Contribution of individual subunits to the multimeric P2X(2) receptor: estimates based on methanethiosulfonate block at T336C.

P2X receptors are membrane proteins that incorporate a cation-selective ion channel that can be opened by the binding of extracellular ATP. They associate as hetero- and homo-multimers of currently unknown stoichiometry. In this study, we have used Xenopus laevis oocytes to express rat P2X(2) receptor subunits, which carry a cysteine mutation at position 336. ATP-induced currents at this mutant receptor subunit were blocked by more than 90% when exposed to [2-(trimethylammonium) ethyl] methanethiosulfonate (MTSET), whereas currents from wild-type subunits were not affected. To compare mutant and wild-type channel expression, we introduced an epitope in their extracellular domains and found for both channels a similar linear relationship between antibody binding and currents induced by ATP. To study the contribution of the individual subunits to the block by MTSET, we coinjected different mixtures of wild-type and mutant-encoding mRNAs. We found that the inhibition by MTSET depended linearly on the proportion of mutant subunits, which was clearly contrary to the hypothesis that a single mutant subunit could act in a dominant fashion. Subsequent concatenation of wild-type and mutant-encoding cDNAs resulted in an inhibition by MTSET that also depended linearly on the number of mutant subunits and was independent of the position of the mutant subunit, as long as only two or three P2X(2) subunits were joined. With four or six subunits joined, however, the inhibition by MTSET became strongly position-dependent. The present results show that a "per-subunit" channel block causes the blocking effects of MTSET and they suggest that not four but maximally three subunits actively participate in the channel formation.

[1]  A. Karlin,et al.  Contribution of the beta subunit M2 segment to the ion-conducting pathway of the acetylcholine receptor. , 1998, Biochemistry.

[2]  T. Egan,et al.  A Domain Contributing to the Ion Channel of ATP-Gated P2X2 Receptors Identified by the Substituted Cysteine Accessibility Method , 1998, The Journal of Neuroscience.

[3]  R. North,et al.  Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons , 1995, Nature.

[4]  R. North,et al.  Families of ion channels with two hydrophobic segments. , 1996, Current opinion in cell biology.

[5]  M. Welsh,et al.  Electrophysiological and Biochemical Evidence That DEG/ENaC Cation Channels Are Composed of Nine Subunits* , 1998, The Journal of Biological Chemistry.

[6]  R. North,et al.  Membrane Topology of an ATP-gated Ion Channel (P2X Receptor)* , 1998, The Journal of Biological Chemistry.

[7]  Xinmin Zhang,et al.  Architecture of a K+ Channel Inner Pore Revealed by Stoichiometric Covalent Modification , 1999, Neuron.

[8]  M. Shapiro,et al.  Stoichiometry and arrangement of heteromeric olfactory cyclic nucleotide-gated ion channels. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[9]  D. Julius,et al.  New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptor , 1994, Nature.

[10]  R. North,et al.  Nucleotide receptors , 1997, Current Opinion in Neurobiology.

[11]  Caterina Virginio,et al.  Baculovirus Expression Provides Direct Evidence for Heteromeric Assembly of P2X2 and P2X3 Receptors , 1997, The Journal of Neuroscience.

[12]  M. Tanouye,et al.  Tandem linkage of Shaker K+ channel subunits does not ensure the stoichiometry of expressed channels. , 1992, Biophysical journal.

[13]  R. North,et al.  A new class of ligand-gated ion channel defined by P2X receptor for extracellular ATP , 1994, Nature.

[14]  L. Schild,et al.  The heterotetrameric architecture of the epithelial sodium channel (ENaC) , 1998, The EMBO journal.

[15]  R. North,et al.  Domains of P2X receptors involved in desensitization. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[16]  M. Mayer,et al.  Structure and function of glutamate and nicotinic acetylcholine receptors , 1995, Current Opinion in Neurobiology.

[17]  Y. Jan,et al.  Determination of the subunit stoichiometry of an inwardly rectifying potassium channel , 1995, Neuron.

[18]  B. Bean,et al.  ATP-activated channels in rat and bullfrog sensory neurons: concentration dependence and kinetics , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  R. North,et al.  Identification of amino acid residues contributing to the pore of a P2X receptor , 1997, The EMBO journal.

[20]  A. Nicke,et al.  P2X1 and P2X3 receptors form stable trimers: a novel structural motif of ligand‐gated ion channels , 1998, The EMBO journal.

[21]  H. Guy,et al.  Membrane topology and multimeric structure of a mechanosensitive channel protein of Escherichia coli. , 1996, The EMBO journal.

[22]  R. North,et al.  Pharmacological characterization of heterologously expressed ATP-gated cation channels (P2x purinoceptors). , 1995, Molecular pharmacology.

[23]  S. Choe,et al.  Molecular assembly of the extracellular domain of P2X2, an ATP-gated ion channel. , 1997, Biochemical and biophysical research communications.