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Abstract:

To gain insight into the way that P2X2 receptors localized at synapses might function, we explored the properties of outside-out patches containing many of these channels as ATP was very rapidly applied and removed. Using a new method to calibrate the speed of exchange of solution over intact patches, we were able to reliably produce applications of ATP lasting <200 μs. For all concentrations of ATP, there was a delay of at least 80 μs between the time when ATP arrived at the receptor and the first detectable flow of inward current. In response to 200-μs pulses of ATP, the time constant of the rising phase of the current was ∼600 μs. Thus, most channel openings occurred when no free ATP was present. The current deactivated with a time constant of ∼60 ms. The amplitude of the peak response to a brief pulse of a saturating concentration of ATP was ∼70% of that obtained during a long application of the same concentration of ATP. Thus, ATP leaves fully liganded channels without producing an opening at least 30% of the time. Extensive kinetic modeling revealed three different schemes that fit the data well, a sequential model and two allosteric models. To account for the delay in opening at saturating ATP, it was necessary to incorporate an intermediate closed state into all three schemes. These kinetic properties indicate that responses to ATP at synapses that use homomeric P2X2 receptors would be expected to greatly outlast the duration of the synaptic ATP transient produced by a single presynaptic spike. Like NMDA receptors, P2X2 receptors provide the potential for complex patterns of synaptic integration over a time scale of hundreds of milliseconds. © The Rockefeller University Press.

Registro:

Documento: Artículo
Título:Responses of rat P2X2 receptors to ultrashort pulses of ATP provide insights into ATP binding and channel gating
Autor:Moffatt, L.; Hume, R.I.
Filiación:Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, United States
Instituto de Química Física de Los Materiales, Medio Ambiente Y Energía, Consejo Nacional de Investigaciones Científicas Y Técnicas, Universidad de Buenos Aires, Buenos Aires, 1428, Argentina
Palabras clave:adenosine triphosphate; n methyl dextro aspartic acid receptor; purine P2X2 receptor; adenosine triphosphate; purine P2 receptor; purine P2X2 receptor; allosterism; article; channel gating; embryo; human; human cell; kinetics; synapse; animal; biological model; cell line; dose response; drug effect; electrophysiology; patch clamp; physiology; protein binding; rat; time; Adenosine Triphosphate; Animals; Cell Line; Dose-Response Relationship, Drug; Electrophysiology; Humans; Ion Channel Gating; Models, Biological; Patch-Clamp Techniques; Protein Binding; Rats; Receptors, Purinergic P2; Synapses; Time Factors
Año:2007
Volumen:130
Número:2
Página de inicio:183
Página de fin:201
DOI: http://dx.doi.org/10.1085/jgp.200709779
Título revista:Journal of General Physiology
Título revista abreviado:J. Gen. Physiol.
ISSN:00221295
CODEN:JGPLA
CAS:adenosine triphosphate, 15237-44-2, 56-65-5, 987-65-5; Adenosine Triphosphate, 56-65-5; purinoceptor P2X2; Receptors, Purinergic P2
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00221295_v130_n2_p183_Moffatt

Referencias:

  • Banke, T.G., Traynelis, S.F., Activation of NR1/NR2B NMDA receptors (2003) Nat. Neurosci, 6, pp. 144-152
  • Barry, P.H., Lynch, J.W., Liquid junction potentials and small cell effects in patch-clamp analysis (1991) J. Membr. Biol, 121, pp. 101-117
  • Bartoletti, S., Flury, B.D., Nel, D.G., Allometric extension (1999) Biometrics, 55, pp. 1210-1214
  • Beato, M., Groot-Kormelink, P.J., Colquhoun, D., Sivilotti, L.G., The activation mechanism of ?1 homomeric glycine receptors (2004) J. Neurosci, 24, pp. 895-906
  • Brooks, S.P., Storey, K.B., Bound and determined: A computer program for making buffers of defined ion concentrations (1992) Anal. Biochem, 201, pp. 119-126
  • Burnstock, G., Physiology and pathophysiology of purinergic neurotransmission (2007) Physiol. Rev, 87, pp. 659-797
  • Burzomato, V., Beato, M., Groot-Kormelink, P.J., Colquhoun, D., Sivilotti, L.G., Single-channel behavior of heteromeric α1β glycine receptors: An attempt to detect a conformational change before the channel opens (2004) J. Neurosci, 24, pp. 10924-10940
  • Clyne, J.D., LaPointe, L.D., Hume, R.I., The role of histidine residues in modulation of the rat P2X2 purinoceptor by zinc and pH (2002) J. Physiol, 539, pp. 347-359
  • Clyne, J.D., Brown, T.C., Hume, R.I., Expression level dependent changes in the properties of P2X2 receptors (2003) Neuropharmacology, 44, pp. 403-412
  • Cockayne, D.A., Dunn, P.M., Zhong, Y., Rong, W.F., Hamilton, S.G., Knight, G.E., Ruan, H.Z., Nunn, P., P2X(2) knockout mice and P2X(2)/P2X(3) double knockout mice reveal a role for the P2X(2) receptor subunit in mediating multiple sensory effects of ATP (2005) J. Physiol, 567, pp. 621-639
  • Colquhoun, D., Sivilotti, L.G., Function and structure in glycine receptors and some of their relatives (2004) Trends Neurosci, 27, pp. 337-344
  • Colquhoun, D., Jonas, P., Sakmann, B., Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices (1992) J. Physiol, 458, pp. 261-287
  • Cotrina, M.L., Lin, J.H., Lopez-Garcia, J.C., Naus, C.C., Nedergaard, M., ATP-mediated glia signaling (2000) J. Neurosci, 20, pp. 2835-2844
  • Diamond, J.S., Neuronal glutamate transporters limit activation of NMDA receptors by neurotransmitter spillover on CA1 pyramidal cells (2001) J. Neurosci, 21, pp. 8328-8338
  • Ding, S., Sachs, F., Single channel properties of P2X2 purinoceptors (1999) J. Gen. Physiol, 113, pp. 695-719
  • Ding, S., Sachs, F., Inactivation of P2X(2) purinoceptors by divalent cations (2000) J. Physiol, 522, pp. 199-214
  • Ding, S., Sachs, F., Evidence for non-independent gating of P2X2 receptors expressed in Xenopus oocytes (2002) BMC Neurosci, 3, p. 17
  • Dzubay, J.A., Jahr, C.E., Kinetics of NMDA channel opening (1996) J. Neurosci, 16, pp. 4129-4134
  • Evans, R.J., Lewis, C., Virginio, C., Lundstrom, K., Buell, G., Surprenant, A., North, R.A., Ionic permeability of, and divalent cation effects on, two ATP-gated cation channels (P2X receptors) expressed in mammalian cells (1996) J. Physiol, 497, pp. 413-422
  • Finger, T.E., Danilova, V., Barrows, J., Bartel, D.L., Vigers, A.J., Stone, L., Hellekant, G., Kinnamon, S.C., ATP signaling is crucial for communication from taste buds to gustatory nerves (2005) Science, 310, pp. 1495-1499
  • Franke, C., Koltgen, D., Hatt, H., Dudel, J., Activation and desensitization of embryonic-like receptor channels in mouse muscle by acetylcholine concentration steps (1992) J. Physiol, 451, pp. 145-158
  • Fujiwara, Y., Kubo, Y., Density-dependent changes of the pore properties of the P2X2 receptor channel (2004) J. Physiol, 558, pp. 31-43
  • Fujiwara, Y., Kubo, Y., Regulation of the desensitization and ion selectivity of ATP-gated P2X2 channels by phosphoinositides (2006) J. Physiol, 576, pp. 135-149
  • Gentet, L.J., Clements, J.D., Binding site stoichiometry and the effects of phosphorylation on human α1 homomeric glycine receptors (2002) J. Physiol, 544, pp. 97-106
  • Grewer, C., Investigation of the α1-glycine receptor channelopening kinetics in the submillisecond time domain (1999) Biophys. J, 77, pp. 727-738
  • Hell, J.W., Edelmann, L., Hartinger, J., Jahn, R., Functional reconstitution of the γ-aminobutyric acid transporter from synaptic vesicles using artificial ion gradients (1991) Biochemistry, 30, pp. 11795-11800
  • Horrigan, F.T., Aldrich, R.W., Coupling between voltage sensor activation, Ca2+ binding and channel opening in large conductance (BK) potassium channels (2002) J. Gen. Physiol, 120, pp. 267-305
  • Huang, Y.J., Maruyama, Y., Dvoryanchikov, G., Pereira, E., Chaudhari, N., Roper, S.D., The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds (2007) Proc. Natl. Acad. Sci. USA, 104, pp. 6436-6441
  • Jayaraman, V., Thiran, S., Hess, G.P., How fast does the γ-aminobutyric acid receptor channel open? Kinetic investigations in the microsecond time region using a laser-pulse photolysis technique (1999) Biochemistry, 38, pp. 11372-11378
  • Kanjhan, R., Housley, G.D., Burton, L.D., Christie, D.L., Kippenberger, A., Thorne, P.R., Luo, L., Ryan, A.F., Distribution of the P2X(2) receptor subunit of the ATP-gated ion channels in the rat central nervous system (1999) J. Comp. Neurol, 407, pp. 11-32
  • Khakh, B.S., Bao, X.R., Labarca, C., Lester, H.A., Neuronal P2X transmitter-gated cation channels change their ion selectivity in seconds (1999) Nat. Neurosci, 2, pp. 322-330
  • Khakh, B.S., W.B. Smith, C.S. Chiu, D.H. Ju, N. Davidson, and H.A. Lester. 2001. Activation-dependent changes in receptor distribution and dendritic morphology in hippocampal neurons expressing P2X(2)-green fluorescent protein receptors. Proc. Natl. Acad. Sci. USA. 98:5288-5293. (published erratum appears in Proc. Natl. Acad. Sci. USA. 2001. 98:7647); Khakh, B.S., Gittermann, D., Cockayne, D.A., Jones, A., ATP modulation of excitatory synapses onto interneurons (2003) J. Neurosci, 23, pp. 7426-7437
  • Kraushaar, U., Jonas, P., Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse (2000) J. Neurosci, 20, pp. 5594-5607
  • Land, B.R., Harris, W.V., Salpeter, E.E., Salpeter, M.M., Diffusion and binding constants for acetylcholine derived from the falling phase of miniature endplate currents (1984) Proc. Natl. Acad. Sci. USA, 81, pp. 1594-1598
  • Li, G., Pei, W., Niu, L., Channel-opening kinetics of GluR2Q(flip) AMPA receptor: A laser-pulse photolysis study (2003) Biochemistry, 42, pp. 12358-12366
  • Li, H., Nowak, L.M., Gee, K.R., Hess, G.P., Mechanism of glutamate receptor-channel function in rat hippocampal neurons investigated using the laser-pulse photolysis (LaPP) technique (2002) Biochemistry, 41, pp. 4753-4759
  • MacDermott, A.B., Mayer, M.L., Westbrook, G.L., NMDAreceptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones (1986) Nature, 321, pp. 519-522
  • Matsubara, N., Billington, A.P., Hess, G.P., How fast does an acetylcholine receptor channel open? Laser-pulse photolysis of an inactive precursor of carbamoylcholine in the microsecond time region with BC3H1 cells (1992) Biochemistry, 31, pp. 5507-5514
  • Mayer, M.L., Westbrook, G.L., Buthrie, P.B., Voltagedependent block by Mg2+ of NMDA responses in spinal cord neurones (1984) Nature, 309, pp. 261-263
  • Mayer, M.L., Westbrook, G.L., Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurones (1987) J. Physiol, 394, pp. 501-527
  • Monod, J., Wyman, J., Changeux, J.P., On nature of allosteric transitions - A plausible model (1965) J. Mol. Biol, 12, pp. 88-118
  • North, R.A., Molecular physiology of P2X receptors (2002) Physiol. Rev, 82, pp. 1013-1067
  • Pankratov, Y., Lalo, U., Verkhratsky, A., North, R.A., Quantal release of ATP in mouse cortex (2007) J. Gen. Physiol, 129, pp. 257-265
  • Pankratov, Y.V., Lalo, U.V., Krishtal, O.A., Role for P2X receptors in long-term potentiation (2002) J. Neurosci, 22, pp. 8363-8369
  • Popescu, G., Auerbach, A., Model gating of NMDA receptors and the shape of their synaptic response (2003) Nat. Neurosci, 6, pp. 476-483
  • Puthussery, T., Fletcher, E.L., P2X2 receptors on ganglion and amacrine cells in cone pathways of the rat retina (2006) J. Comp. Neurol, 496, pp. 595-609
  • Reid, C.A., Bekkers, J.M., Clements, J.D., N- and P/Q-type Ca2+ channels mediate transmitter release with a similar cooperativity at rat hippocampal autapses (1998) J. Neurosci, 18, pp. 2849-2855
  • Ren, J., Bian, X.C., DeVries, M., Schnegelsberg, B., Cockayne, D.A., Ford, A., Galligan, J.J., P2X(2) subunits contribute to fast synaptic excitation in myenteric neurons of the mouse small intestine (2003) J. Physiol, 552, pp. 809-821
  • Rogers, A.W., Darzynkiewicz, Z., Barnard, E.A., Salpeter, M.M., Number and location of acetylcholinesterase molecules at motor endplates of the mouse (1966) Nature, 210, pp. 1003-1006
  • Romanov, R.A., Rogachevskaja, O.A., Bystrova, M.F., Jiang, P., Margolskee, R.F., Kolesnikov, S.S., Afferent neurotransmission mediated by hemichannels in mammalian taste cells (2007) EMBO J, 26, pp. 657-667
  • Rubio, M.E., Soto, F., Distinct localization of P2X receptors at excitatory postsynaptic specializations (2001) J. Neurosci, 21, pp. 641-653
  • Sachs, F., Practical limits on the maximal speed of solution exchange for patch clamp experiments (1999) Biophys. J, 77, pp. 682-690
  • Stiles, J.R., Kovyazina, I.V., Salpeter, E.E., Salpeter, M.M., The temperature sensitivity of miniature endplate currents is mostly governed by channel gating: Evidence from optimized recordings and Monte Carlo simulations (1999) Biophys. J, 77, pp. 1177-1187
  • Stilson, S., McClellan, A., Devasia, S., High-speed solution switching using piezo-based micropositioning stages (2001) IEEE Trans. Biomed. Eng, 48, pp. 806-814
  • Stout, C.E., Costantin, J.L., Naus, C.C., Charles, A.C., Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels (2002) J. Biol. Chem, 277, pp. 10482-10488
  • Tang, C.M., Dichter, M., Morad, M., Modulation of the N-methyl-D-aspartate channel by extracellular H+ (1990) Proc. Natl. Acad. Sci. USA, 87, pp. 6445-6449
  • Tong, G., Jahr, C.E., Block of glutamate transporters potentiates postsynaptic excitation (1994) Neuron, 13, pp. 1195-1203
  • Traynelis, S.F., Cull-Candy, S.G., Proton inhibition of N-methyl-D-aspartate receptors in cerebellar neurons (1990) Nature, 345, pp. 347-350
  • Virginio, C., MacKenzie, A., Rassendren, F.A., North, R.A., Surprenant, A., Pore dilation of neuronal P2X receptor channels (1999) Nat. Neurosci, 2, pp. 315-321
  • Westbrook, G.L., Mayer, M.L., Micromolar concentrations of Zn2+ antagonize NMDA and GABA responses of hippocampal neurons (1987) Nature, 328, pp. 640-643
  • Westfall, T.D., Kennedy, C., Sneddon, P., Enhancement of sympathetic purinergic neurotransmission in the guinea-pig isolated vas deferens by the novel ecto-ATPase inhibitor ARL 67156 (1996) Br. J. Pharmacol, 117, pp. 867-872
  • Wildman, S.S., King, B.F., Burnstock, G., Zn2+ modulation of ATP-responses at recombinant P2X2 receptors and its dependence on extracellular pH (1998) Br. J. Pharmacol, 123, pp. 1214-1220
  • Xia, Z., Dudek, H., Miranti, C.K., Greenberg, M.E., Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism (1996) J. Neurosci, 16, pp. 5425-5436
  • Zafra, F., Aragon, C., Olivares, L., Danbolt, N., Gimenez, C., Storm-Mathisen, J., Glycine transporters are differentially expressed among CNS cells (1995) J. Neurosci, 15, pp. 3952-3969
  • Zhou, Z., Hume, R.I., Two mechanisms for inward rectification of current flow through the purinoceptor P2X(2) class of ATP-gated channels (1998) J. Physiol, 507, pp. 353-364

Citas:

---------- APA ----------
Moffatt, L. & Hume, R.I. (2007) . Responses of rat P2X2 receptors to ultrashort pulses of ATP provide insights into ATP binding and channel gating. Journal of General Physiology, 130(2), 183-201.
http://dx.doi.org/10.1085/jgp.200709779
---------- CHICAGO ----------
Moffatt, L., Hume, R.I. "Responses of rat P2X2 receptors to ultrashort pulses of ATP provide insights into ATP binding and channel gating" . Journal of General Physiology 130, no. 2 (2007) : 183-201.
http://dx.doi.org/10.1085/jgp.200709779
---------- MLA ----------
Moffatt, L., Hume, R.I. "Responses of rat P2X2 receptors to ultrashort pulses of ATP provide insights into ATP binding and channel gating" . Journal of General Physiology, vol. 130, no. 2, 2007, pp. 183-201.
http://dx.doi.org/10.1085/jgp.200709779
---------- VANCOUVER ----------
Moffatt, L., Hume, R.I. Responses of rat P2X2 receptors to ultrashort pulses of ATP provide insights into ATP binding and channel gating. J. Gen. Physiol. 2007;130(2):183-201.
http://dx.doi.org/10.1085/jgp.200709779