Agonist antagonist interactions at the rapidly desensitizing P2X3 receptor

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Helms, Nick ^a   Kowalski, Maria ^a   Illes, Peter ^a   Riedel, Thomas ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5 [[(3 PHENOXYBENZYL)(1,2,3,4 TETRAHYDRO 1 NAPHTHYL)AMINO]CARBONYL]TRIMELLITIC ACID; ALPHA,BETA METHYLENEADENOSINE TRIPHOSPHATE; PURINERGIC P2X3 RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; PURINERGIC RECEPTOR STIMULATING AGENT; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; TNP ATP; UNCLASSIFIED DRUG;

ARTICLE; BINDING COMPETITION; CONTROLLED STUDY; DISSOCIATION CONSTANT; DRUG BINDING SITE; DRUG SELECTIVITY; HUMAN; HUMAN CELL; INTRACELLULAR RECORDING; MOLECULAR INTERACTION; PATCH CLAMP TECHNIQUE; RECEPTOR DOWN REGULATION; SIMULATION; STATISTICAL MODEL; WHOLE CELL; WILD TYPE;

ADENOSINE TRIPHOSPHATE; BINDING SITES; BINDING, COMPETITIVE; DRUG INTERACTIONS; HEK293 CELLS; HUMANS; KINETICS; MARKOV CHAINS; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; MUTATION; PATCH-CLAMP TECHNIQUES; PHENOLS; POLYCYCLIC COMPOUNDS; PROTEIN BINDING; PURINERGIC P2 RECEPTOR AGONISTS; PURINERGIC P2 RECEPTOR ANTAGONISTS; PYRIDOXAL PHOSPHATE; RECEPTORS, PURINERGIC P2X3;

EID: 84891426451     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079213     Document Type: Article

References (36)

1. Khakh BS, North RA (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442: 527-532. doi:10.1038/nature04886. PubMed: 16885977.
2. Köles L, Gerevich Z, Oliveira JF, Zadori ZS, Wirkner K et al. (2008) Interaction of P2 purinergic receptors with cellular macromolecules. Naunyn Schmiedebergs Arch Pharmacol 377: 1-33. doi:10.1007/s00210-007-0222-2. PubMed: 18273661.
3. Newbolt A, Stoop R, Virginio C, Surprenant A, North RA et al. (1998) Membrane Topology of an ATP-gated Ion Channel (P2X Receptor). J Biol Chem 273: 15177-15182. doi:10.1074/jbc.273.24.15177.
4. North RA (2002) Molecular Physiology of P2X Receptors. Physiol Rev 82: 1013-1067. doi:10.1152/physrev.00015.2002. PubMed: 12270951.
5. Kawate T, Michel JC, Birdsong WT, Gouaux E (2009) Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 460: 592-598. doi:10.1038/nature08198. PubMed: 19641588.
6. Khakh BS, Burnstock G, Kennedy C, King BF, North RA et al. (2001) International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacol Rev 53: 107-118. PubMed: 11171941.
7. Chizh BA, Illes P (2001) P2X receptors and nociception. Pharmacol Rev 53: 553-568. PubMed: 11734618.
8. Burnstock G (2009) Purinergic receptors and pain. Curr Pharm Des 15: 1717-1735. doi:10.2174/138161209788186335. PubMed: 19442186.
9. Chen C-C, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G et al. (1995) A P2X purinoceptor expressed by a subset of sensory neurons. Nature 377: 428-431. doi:10.1038/377428a0. PubMed: 7566119.
10. Lewis C, Neidhart S, Holy C, North RA, Buell G et al. (1995) Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377: 432-435. doi:10.1038/377432a0. PubMed: 7566120.
11. Burnstock G, Krügel U, Abbracchio MP, Illes P (2011) Purinergic signalling: From normal behaviour to pathological brain function. Prog Neurobiol Available: http://www.ncbi.nlm.nih.gov/pubmed/21907261. Accessed 19 September 2011 PubMed: 21907261.
12. Kennedy C, Assis TS, Currie AJ, Rowan EG (2003) Crossing the pain barrier: P2 receptors as targets for novel analgesics. J Physiol Lond 553: 683-694. doi:10.1113/jphysiol.2003.049114. PubMed: 14514872.
13. Wirkner K, Sperlagh B, Illes P (2007) P2X3 Receptor Involvement in Pain States. Mol Neurobiol 36: 165-183. doi:10.1007/s12035-007-0033-y. PubMed: 17952660.
14. Neelands TR, Burgard EC, Uchic ME, McDonald HA, Niforatos W et al. (2003) 2′, 3′-O-(2,4,6,Trinitrophenyl)-ATP and A-317491 are competitive antagonists at a slowly desensitizing chimeric human P2X3 receptor. Br J Pharmacol 140: 202-210. doi:10.1038/sj.bjp.0705411. PubMed: 12967950.
15. Spelta V, Jiang L-H, Surprenant A, North RA (2002) Kinetics of antagonist actions at rat P2X2/3 heteromeric receptors. Br J Pharmacol 135: 1524-1530. doi:10.1038/sj.bjp.0704591. PubMed: 11906966.
16. Riedel T, Wiese S, Leichsenring A, Illes P (2012) Effects of Nucleotide Analogues at the P2X3 Receptor and its Mutants Identify the Agonist Binding Pouch. Molecular Pharmacology. Available: http://molpharm.aspetjournals.org/ content/early/2012/04/11/mol.112.077818.abstract.
17. Bodnar M, Wang H, Riedel T, Hintze S, Kato E et al. (2011) Amino acid residues constituting the agonist binding site of the human P2X3 receptor. J Biol Chem 286: 2739-2749. doi:10.1074/jbc.M110.167437. PubMed: 21098022.
18. Milescu LS, Akk G, Sachs F (2005) Maximum Likelihood Estimation of Ion Channel Kinetics from Macroscopic Currents. Biophys J 88: 2494-2515. doi:10.1529/biophysj.104.053256. PubMed: 15681642.
19. Virginio C, Robertson G, Surprenant A, North RA (1998) Trinitrophenyl-Substituted Nucleotides Are Potent Antagonists Selective for P2X1, P2X3, and Heteromeric P2X2/3 Receptors. Mol Pharmacol 53: 969-973. PubMed: 9614197.
20. Jarvis MF, Burgard EC, McGaraughty S, Honore P, Lynch K et al. (2002) A-317491, a novel potent and selective non-nucleotide antagonist of P2X3 and P2X2/3 receptors, reduces chronic inflammatory and neuropathic pain in the rat. Proc Natl Acad Sci U S A 99: 17179-17184. doi:10.1073/pnas.252537299. PubMed: 12482951.
21. Jarvis MF, Khakh BS (2009) ATP-gated P2X cation-channels. Neuropharmacology 56: 208-215. doi:10.1016/j.neuropharm.2008.06.067. PubMed: 18657557.
22. Syed N-H, Kennedy C (2012) Pharmacology of P2X receptors. Wiley Interdisciplinary Rev Membr Transp Signal 1: 16-30. doi:10.1002/wmts.1.
23. Hausmann R, Rettinger J, Gerevich Z, Meis S, Kassack MU et al. (2006) The Suramin Analog 4,4′,4″,4‴-(Carbonylbis(imino-5,1,3- benzenetriylbis (carbonylimino)))tetra-kis-benzenesulfonic Acid (NF110) Potently Blocks P2X3 Receptors: Subtype Selectivity Is Determined by Location of Sulfonic Acid Groups. Molecular Pharmacology 69: 2058-2067 doi:10.1124/mol.106. 022665.
24. Burgard EC, Niforatos W, Van Biesen T, Lynch KJ, Kage KL et al. (2000) Competitive antagonism of recombinant P2X(2/3) receptors by 2′, 3′-O-(2,4,6-trinitrophenyl) adenosine 5′-triphosphate (TNP-ATP). Mol Pharmacol 58: 1502-1510.
25. Buell G, Lewis C, Collo G, North RA, Surprenant A (1996) An antagonist-insensitive P2X receptor expressed in epithelia and brain. EMBO J 15: 55-62. PubMed: 8598206.
26. Allsopp RC, El Ajouz S, Schmid R, Evans RJ (2011) Cysteine Scanning Mutagenesis (Residues Glu52-Gly96) of the Human P2X1 Receptor for ATP. J Biol Chem 286: 29207-29217. doi:10.1074/jbc.M111.260364.
27. Hattori M, Gouaux E (2012) Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature. Available: http://www.nature.com/ nature/journal/vaop/ncurrent/full/nature11010.html#/supplementary-information. Accessed 30 April 2012.
28. Brown SG, Kim Y-C, Kim S-A, Jacobson KA, Burnstock G et al. (2001) Actions of a series of PPADS analogs at P2X1 and P2X3 receptors. Drug Dev Res 53: 281-291. doi:10.1002/ddr.1197.
29. Egan TM, Khakh BS (2004) Contribution of calcium ions to P2X channel responses. J Neurosci 24: 3413-3420. doi:10.1523/JNEUROSCI.5429-03.2004. PubMed: 15056721.
30. Browne LE (2012) Structure of P2X receptors. Wiley Interdisciplinary Rev Membr Transp Signal 1: 56-69. doi:10.1002/wmts.24.
31. El-Ajouz S, Ray D, Allsopp RC, Evans RJ (2012) Molecular basis of selective antagonism of the P2X1 receptor for ATP by NF449 and suramin: contribution of basic amino acids in the cysteine-rich loop. Br J Pharmacol 165: 390-400. doi:10.1111/j.1476-5381.2011.01534.x. PubMed: 21671897.
32. Wolf C, Rosefort C, Fallah G, Kassack MU, Hamacher A et al. (2011) Molecular Determinants of Potent P2X2 Antagonism Identified by Functional Analysis, Mutagenesis, and Homology Docking. Mol Pharmacol 79: 649-661. doi:10.1124/mol.110.068700. PubMed: 21191044.
33. Michel AD, Ng S-W, Roman S, Clay WC, Dean DK et al. (2009) Mechanism of action of species-selective P2X7 receptor antagonists. Br J Pharmacol 156: 1312-1325. doi:10.1111/j.1476-5381.2009.00135.x. PubMed: 19309360.
34. Michel AD, Clay WC, Ng SW, Roman S, Thompson K et al. (2008) Identification of regions of the P2X7 receptor that contribute to human and rat species differences in antagonist effects. Br J Pharmacol 155: 738-751. doi:10.1038/bjp.2008.306. PubMed: 18660826.
35. Sokolova E, Skorinkin A, Moiseev I, Agrachev A, Nistri A et al. (2006) Experimental and Modeling Studies of Desensitization of P2X3 Receptors. Mol Pharmacol 70: 373-382. doi:10.1124/mol.106.023564. PubMed: 16627751.
36. Karoly R, Mike A, Illes P, Gerevich Z (2008) The Unusual State-Dependent Affinity of P2X3 Receptors Can Be Explained by an Allosteric Two-Open-State Model. Mol Pharmacol 73: 224-234. doi:10.1124/mol.107.038901. PubMed: 17925459.