP > ADP. Among P2 receptor antagonists, pyridoxal-phosphate-6-azophenyl-2′,4′-disulphonic acid (30 μM), 4,4′,4′′,4′′′-[carbonylbis(imino-5,1,3-benzenetriyl-bis(carbonylimino))]tetrakis-1,3-benzenedisulfonic acid (100 nM), and 8,8′-[carbonybis(imino-3,1-phenylenecarbonylimino)]bis1,3,5-naphthalenetrisulphonic acid (10 μM) significantly inhibited the outflow of [3H]noradrenaline, evoked by ATP, whereas Brilliant Blue G (100 nM), 2′-deoxy-N6-methyladenosine 3′,5′-bisphosphate tetraammonium (10 μM), the A1 receptor antagonist 8-cyclopentyl-1,3-dipropylxanthine (250 nM), and the A2A receptor antagonist 3,7-dimethyl-1-propargylxanthine (250 nM) were ineffective. Pretreatment with the Gi protein inhibitor pertussis toxin (2.5 μg/ml) did not change the effect of ATP on [3H]noradrenaline outflow. In contrast, a decrease in extracellular pH from 7.4 to 6.6 significantly attenuated the response by ATP. When extracellular Na+ was replaced by choline chloride and in the presence of the noradrenaline uptake inhibitor desipramine (10 μM), the ATP-evoked [3H]noradrenaline outflow was almost completely abolished, indicating that its underlying mechanism is the sodium-dependent reversal of the noradrenaline transporter. Reverse transcription-polymerase chain reaction analysis revealed that mRNA encoding P2X1, P2X2, P2X3, P2X4, P2X6, P2X7, and P2Y1 receptor subunits were expressed in the brainstem containing catecholaminergic nuclei projecting to the hippocampus, whereas mRNA encoding P2X5, P2Y2, P2Y4, and P2Y6 receptors were absent. Taken together, these results indicate that noradrenergic terminals of the rat hippocampus are equipped with presynaptic facilitatory P2X receptors, displaying a pharmacological profile similar to homomeric P2X1 and P2X3 receptors.

Footnotes

  • This study was supported by the Hungarian Research Foundation (Grants OTKA T037457 to B.S. and TS040736 to E.S.V), by the Hungarian Medical Research Council (Grant 472/2003 to B.S.), and by the Volkswagen Foundation (to B.S.).

  • Article, publication date, and citation information can be found at http://jpet.aspetjournals.org.

  • doi:10.1124/jpet.104.066712.

  • ABBREVIATIONS: [3H]NA, [3H]noradrenaline; EFS, electrical field stimulation; α,β-methyleneATP, α,β-methylene-adenosine 5′-triphosphate; PPADS, pyridoxal-phosphate-6-azophenyl-2′,4′-disulphonic acid; NF023, 8,8′-[carbonybis(imino-3,1-phenylenecarbonylimino)]bis1,3,5-naphthalenetrisulphonic acid; NF449, 4,4′,4′′,4′′′-[carbonylbis(imino-5,1,3-benzenetriyl-bis(carbonylimino))]tetrakis-1,3-benzenedisulfonic acid; MRS2179, 2′-deoxy-N6-methyladenosine 3′,5′-bisphosphate tetraammonium; DPCPX, 8-cyclopentyl-1,3-dipropylxanthine; DMPX, 3,7-dimethyl-1-propargylxanthine; TTX, tetrodotoxin; AP-5, D(-)-2-amino-5-phosphonopentanoic acid; CNQX, 6-cyano-7-nitroquinoxaline-2,3-dione-disodium; HPLC, high-performance liquid chromatography; RT, reverse transcription; PCR, polymerase chain reaction.

  • ↵1 These authors contributed equally to the study.

    • Received February 9, 2004.
    • Accepted April 14, 2004.
  • The American Society for Pharmacology and Experimental Therapeutics
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Journal of Pharmacology and Experimental Therapeutics: 310 (3)
Journal of Pharmacology and Experimental Therapeutics
Vol. 310, Issue 3
1 Sep 2004
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Research ArticleNEUROPHARMACOLOGY

P2X Receptor Activation Elicits Transporter-Mediated Noradrenaline Release from Rat Hippocampal Slices

Lilla Papp, Tamás Balázsa, Attila Köfalvi, Ferenc Erdélyi, Gábor Szabó, E. Sylvester Vizi and Beáta Sperlágh
Journal of Pharmacology and Experimental Therapeutics September 1, 2004, 310 (3) 973-980; DOI: https://doi.org/10.1124/jpet.104.066712

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Research ArticleNEUROPHARMACOLOGY

P2X Receptor Activation Elicits Transporter-Mediated Noradrenaline Release from Rat Hippocampal Slices

Lilla Papp, Tamás Balázsa, Attila Köfalvi, Ferenc Erdélyi, Gábor Szabó, E. Sylvester Vizi and Beáta Sperlágh
Journal of Pharmacology and Experimental Therapeutics September 1, 2004, 310 (3) 973-980; DOI: https://doi.org/10.1124/jpet.104.066712
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