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The Journal of Neuroscience, February 15, 2003, 23(4):1246

Intracellular Cross Talk and Physical Interaction between Two Classes of Neurotransmitter-Gated Channels

Éric Boué-Grabot^{1, 4, *}, Carlos Barajas-López^{2, *}, Yassar Chakfe¹, Dominique Blais¹, Danny Bélanger¹, Michel B. Émerit³, and Philippe Séguéla¹

¹ Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, Quebec, Canada H3A 2B4, ² Department of Cell Biology and Anatomy, Queen's University, Kingston, Ontario, Canada K7L 3N6, ³ Institut National de la Santé et de la Recherche Médicale U288, Pitié-Salpêtrière, 75013 Paris, France, and ⁴ Centre National de la Recherche Scientifique Unité Mixte de Recherche 5543, Université Victor Segalen Bordeaux 2, 33076 Bordeaux cedex, France

Fast chemical communications in the nervous system are mediated by several classes of receptor channels believed to be independent functionally and physically. We show here that concurrent activation of P2X₂ ATP-gated channels and 5-HT₃ serotonin-gated channels leads to functional interaction and nonadditive currents (47-73% of the predicted sum) in mammalian myenteric neurons as well as in Xenopus oocytes or transfected human embryonic kidney (HEK) 293 cell heterologous systems. We also show that these two cation channels coimmunoprecipitate constitutively and are associated in clusters. In heterologous systems, the inhibitory cross talk between P2X₂ and 5-HT₃ receptors is disrupted when the intracellular C-terminal domain of the P2X₂ receptor subunit is deleted and when minigenes coding for P2X₂ or 5-HT₃A receptor subunit cytoplasmic domains are overexpressed. Injection of fusion proteins containing the C-terminal domain of P2X₂ receptors in myenteric neurons also disrupts the functional interaction between native P2X₂ and 5-HT₃ receptors. Therefore, activity-dependent intracellular coupling of distinct receptor channels underlies ionotropic cross talks that may significantly contribute to the regulation of neuronal excitability and synaptic plasticity.

Key words: P2X purinoceptor; ATP; 5-HT3; serotonin; ionotropic; ligand-gated cation channel; myenteric neurons

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^* E.B.-G. and C.B.-L. contributed equally to this work.

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Copyright © 2003 Society for Neuroscience  0270-6474/03/2341246-08$05.00/0

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