Structure of P2X receptors

Wiley Interdisciplinary Reviews: Membrane Transport and Signaling

Volumn 1, Issue 1, 2012, Pages 56-69

  Browne, Liam E ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; 2 [(3,4 DIFLUOROPHENYL)AMINO] N [2 METHYL 5 (1 PIPERAZINYLMETHYL)PHENYL]ACETAMIDE; 3 [1 [[[3' NITRO (1,1' BIPHENYL) 4 YL]OXY]METHYL] 3 (4 PYRIDINYL)PROPYL] 2,4 THIAZOLIDINEDIONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ADENOSINE TRIPHOSPHATE; PURINERGIC P2X RECEPTOR; PURINERGIC P2X RECEPTOR ANTAGONIST; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL MUTAGENESIS; HYDROGEN BOND; INTRACELLULAR TRANSPORT; LIGAND BINDING; MEMBRANE TRANSPORT; POROSITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

EID: 84871482119     PISSN: 2190460X     EISSN: 21904618     Source Type: Journal    
DOI: 10.1002/wmts.24     Document Type: Article

References (112)

1. North RA. Molecular physiology of P2X receptors. Physiol Rev 2002, 82:1013-1067.
2. North RA. Families of ion channels with two hydrophobic segments. Curr Opin Cell Biol 1996, 8:474-483.
3. Khakh BS, North RA. P2X receptors as cell-surface ATP sensors in health and disease. Nature 2006, 442:527-532.
4. Surprenant A, North RA. Signaling at purinergic P2X receptors. Annu Rev Physiol 2009, 71:333-359.
5. Lecut C, Frederix K, Johnson DM, Deroanne C, Thiry M, Faccinetto C, Maree R, Evans RJ, Volders PG, Bours V, et al. P2X1 ion channels promote neutrophil chemotaxis through Rho kinase activation. J Immunol 2009, 183:2801-2809.
6. Mulryan K, Gitterman DP, Lewis CJ, Vial C, Leckie BJ, Cobb AL, Brown JE, Conley EC, Buell G, Pritchard CA, et al. Reduced vas deferens contraction and male infertility in mice lacking P2X1 receptors. Nature 2000, 403:86-89.
7. Souslova V, Cesare P, Ding Y, Akopian AN, Stanfa L, Suzuki R, Carpenter K, Dickenson A, Boyce S, Hill R, et al. Warm-coding deficits and aberrant inflammatory pain in mice lacking P2X3 receptors. Nature 2000, 407:1015-1017.
8. Jarvis MF, Burgard EC, McGaraughty S, Honore P, Lynch K, Brennan TJ, Subieta A, Van Biesen T, Cartmell J, Bianchi B, et al. 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 2002, 99:17179-17184.
9. Cockayne DA, Hamilton SG, Zhu QM, Dunn PM, Zhong Y, Novakovic S, Malmberg AB, Cain G, Berson A, Kassotakis L, et al. Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature 2000, 407:1011-1015.
10. Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 2005, 310:1495-1499.
11. Sim JA, Chaumont S, Jo J, Ulmann L, Young MT, Cho K, Buell G, North RA, Rassendren F. Altered hippocampal synaptic potentiation in P2X4 knock-out mice. J Neurosci 2006, 26:9006-9009.
12. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 2003, 424:778-783.
13. Ke HZ, Qi H, Weidema AF, Zhang Q, Panupinthu N, Crawford DT, Grasser WA, Paralkar VM, Li M, Audoly LP, et al. Deletion of the P2X7 nucleotide receptor reveals its regulatory roles in bone formation and resorption. Mol Endocrinol 2003, 17:1356-1367.
14. Solle M, Labasi J, Perregaux DG, Stam E, Petrushova N, Koller BH, Griffiths RJ, Gabel CA. Altered cytokine production in mice lacking P2X(7) receptors. J Biol Chem 2001, 276:125-132.
15. Chessell IP, Hatcher JP, Bountra C, Michel AD, Hughes JP, Green P, Egerton J, Murfin M, Richardson J, Peck WL, et al. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 2005, 114:386-396.
16. Honore P, Donnelly-Roberts D, Namovic MT, Hsieh G, Zhu CZ, Mikusa JP, Hernandez G, Zhong C, Gauvin DM, Chandran P, et al. A-740003 [N-(1-{[(cyanoi mino)(5-quinolinylamino) methyl]amino}-2, 2-dimeth- ylpropyl)-2-(3, 4-dimethoxyphenyl)acetamide], a novel and selective P2X7 receptor antagonist, dose-dependently reduces neuropathic pain in the rat. J Pharmacol Exp Ther 2006, 319:1376-1385.
17. Kawate T, Michel JC, Birdsong WT, Gouaux E. Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 2009, 460:592-598.
18. Browne LE, Jiang LH, North RA. New structure enlivens interest in P2X receptors. Trends Pharmacol Sci 2010, 31:229-237.
19. Nicke A, Baumert HG, Rettinger J, Eichele A, Lambrecht G, Mutschler E, Schmalzing G. P2X1 and P2X3 receptors form stable trimers: a novel structural motif of ligand-gated ion channels. EMBO J 1998, 17:3016-3028.
20. Bean BP. ATP-activated channels in rat and bullfrog sensory neurons: concentration dependence and kinetics. J Neurosci 1990, 10:1-10.
21. Stoop R, Thomas S, Rassendren F, Kawashima E, Buell G, Surprenant A, North RA. Contribution of individual subunits to the multimeric P2X(2) receptor: estimates based on methanethiosulfonate block at T336C. Mol Pharmacol 1999, 56:973-981.
22. Ding S, Sachs F. Single channel properties of P2X2 purinoceptors. J Gen Physiol 1999, 113:695-720.
23. Jiang LH, Kim M, Spelta V, Bo X, Surprenant A, North RA. Subunit arrangement in P2X receptors. J Neurosci 2003, 23:8903-8910.
24. Nagaya N, Tittle RK, Saar N, Dellal SS, Hume RI. An intersubunit zinc binding site in rat P2X2 receptors. J Biol Chem 2005, 280:25982-25993.
25. Wilkinson WJ, Jiang LH, Surprenant A, North RA. Role of ectodomain lysines in the subunits of the heteromeric P2X2/3 receptor. Mol Pharmacol 2006, 70:1159-1163.
26. Barrera NP, Ormond SJ, Henderson RM, Murrell-Lagnado RD, Edwardson JM. Atomic force microscopy imaging demonstrates that P2X2 receptors are trimers but that P2X6 receptor subunits do not oligomerize. J Biol Chem 2005, 280:10759-10765.
27. Shinozaki Y, Sumitomo K, Tsuda M, Koizumi S, Inoue K, Torimitsu K. Direct observation of ATP-induced conformational changes in single P2X4 receptors. PLoS Biol 2009, 7:e103.
28. Mio K, Ogura T, Yamamoto T, Hiroaki Y, Fujiyoshi Y, Kubo Y, Sato C. Reconstruction of the P2X(2) receptor reveals a vase-shaped structure with lateral tunnels above the membrane. Structure 2009, 17:266-275.
29. Young MT, Fisher JA, Fountain SJ, Ford RC, North RA, Khakh BS. Molecular shape, architecture, and size of P2X4 receptors determined using fluorescence resonance energy transfer and electron microscopy. J Biol Chem 2008, 283:26241-26251.
30. Clyne JD, Wang LF, Hume RI. Mutational analysis of the conserved cysteines of the rat P2X2 purinoceptor. J Neurosci 2002, 22:3873-3880.
31. Ennion SJ, Evans RJ. Conserved cysteine residues in the extracellular loop of the human P2X(1) receptor form disulfide bonds and are involved in receptor trafficking to the cell surface. Mol Pharmacol 2002, 61:303-311.
32. Rokic MB, Tvrdonova V, Vavra V, Jindrichova M, Obsil T, Stojilkovic SS, Zemkova H. Roles of conserved ectodomain cysteines of the rat P2X4 purinoreceptor in agonist binding and channel gating. Physiol Res 2010, 59:927-935.
33. Fountain SJ, Parkinson K, Young MT, Cao L, Thompson CR, North RA. An intracellular P2X receptor required for osmoregulation in Dictyostelium discoideum. Nature 2007, 448:200-203.
34. Torres GE, Egan TM, Voigt MM. N-Linked glycosylation is essential for the functional expression of the recombinant P2X2 receptor. Biochemistry 1998, 37:14845-14851.
35. Marquez-Klaka B, Rettinger J, Bhargava Y, Eisele T, Nicke A. Identification of an intersubunit cross-link between substituted cysteine residues located in the putative ATP binding site of the P2X1 receptor. J Neurosci 2007, 27:1456-1466.
36. Marquez-Klaka B, Rettinger J, Nicke A. Inter-subunit disulfide cross-linking in homomeric and heteromeric P2X receptors. Eur Biophys J 2009, 38:329-338.
37. Jiang LH, Rassendren F, Spelta V, Surprenant A, North RA. Amino acid residues involved in gating identified in the first membrane-spanning domain of the rat P2X(2) receptor. J Biol Chem 2001, 276:14902-14908.
38. Higaki JN, Fletterick RJ, Craik CS. Engineered metalloregulation in enzymes. Trends Biochem Sci 1992, 17:100-104.
39. Thornton JM. Disulphide bridges in globular proteins. J Mol Biol 1981, 151:261-287.
40. Tittle RK, Power JM, Hume RI. A histidine scan to probe the flexibility of the rat P2X2 receptor zinc-binding site. J Biol Chem 2007, 282: 19526-19533.
41. Gonzales EB, Kawate T, Gouaux E. Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 2009, 460:599-604.
42. Ennion S, Hagan S, Evans RJ. The role of positively charged amino acids in ATP recognition by human P2X1 receptors. J Biol Chem 2000, 275: 35656.
43. Jiang LH, Rassendren F, Surprenant A, North RA. Identification of amino acid residues contributing to the ATP-binding site of a purinergic P2X receptor. J Biol Chem 2000, 275:34190-34196.
44. Roberts JA, Digby HR, Kara M, El Ajouz S, Sutcliffe MJ, Evans RJ. 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 2008, 283:20126-20136.
45. Roberts JA, Evans RJ. ATP binding at human P2X1 receptors. Contribution of aromatic and basic amino acids revealed using mutagenesis and partial agonists. J Biol Chem 2004, 279:9043-9055.
46. Roberts JA, Evans RJ. Contribution of conserved polar glutamine, asparagine and threonine residues and glycosylation to agonist action at human P2X1 receptors for ATP. J Neurochem 2006, 96: 843-852.
47. Roberts JA, Evans RJ. Cysteine substitution mutants give structural insight and identify ATP binding and activation sites at P2X receptors. J Neurosci 2007, 27:4072-4082.
48. Roberts JA, Valente M, Allsopp RC, Watt D, Evans RJ. Contribution of the region Glu181 to Val200 of the extracellular loop of the human P2X1 receptor to agonist binding and gating revealed using cysteine scanning mutagenesis. J Neurochem 2009, 109:1042-1052.
49. Zemkova H, Yan Z, Liang Z, Jelinkova I, Tomic M, Stojilkovic SS. Role of aromatic and charged ectodomain residues in the P2X(4) receptor functions. J Neurochem 2007, 102:1139-1150.
50. Jiang R, Lemoine D, Martz A, Taly A, Gonin S, Prado de Carvalho L, Specht A, Grutter T. Agonist trapped in ATP-binding sites of the P2X2 receptor. Proc Natl Acad Sci U S A 2011, 108:9066-9071.
51. Dunn PM, Blakeley AG. Suramin: a reversible P2-purinoceptor antagonist in the mouse vas deferens. Br J Pharmacol 1988, 93:243-245.
52. Sim JA, Broomhead HE, North RA. Ectodomain lysines and suramin block of P2X1 receptors. J Biol Chem 2008, 283:29841-29846.
53. Buell G, Lewis C, Collo G, North RA, Surprenant A. An antagonist-insensitive P2X receptor expressed in epithelia and brain. EMBO J 1996, 15:55-62.
54. Michel AD, Clay WC, Ng SW, Roman S, Thompson K, Condreay JP, Hall M, Holbrook J, Livermore D, Senger S. Identification of regions of the P2X(7) receptor that contribute to human and rat species differences in antagonist effects. Br J Pharmacol 2008, 155:738-751.
55. Michel AD, Ng SW, Roman S, Clay WC, Dean DK, Walter DS. Mechanism of action of species-selective P2X(7) receptor antagonists. Br J Pharmacol 2009, 156:1312-1325.
56. Li Z, Migita K, Samways DS, Voigt MM, Egan TM. Gain and loss of channel function by alanine substitutions in the transmembrane segments of the rat ATP-gated P2X2 receptor. J Neurosci 2004, 24:7378-7386.
57. Silberberg SD, Chang TH, Swartz KJ. Secondary structure and gating rearrangements of transmembrane segments in rat P2X4 receptor channels. J Gen Physiol 2005, 125:347-359.
58. Samways DS, Migita K, Li Z, Egan TM. On the role of the first transmembrane domain in cation permeability and flux of the ATP-gated P2X2 receptor. J Biol Chem 2008, 283:5110-5117.
59. Samways DS, Egan TM. Acidic amino acids impart enhanced Ca2+ permeability and flux in two members of the ATP-gated P2X receptor family. J Gen Physiol 2007, 129:245-256.
60. Jindrichova M, Vavra V, Obsil T, Stojilkovic SS, Zemkova H. Functional relevance of aromatic residues in the first transmembrane domain of P2X receptors. J Neurochem 2009, 109:923-934.
61. Li M, Kawate T, Silberberg SD, Swartz KJ. Pore-opening mechanism in trimeric P2X receptor channels. Nat Commun 2010, 1:1-7.
62. Li M, Chang TH, Silberberg SD, Swartz KJ. Gating the pore of P2X receptor channels. Nat Neurosci 2008, 11:883-887.
63. Rassendren F, Buell G, Newbolt A, North RA, Surprenant A. Identification of amino acid residues contributing to the pore of a P2X receptor. EMBO J 1997, 16:3446-3454.
64. Kracun S, Chaptal V, Abramson J, Khakh BS. Gated access to the pore of a P2X receptor: structural implications for closed-open transitions. J Biol Chem 2010, 285:10110-10121.
65. Cao L, Young MT, Broomhead HE, Fountain SJ, North RA. Thr339-to-serine substitution in rat P2X2 receptor second transmembrane domain causes constitutive opening and indicates a gating role for Lys308. J Neurosci 2007, 27:12916-12923.
66. Sargent PB. The diversity of neuronal nicotinic acetylcholine receptors. Annu Rev Neurosci 1993, 16: 403-443.
67. Boulter J, Hollmann M, O'Shea-Greenfield A, Hartley M, Deneris E, Maron C, Heinemann S. Molecular cloning and functional expression of glutamate receptor subunit genes. Science 1990, 249:1033-1037.
68. Zhou Z, Hume RI. Two mechanisms for inward rectification of current flow through the purinoceptor P2X2 class of ATP-gated channels. J Physiol 1998, 507:353-364.
69. Fujiwara Y, Keceli B, Nakajo K, Kubo Y. Voltage- and [ATP]-dependent gating of the P2X(2) ATP receptor channel. J Gen Physiol 2009, 133:93-109.
70. Stanfield PR, Davies NW, Shelton PA, Sutcliffe MJ, Khan IA, Brammar WJ, Conley EC. A single aspartate residue is involved in both intrinsic gating and blockage by Mg2+ of the inward rectifier, IRK1. J Physiol 1994, 478:1-6.
71. Keceli B, Kubo Y. Functional and structural identification of amino acid residues of the P2X2 receptor channel critical for the voltage- and [ATP]-dependent gating. J Physiol 2009, 587(Pt 24):5801-5818.
72. Cao L, Broomhead HE, Young MT, North RA. Polar residues in the second transmembrane domain of the rat P2X2 receptor that affect spontaneous gating, unitary conductance, and rectification. J Neurosci 2009, 29:14257-14264.
73. Bo X, Jiang LH, Wilson HL, Kim M, Burnstock G, Surprenant A, North RA. Pharmacological and biophysical properties of the human P2X5 receptor. Mol Pharmacol 2003, 63:1407-1416.
74. Ruppelt A, Ma W, Borchardt K, Silberberg SD, Soto F. Genomic structure, developmental distribution and functional properties of the chicken P2X(5) receptor. J Neurochem 2001, 77:1256-1265.
75. Ding S, Sachs F. Ion permeation and block of P2X(2) purinoceptors: single channel recordings. J Membr Biol 1999, 172:215-223.
76. Migita K, Haines WR, Voigt MM, Egan TM. Polar residues of the second transmembrane domain influence cation permeability of the ATP-gated P2X(2) receptor. J Biol Chem 2001, 276:30934-30941.
77. Browne LE, Cao L, Broomhead HE, Bragg L, Wilkinson WJ, North RA. P2X receptor channels show threefold symmetry in ionic charge selectivity and unitary conductance. Nat Neurosci 2011, 14:17-18.
78. Qu W, Moorhouse AJ, Chandra M, Pierce KD, Lewis TM, Barry PH. A single P-loop glutamate point mutation to either lysine or arginine switches the cation-anion selectivity of the CNGA2 channel. J Gen Physiol 2006, 127:375-389.
79. Galzi JL, Devillers-Thiery A, Hussy N, Bertrand S, Changeux JP, Bertrand D. Mutations in the channel domain of a neuronal nicotinic receptor convert ion selectivity from cationic to anionic. Nature 1992, 359:500-505.
80. Gunthorpe MJ, Lummis SC. Conversion of the ion selectivity of the 5-HT(3a) receptor from cationic to anionic reveals a conserved feature of the ligand-gated ion channel superfamily. J Biol Chem 2001, 276:10977-10983.
81. Fountain SJ, Cao L, Young MT, North RA. Permeation properties of a P2X receptor in the green algae Ostreococcus tauri. J Biol Chem 2008, 283:15122-15126.
82. Silberberg SD, Li M, Swartz KJ. Ivermectin interaction with transmembrane helices reveals widespread rearrangements during opening of P2X receptor channels. Neuron 2007, 54:263-274.
83. Hilf RJ, Dutzler R. X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 2008, 452:375-379.
84. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J Mol Biol 2005, 346:967-989.
85. Sobolevsky AI, Rosconi MP, Gouaux E. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 2009, 462:745-756.
86. Long SB, Campbell EB, Mackinnon R. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 2005, 309:897-903.
87. Alam A, Jiang Y. High-resolution structure of the open NaK channel. Nat Struct Mol Biol 2009, 16:30-34.
88. Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R. The open pore conformation of potassium channels. Nature 2002, 417:523-526.
89. Akitake B, Anishkin A, Liu N, Sukharev S. Straightening and sequential buckling of the pore-lining helices define the gating cycle of MscS. Nat Struct Mol Biol 2007, 14:1141-1149.
90. Zhao Y, Yarov-Yarovoy V, Scheuer T, Catterall WA. A gating hinge in Na+ channels; a molecular switch for electrical signaling. Neuron 2004, 41:859-865.
91. Egan TM, Haines WR, Voigt MM. A domain contributing to the ion channel of ATP-gated P2X2 receptors identified by the substituted cysteine accessibility method. J Neurosci 1998, 18:2350-2359.
92. Khakh BS, Bao XR, Labarca C, Lester HA. Neuronal P2X transmitter-gated cation channels change their ion selectivity in seconds. Nat Neurosci 1999, 2:322-330.
93. Evans RJ, Lewis C, Virginio C, Lundstrom K, Buell G, Surprenant A, North RA. Ionic permeability of, and divalent cation effects on, two ATP-gated cation channels (P2X receptors) expressed in mammalian cells. J Physiol 1996, 497:413-422.
94. Virginio C, MacKenzie A, North RA, Surprenant A. Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. J Physiol 1999, 519(Pt 2):335-346.
95. Virginio C, MacKenzie A, Rassendren FA, North RA, Surprenant A. Pore dilation of neuronal P2X receptor channels. Nat Neurosci 1999, 2:315-321.
96. Khakh BS, Lester HA. Dynamic selectivity filters in ion channels. Neuron 1999, 23:653-658.
97. Chen J, Kim D, Bianchi BR, Cavanaugh EJ, Faltynek CR, Kym PR, Reilly RM. Pore dilation occurs in TRPA1 but not in TRPM8 channels. Mol Pain 2009, 5:3.
98. Chung MK, Guler AD, Caterina MJ. TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat Neurosci 2008, 11:555-564.
99. Samways DS, Khakh BS, Egan TM. Tunable calcium current through TRPV1 receptor channels. J Biol Chem 2008, 283:31274-31278.
100. Khakh BS, Egan TM. Contribution of transmembrane regions to ATP-gated P2X2 channel permeability dynamics. J Biol Chem 2005, 280: 6118-6129.
101. Surprenant A, Rassendren F, Kawashima E, North RA, Buell G. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 1996, 272:735-738.
102. Jiang LH, Rassendren F, Mackenzie A, Zhang YH, Surprenant A, North RA. N-methyl-D-glucamine and propidium dyes utilize different permeation pathways at rat P2X(7) receptors. Am J Physiol Cell Physiol 2005, 289:C1295-C1302.
103. Yan Z, Li S, Liang Z, Tomic M, Stojilkovic SS. The P2X7 receptor channel pore dilates under physiological ion conditions. J Gen Physiol 2008, 132: 563-573.
104. Fisher JA, Girdler G, Khakh BS. Time-resolved measurement of state-specific P2X2 ion channel cytosolic gating motions. J Neurosci 2004, 24:10475-10487.
105. Chaumont S, Khakh BS. Patch-clamp coordinated spectroscopy shows P2X2 receptor permeability dynamics require cytosolic domain rearrangements but not Panx-1 channels. Proc Natl Acad Sci U S A 2008, 105:12063-12068.
106. Fujiwara Y, Kubo Y. Density-dependent changes of the pore properties of the P2X2 receptor channel. J Physiol 2004, 558(Pt 1):31-43.
107. Yan Z, Khadra A, Li S, Tomic M, Sherman A, Stojilkovic SS. Experimental characterization and mathematical modeling of P2X7 receptor channel gating. J Neurosci 2010, 30:14213-14224.
108. Young MT, Zhang YH, Cao L, Broomhead H, Jiang LH. Role of the domain encompassing Arg304-Ile328 in rat P2X2 receptor conformation revealed by alterations in complex glycosylation at Asn298. Biochem J 2008, 416:137-143.
109. Yan Z, Liang Z, Obsil T, Stojilkovic SS. Participation of the Lys313-Ile333 sequence of the purinergic P2X4 receptor in agonist binding and transduction of signals to the channel gate. J Biol Chem 2006, 281:32649-32659.
110. Jiang R, Martz A, Gonin S, Taly A, de Carvalho LP, Grutter T. A putative extracellular salt bridge at the subunit interface contributes to the ion channel function of the ATP-gated P2X2 receptor. J Biol Chem 2010, 285:15805-15815.
111. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 2004, 25:1605-1612.
112. Smart OS, Neduvelil JG, Wang X, Wallace BA, Sansom MS. HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J Mol Graph 1996, 14:354-360, 376.