Allosteric nature of P2X receptor activation probed by photoaffinity labelling

British Journal of Pharmacology

Volumn 167, Issue 6, 2012, Pages 1301-1310

  Bhargava, Y ^a,b   Rettinger, J ^a,c   Mourot, A ^a,d  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c SORBONNE UNIVERSITÉ   (France)

^d MULTI CHANNEL SYSTEMS MCS GMBH   (Germany)

Author keywords

allosteric activation; binding; gating; ion channel; P2X receptors; photolabelling

Indexed keywords

2',3' O (4 BENZOYLBENZOYL)ADENOSINE TRIPHOSPHATE; ALPHA,BETA METHYLENEADENOSINE TRIPHOSPHATE; CHIMERIC PROTEIN; PURINERGIC P2X RECEPTOR; PURINERGIC P2X RECEPTOR AGONIST; PURINERGIC P2X2 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; COVALENT BOND; DRUG BINDING SITE; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; DRUG RECEPTOR BINDING; ELECTROPHYSIOLOGY; FEMALE; LIGAND BINDING; NONHUMAN; PHOTOAFFINITY LABELING; PHOTOCHEMISTRY; PRIORITY JOURNAL; RECEPTOR UPREGULATION; ULTRAVIOLET RADIATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; ION CHANNEL GATING; OOCYTES; PHOTOAFFINITY LABELS; PROTEIN BINDING; PURINERGIC P2X RECEPTOR AGONISTS; RECEPTORS, PURINERGIC P2X2; ULTRAVIOLET RAYS; XENOPUS LAEVIS;

EID: 84867763158     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.02083.x     Document Type: Article

References (33)

1. Agboh KC, Powell AJ, Evans RJ, (2009). Characterisation of ATP analogues to cross-link and label P2X receptors. Neuropharmacology 56: 230-236.
2. Aschrafi A, Sadtler S, Niculescu C, Rettinger J, Schmalzing G, (2004). Trimeric architecture of homomeric P2X2 and heteromeric P2X1+2 receptor subtypes. J Mol Biol 342: 333-343.
3. Barrera NP, Ormond SJ, Henderson RM, Murrell-Lagnado RD, Edwardson JM, (2005). Atomic force microscopy imaging demonstrates that P2X2 receptors are trimers but that P2X6 receptor subunits do not oligomerize. J Biol Chem 280: 10759-10765.
4. Biskup C, Kusch J, Schulz E, Nache V, Schwede F, Lehmann F, et al,. (2007). Relating ligand binding to activation gating in CNGA2 channels. Nature 446: 440-443.
5. Bongartz EV, Rettinger J, Hausmann R, (2010). Aminoglycoside block of P2X2 receptors heterologously expressed in Xenopus laevis oocytes. Purinergic Signal 6: 393-403.
6. Brown RL, Gerber WV, Karpen JW, (1993). Specific labeling and permanent activation of the retinal rod cGMP-activated channel by the photoaffinity analog 8-p-azidophenacylthio-cGMP. Proc Natl Acad Sci U S A 90: 5369-5373.
7. Ding S, Sachs F, (1999). Single channel properties of P2X2 purinoceptors. J Gen Physiol 113: 695-720.
8. Erb L, Lustig KD, Ahmed AH, Gonzalez FA, Weisman GA, (1990). Covalent incorporation of 3'-O-(4-benzoyl)benzoyl-ATP into a P2 purinoceptor in transformed mouse fibroblasts. J Biol Chem 265: 7424-7431.
9. Evans RJ, (2009). Orthosteric and allosteric binding sites of P2X receptors. Eur Biophys J 38: 319-327.
10. Forman SA, Zhou QL, Stewart DS, (2007). Photoactivated 3-azioctanol irreversibly desensitizes muscle nicotinic ACh receptors via interactions at alphaE262. Biochemistry 46: 11911-11918.
11. Jiang R, Lemoine D, Martz A, Taly A, Gonin S, Prado de Carvalho L, et al,. (2011). Agonist trapped in ATP-binding sites of the P2X2 receptor. Proc Natl Acad Sci U S A 108: 9066-9071.
12. Kapfer I, Jacques P, Toubal H, Goeldner MP, (1995). Comparative photoaffinity labeling study between azidophenyl, difluoroazidophenyl, and tetrafluoroazidophenyl derivatives for the GABA-gated chloride channels. Bioconjug Chem 6: 109-114.
13. Karpen JW, Brown RL, (1996). Covalent activation of retinal rod cGMP-gated channels reveals a functional heterogeneity in the ligand binding sites. J Gen Physiol 107: 169-181.
14. Karpen JW, Ruiz M, (2002). Ion channels: does each subunit do something on its own? Trends Biochem Sci 27: 402-409.
15. Kawate T, Michel JC, Birdsong WT, Gouaux E, (2009). Crystal structure of the ATP-gated P2X4 ion channel in the closed state. Nature 460: 592-598.
16. Khakh BS, North RA, (2006). P2X receptors as cell-surface ATP sensors in health and disease. Nature 442: 527-532.
17. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). NC3Rs Reporting Guidelines Working Group. Br J Pharmacol 160: 1577-1579.
18. Le Novere N, Changeux JP, (1999). The Ligand Gated Ion Channel Database. Nucleic Acids Res 27: 340-342.
19. Li M, Chang TH, Silberberg SD, Swartz KJ, (2008). Gating the pore of P2X receptor channels. Nat Neurosci 11: 883-887.
20. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
21. Marquez-Klaka B, Rettinger J, Bhargava Y, Eisele T, Nicke A, (2007). Identification of an intersubunit cross-link between substituted cysteine residues located in the putative ATP binding site of the P2X1 receptor. J Neurosci 27: 1456-1466.
22. Mourot A, Kotzyba-Hibert F, Goeldner M, Bamberg E, (2006). Photo-induced covalent attachment of agonists as a tool to study allosteric mechanisms of nicotinic acetylcholine receptors. J Mol Neurosci 30: 3-4.
23. Mourot A, Bamberg E, Rettinger J, (2008). Agonist- and competitive antagonist-induced movement of loop 5 on the alpha subunit of the neuronal alpha4beta4 nicotinic acetylcholine receptor. J Neurochem 105: 413-424.
24. Nicke A, Baumert HG, Rettinger J, Eichele A, Lambrecht G, Mutschler E, et al,. (1998). P2X1 and P2X3 receptors form stable trimers: a novel structural motif of ligand-gated ion channels. EMBO J 17: 3016-3028.
25. North RA, (2002). Molecular physiology of P2X receptors. Physiol Rev 82: 1013-1067.
26. North RA, Surprenant A, (2000). Pharmacology of cloned P2X receptors. Annu Rev Pharmacol Toxicol 40: 563-580.
27. Rettinger J, Schmalzing G, (2003). Activation and desensitization of the recombinant P2X1 receptor at nanomolar ATP concentrations. J Gen Physiol 121: 451-461.
28. Rettinger J, Schmalzing G, (2004). Desensitization masks nanomolar potency of ATP for the P2X1 receptor. J Biol Chem 279: 6426-6433.
29. Ruiz ML, Karpen JW, (1997). Single cyclic nucleotide-gated channels locked in different ligand-bound states. Nature 389: 389-392.
30. Valera S, Hussy N, Evans RJ, Adami N, North RA, Surprenant A, et al,. (1994). A new class of ligand-gated ion channel defined by P2x receptor for extracellular ATP. Nature 371: 516-519.
31. 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.
32. Werner P, Seward EP, Buell GN, North RA, (1996). Domains of P2X receptors involved in desensitization. Proc Natl Acad Sci U S A 93: 15485-15490.
33. Zhong H, Rusch D, Forman SA, (2008). Photo-activated azi-etomidate, a general anesthetic photolabel, irreversibly enhances gating and desensitization of gamma-aminobutyric acid type A receptors. Anesthesiology 108: 103-112.