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The Journal of Neuroscience, July 20, 2005, 25(29):6911-6920; doi:10.1523/JNEUROSCI.0561-05.2005

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Cellular/Molecular
An Angstrom Scale Interaction between Plasma Membrane ATP-Gated P2X₂ and ₄₂ Nicotinic Channels Measured with Fluorescence Resonance Energy Transfer and Total Internal Reflection Fluorescence Microscopy

Baljit S. Khakh,¹ James A. Fisher,¹ Raad Nashmi,² David N. Bowser,¹ and Henry A. Lester²

¹Medical Research Council Laboratory of Molecular Biology, Cambridge CB2 2QH, United Kingdom, and ²Division of Biology, California Institute of Technology, Pasadena, California 91125

Structurally distinct nicotinic and P2X channels interact functionally, such that coactivation results in cross-inhibition of one or both channel types. It is hypothesized, but not yet proven, that nicotinic and P2X channels interact at the plasma membrane. Here, we show that plasma membrane ₄₂ nicotinic and P2X₂ channels form a molecular scale partnership and also influence each other when coactivated, resulting in nonadditive cross-inhibitory responses. Total internal reflection fluorescence and fluorescence resonance energy transfer microscopy between fluorescently labeled P2X₂ and ₄₂ nicotinic channels demonstrated close spatial arrangement of the channels in human embryonic kidney cells and in hippocampal neuron membranes. The data suggest that P2X₂ and ₄₂ channels may form a dimer, with the channels 80 Å apart. The measurements also show that P2X₂ subunits interact specifically and robustly with the ₂ subunits in ₄₂ channels. The data provide direct evidence for the close spatial apposition of full-length P2X₂ and ₄₂ channels within 100 nm of the plasma membrane of living cells.

Key words: channel; cholinergic; purinergic; acetylcholine receptor; ACh; fluorescence microscopy; P2X

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Received Feb 10, 2005; revised June 13, 2005; accepted June 14, 2005.

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