Salt bridge switching from Arg290/Glu167 to Arg290/ATP promotes the closed-to-open transition of the P2X2 receptor

Molecular Pharmacology

Volumn 83, Issue 1, 2013, Pages 73-84

  Hausmann, Ralf ^a   Günther, Janka ^a   Kless, Achim ^b   Kuhlmann, Daniel ^a   Kassack, Matthias U ^c   Bahrenberg, Gregor ^b   Markwardt, Fritz ^d   Schmalzing, Günther ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b GRÜNENTHAL GMBH   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARGININE; DISULFIDE; GLUTAMIC ACID; PHOSPHATE; PURINERGIC P2X2 RECEPTOR;

ANIMAL CELL; ARTICLE; GENE REARRANGEMENT; GENE SWITCHING; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; XENOPUS LAEVIS; ZEBRA FISH;

ADENOSINE TRIPHOSPHATE; ANIMALS; ARGININE; BINDING SITES; FEMALE; GLUTAMIC ACID; ION CHANNEL GATING; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; OOCYTES; PATCH-CLAMP TECHNIQUES; PURINERGIC P2X RECEPTOR AGONISTS; PURINERGIC P2X RECEPTOR ANTAGONISTS; RATS; RECEPTORS, PURINERGIC P2X2; RECEPTORS, PURINERGIC P2X4; RECOMBINANT PROTEINS; STATIC ELECTRICITY; XENOPUS LAEVIS;

EID: 84871574635     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.081489     Document Type: Article

References (50)

1. Allsopp RC, El Ajouz S, Schmid R, and Evans RJ (2011) Cysteine scanning mutagenesis (residues Glu52-Gly96) of the human P2X1 receptor for ATP: mapping agonist binding and channel gating. J Biol Chem 286:29207-29217.
2. 1+2 receptor subtypes. J Mol Biol 342:333-343.
3. Cao L, Broomhead HE, Young MT, and North RA (2009) Polar residues in the second transmembrane domain of the rat P2X2 receptor that affect spontaneous gating, unitary conductance, and rectification. J Neurosci 29:14257-14264.
4. Careaga CL and Falke JJ (1992a) Structure and dynamics of Escherichia coli chemosensory receptors. Engineered sulfhydryl studies. Biophys J 62:209-216, discussion 217-219.
5. Careaga CL and Falke JJ (1992b) Thermal motions of surface alpha-helices in the D-galactose chemosensory receptor. Detection by disulfide trapping. J Mol Biol 226:1219-1235.
6. Carter PJ, Winter G, Wilkinson AJ, and Fersht AR (1984) The use of double mutants to detect structural changes in the active site of the tyrosyl-tRNA synthetase (Bacillus stearothermophilus). Cell 38:835-840.
7. Du J, Dong H, and Zhou HX (2012) Gating mechanism of a P2X4 receptor developed from normal mode analysis and molecular dynamics simulations. Proc Natl Acad Sci USA 109:4140-4145.
8. Ennion S, Hagan S, and Evans RJ (2000) The role of positively charged amino acids in ATP recognition by human P2X(1) receptors. J Biol Chem 275:29361-29367. (Pubitemid 32043808)
9. Faiman GA and Horovitz A (1996) On the choice of reference mutant states in the application of the double-mutant cycle method. Protein Eng 9:315-316. (Pubitemid 26148312)
10. Fallah G, Römer T, Detro-Dassen S, Braam U, Markwardt F, and Schmalzing G (2011) TMEM16A(a)/anoctamin-1 shares a homodimeric architecture with CLC chloride channels. Mol Cell Proteomics 10:M110.004697.
11. Fischer W, Zadori Z, Kullnick Y, Gröger-Arndt H, Franke H, Wirkner K, Illes P, and Mager PP (2007) Conserved lysin and arginin residues in the extracellular loop of P2X(3) receptors are involved in agonist binding. Eur J Pharmacol 576:7-17. (Pubitemid 47588249)
12. Franklin C, Braam U, Eisele T, Schmalzing G, and Hausmann R (2007) Lack of evidence for direct phosphorylation of recombinantly expressed P2X(2) and P2X (3) receptors by protein kinase C. Purinergic Signal 3:377-388.
13. Guerlet G, Taly A, Prado de Carvalho L, Martz A, Jiang R, Specht A, Le Novère N, and Grutter T (2008) Comparative models of P2X2 receptor support inter-subunit ATP-binding sites. Biochem Biophys Res Commun 375:405-409.
14. Hattori M and Gouaux E (2012) Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature 485:207-212.
15. Hausmann R, Bodnar M, Woltersdorf R, Wang H, Fuchs M, Messemer N, Qin Y, Günther J, Riedel T, and Grohmann M et al. (2012) ATP binding site mutagenesis reveals different subunit stoichiometry of functional P2X2/3 and P2X2/6 receptors. J Biol Chem 287:13930-13943.
16. Hausmann R, Rettinger J, Gerevich Z, Meis S, Kassack MU, Illes P, Lambrecht G, and Schmalzing G (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. Mol Pharmacol 69:2058-2067. (Pubitemid 43894325)
17. Hessa T, Kim H, Bihlmaier K, Lundin C, Boekel J, Andersson H, Nilsson I, White SH, and von Heijne G (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377-381. (Pubitemid 40203311)
18. + channel pore through mutant cycles with a peptide inhibitor. Science 268:307-310.
19. Hong H, Szabo G, and Tamm LK (2006) Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for pore opening. Nat Chem Biol 2:627-635. (Pubitemid 44610347)
20. Horovitz A (1996) Double-mutant cycles: a powerful tool for analyzing protein structure and function. Fold Des 1:R121-R126.
21. Horovitz A, Serrano L, Avron B, Bycroft M, and Fersht AR (1990) Strength and cooperativity of contributions of surface salt bridges to protein stability. J Mol Biol 216:1031-1044.
22. Jiang R, Martz A, Gonin S, Taly A, de Carvalho LP, and Grutter T (2010) A putative extracellular salt bridge at the subunit interface contributes to the ion channel function of the ATP-gated P2X2 receptor. J Biol Chem 285:15805-15815.
23. Jiang R, Taly A, Lemoine D, Martz A, Cunrath O, and Grutter T (2012) Tightening of the ATP-binding sites induces the opening of P2X receptor channels. EMBO J 31:2134-2143.
24. Kaczmarek-Hájek K, Lörinczi E, Hausmann R, and Nicke A (2012) Molecular and functional properties of P2X receptors - recent progress and persisting challenges. Purinergic Signal 8:375-417.
25. Kash TL, Jenkins A, Kelley JC, Trudell JR, and Harrison NL (2003) Coupling of agonist binding to channel gating in the GABA(A) receptor. Nature 421:272-275. (Pubitemid 36139131)
26. Kawate T, Michel JC, Birdsong WT, and Gouaux E (2009) Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 460:592-598.
27. Kawate T, Robertson JL, Li M, Silberberg SD, and Swartz KJ (2011) Ion access pathway to the transmembrane pore in P2X receptor channels. J Gen Physiol 137:579-590.
28. Kracun S, Chaptal V, Abramson J, and Khakh BS (2010) Gated access to the pore of a P2X receptor: structural implications for closed-open transitions. J Biol Chem 285:10110-10121.
29. Kumar S and Nussinov R (1999) Salt bridge stability in monomeric proteins. J Mol Biol 293:1241-1255.
30. Laha KT and Wagner DA (2011) A state-dependent salt-bridge interaction exists across the β/α intersubunit interface of the GABAA receptor. Mol Pharmacol 79:662-671.
31. Li M, Chang TH, Silberberg SD, and Swartz KJ (2008) Gating the pore of P2X receptor channels. Nat Neurosci 11:883-887.
32. Li M, Kawate T, Silberberg SD, and Swartz KJ (2010) Pore-opening mechanism in trimeric P2X receptor channels. Nat Commun 1:44.
33. Liu X, Alexander C, Serrano J, Borg E, and Dawson DC (2006) Variable reactivity of an engineered cysteine at position 338 in cystic fibrosis transmembrane conductance regulator reflects different chemical states of the thiol. J Biol Chem 281:8275-8285. (Pubitemid 43847448)
34. Meis S, Hamacher A, and Hongwiset D et al. (2010) NF546 [4,49-(carbonylbis(imino-3,1-phenylene-carbonylimino-3,1-(4-methyl-phenylene) -carbonylimino))-bis(1,3-xylene-alpha,alpha′-diphosphonic acid) tetrasodium salt] is a non-nucleotide P2Y11 agonist and stimulates release of interleukin-8 from human monocyte-derived dendritic cells. J Pharmacol Exp Ther 332:238-247.
35. Moroni A and Thiel G (2006) Flip-flopping salt bridges gate an ion channel. Nat Chem Biol 2:572-573. (Pubitemid 44610339)
36. Nagano N, Ota M, and Nishikawa K (1999) Strong hydrophobic nature of cysteine residues in proteins. FEBS Lett 458:69-71. (Pubitemid 29415674)
37. 3 receptors form stable trimers: a novel structural motif of ligand-gated ion channels. EMBO J 17:3016-3028.
38. Nicke A, Rettinger J, Büttner C, Eichele A, Lambrecht G, and Schmalzing G (1999) Evolving view of quaternary structures of ligand-gated ion channels. Prog Brain Res 120:61-80. (Pubitemid 29457012)
39. North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013-1067.
40. 1 receptor at nanomolar ATP concentrations. J Gen Physiol 121:451-461.
41. Roberts JA, Allsopp RC, El Ajouz S, Vial C, Schmid R, Young MT, and Evans RJ (2012) Agonist binding evokes extensive conformational changes in the extracellular domain of the ATP-gated human P2X1 receptor ion channel. Proc Natl Acad Sci USA 109:4663-4667.
42. Roberts JA, Digby HR, Kara M, El Ajouz S, Sutcliffe MJ, and Evans RJ (2008) Cysteine substitution mutagenesis and the effects of methanethiosulfonate reagents at P2X2 and P2X4 receptors support a core common mode of ATP action at P2X receptors. J Biol Chem 283:20126-20136.
43. Roberts JA and Evans RJ (2004) ATP binding at human P2X1 receptors. Contribution of aromatic and basic amino acids revealed using mutagenesis and partial agonists. J Biol Chem 279:9043-9055. (Pubitemid 38295968)
44. Samways DS, Khakh BS, Dutertre S, and Egan TM (2011) Preferential use of unobstructed lateral portals as the access route to the pore of human ATP-gated ion channels (P2X receptors). Proc Natl Acad Sci USA 108:13800-13805.
45. Schmalzing G, Gloor S, Omay H, Kröner S, Appelhans H, and Schwarz W (1991) Up-regulation of sodium pump activity in Xenopus laevis oocytes by expression of heterologous β 1 subunits of the sodium pump. Biochem J 279:329-336.
46. Schreiber G and Fersht AR (1995) Energetics of protein-protein interactions: analysis of the barnase-barstar interface by single mutations and double mutant cycles. J Mol Biol 248:478-486.
47. Serrano L, Horovitz A, Avron B, Bycroft M, and Fersht AR (1990) Estimating the contribution of engineered surface electrostatic interactions to protein stability by using double-mutant cycles. Biochemistry 29:9343-9352. (Pubitemid 20329069)
48. Sowdhamini R, Srinivasan N, Shoichet B, Santi DV, Ramakrishnan C, and Balaram P (1989) Stereochemical modeling of disulfide bridges. Criteria for introduction into proteins by site-directed mutagenesis. Protein Eng 3:95-103. (Pubitemid 20055084)
49. Venkatachalan SP and Czajkowski C (2008) A conserved salt bridge critical for GABA(A) receptor function and loop C dynamics. Proc Natl Acad Sci USA 105:13604-13609.
50. Wolf C, Rosefort C, Fallah G, Kassack MU, Hamacher A, Bodnar M, Wang H, Illes P, Kless A, and Bahrenberg G et al. (2011) Molecular determinants of potent P2X2 antagonism identified by functional analysis, mutagenesis, and homology docking. Mol Pharmacol 79:649-661.