New structure enlivens interest in P2X receptors

Trends in Pharmacological Sciences

Volumn 31, Issue 5, 2010, Pages 229-237

  Browne, Liam E ^a   Jiang, Lin Hua ^b   North, R Alan ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF LEEDS   (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; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ADENOSINE TRIPHOSPHATE; GW 791343; NF 449; PURINERGIC P2X RECEPTOR; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; SURAMIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; DICTYOSTELIUM; DRUG POTENCY; DRUG RECEPTOR BINDING; DRUG SELECTIVITY; DRUG SENSITIVITY; GENE MUTATION; HUMAN; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SITE DIRECTED MUTAGENESIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; HUMANS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PERMEABILITY; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, PURINERGIC P2;

EID: 77952551628     PISSN: 01656147     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tips.2010.02.004     Document Type: Review

References (96)

1. Burnstock G., Kennedy C. Is there a basis for distinguishing two types of P2-purinoceptor?. Gen. Pharmacol. 1985, 16:433-440.
2. Burnstock G., Holman M.E. The transmission of excitation from autonomic nerve to smooth muscle. J. Physiol. 1961, 155:115-133.
3. Fatt P., Katz B. The electric activity of the motor end-plate. Proc. R. Soc. Lond. B. 1952, 140:183-186. PMID: 13003923.
4. Krnjević K. Glutamate and gamma-aminobutyric acid in brain. Nature 1970, 228:119-124.
5. Surprenant A., et al. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 1996, 272:735-738.
6. North R.A. Molecular physiology of P2X receptors. Physiol. Rev. 2002, 82:1013-1067.
7. Khakh B.S., North R.A. P2X receptors as cell-surface ATP sensors in health and disease. Nature 2006, 442:527-532.
8. Surprenant A., North R.A. Signaling at purinergic P2X receptors. Annu. Rev. Physiol. 2009, 71:333-359.
9. Gever J.R., et al. Pharmacology of P2X channels. Pflugers Arch. 2006, 452:513-537.
10. Kawate T., et al. Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 2009, 460:592-598.
11. Sali A., Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234:779-815.
12. Davis I.W., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-383.
13. Pettersen E.F., et al. UCSF Chimera--a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
14. North R.A. Families of ion channels with two hydrophobic segments. Curr. Opin. Cell Biol. 1996, 8:474-483.
15. Bean B.P. ATP-activated channels in rat and bullfrog sensory neurons: concentration dependence and kinetics. J. Neurosci. 1990, 10:1-10.
16. Nicke A., et al. P2X1 and P2X3 receptors form stable trimers: a novel structural motif of ligand-gated ion channels. EMBO J. 1998, 17:3016-3028.
17. Jiang L.H., et al. Subunit arrangement in P2X receptors. J. Neurosci. 2003, 23:8903-8910.
18. Stoop R., et al. Contribution of individual subunits to the multimeric P2X2 receptor: estimates based on methanethiosulfonate block at T336C. Mol. Pharmacol. 1999, 56:973-981.
19. Barrera N.P., et al. 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.
20. Young M.T., et al. Molecular shape, architecture, and size of P2X4 receptors determined using fluorescence resonance energy transfer and electron microscopy. J. Biol. Chem. 2008, 283:26241-26251.
21. Clyne J.D., et al. Mutational analysis of the conserved cysteines of the rat P2X2 purinoceptor. J. Neurosci. 2002, 22:3873-3880.
22. Ennion S.J., Evans R.J. Conserved cysteine residues in the extracellular loop of the human P2X1 receptor form disulfide bonds and are involved in receptor trafficking to the cell surface. Mol. Pharmacol. 2002, 61:303-311.
23. Fountain S.J., et al. An intracellular P2X receptor required for osmoregulation in Dictyostelium discoideum. Nature 2007, 448:200-203.
24. Nagaya N., et al. An intersubunit zinc binding site in rat P2X2 receptors. J. Biol. Chem. 2005, 280:25982-25993.
25. Tittle R.K., et al. A histidine scan to probe the flexibility of the rat P2X2 receptor zinc-binding site. J. Biol. Chem. 2007, 282:19526-19533.
26. Marquez-Klaka B., et al. Inter-subunit disulfide cross-linking in homomeric and heteromeric P2X receptors. Eur. Biophys. J. 2009, 38:329-338.
27. Marquez-Klaka B., et al. 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.
28. Jiang L.H., et al. Amino acid residues involved in gating identified in the first membrane-spanning domain of the rat P2X2 receptor. J. Biol. Chem. 2001, 276:14902-14908.
29. Wilkinson W.J., et al. Role of ectodomain lysines in the subunits of the heteromeric P2X2/3 receptor. Mol. Pharmacol. 2006, 70:1159-1163.
30. Jiang L.H., et al. Identification of amino acid residues contributing to the ATP-binding site of a purinergic P2X receptor. J. Biol. Chem. 2000, 275:34190-34196.
31. Sim J.A., et al. Ectodomain lysines and suramin block of P2X1 receptors. J. Biol. Chem. 2008, 283:29841-29846.
32. Buell G., et al. An antagonist-insensitive P2X receptor expressed in epithelia and brain. EMBO J. 1996, 15:55-62.
33. Michel A.D., et al. Mechanism of action of species-selective P2X7 receptor antagonists. Br. J. Pharmacol. 2009, 156:1312-1325.
34. Samways D.S.K., et al. 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.
35. 2+ permeability and flux in two members of the ATP-gated P2X receptor family. J. Gen. Physiol. 2007, 129:245-256.
36. Haines W.R., et al. On the contribution of the first transmembrane domain to whole-cell current through an ATP-gated ionotropic P2X receptor. J. Neurosci. 2001, 21:5885-5892.
37. Li M., et al. Gating the pore of P2X receptor channels. Nat. Neurosci. 2008, 11:883-887.
38. Migita K., et al. Polar residues of the second transmembrane domain influence cation permeability of the ATP-gated P2X2 receptor. J. Biol. Chem. 2001, 276:30934-30941.
39. Egan T.M., Khakh B.S. Contribution of calcium ions to P2X channel responses. J. Neurosci. 2004, 24:3413-3420.
40. Rassendren F., et al. Identification of amino acid residues contributing to the pore of a P2X receptor. EMBO J. 1997, 16:3446-3454.
41. Egan T.M., et al. 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.
42. Kracun, S. et al. (2010) Gated access to the pore of a P2X receptor: structural implications for the closed-open transitions. J. Biol. Chem. [Epub ahead of print], PMID: 20093367.
43. Cao L., et al. 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.
44. Silberberg S., et al. Ivermectin interaction with transmembrane helices reveals widespread rearrangements during opening of P2X receptor channels. Neuron 2007, 54:263-274.
45. Fujiwara Y., et al. Voltage- and [ATP]-dependent gating of the P2X2 ATP receptor channel. J. Gen. Physiol. 2009, 133:93-109.
46. Khakh B.S., et al. Neuronal P2X transmitter-gated cation channels change their ion selectivity in seconds. Nat. Neurosci. 1999, 2:322-330.
47. Virginio C., et al. Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. J. Physiol. 1999, 519:335-346.
48. Virginio C., et al. Pore dilation of neuronal P2X receptor channels. Nat. Neurosci. 1999, 2:315-321.
49. Jiang L.H., et al. N-methyl-D-glucamine and propidium dyes utilize different permeation pathways at rat P2X7 receptors. Am. J. Physiol. Cell Physiol. 2005, 289:C1295-1302.
50. Khakh B.S., Egan T.M. Contribution of transmembrane regions to ATP-gated P2X2 channel permeability dynamics. J. Biol. Chem. 2005, 280:6118-6129.
51. Doyle D.A. Structural changes during ion channel gating. Trends Neurosci. 2004, 27:298-302.
52. Gandhi C.S., Rees D.C. Biochemistry. Opening the molecular floodgates. Science 2008, 321:1166-1167.
53. Hong K., Driscoll M. A transmembrane domain of the putative channel subunit MEC-4 influences mechanotransduction and neurodegeneration in C. elegans. Nature 1994, 367:470-473.
54. Huang M., Chalfie M. Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans. Nature 1994, 367:467-470.
55. Canessa C.M., et al. Epithelial sodium channel related to proteins involved in neurodegeneration. Nature 1993, 361:467-470.
56. Brake A.J., et al. New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptor. Nature 1994, 371:519-523.
57. Valera S., et al. A new class of ligand-gated ion channel defined by P2x receptor for extracellular ATP. Nature 1994, 371:516-519.
58. Burnstock G. Purinergic nerves. Pharmacol. Rev. 1972, 24:509-581.
59. Jasti J., et al. Structure of acid-sensing ion channel 1 at 1.9Å resolution and low pH. Nature 2007, 449:316-323.
60. Gonzales E.B., et al. Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 2009, 460:599-604.
61. Kellenberger S., Schild L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol. Rev. 2002, 82:735-767.
62. Donnelly-Roberts D., et al. Painful purinergic receptors. J. Pharmacol. Exp. Ther. 2008, 324:409-415.
63. Romagnoli R., et al. The P2X7 receptor as a therapeutic target. Expert Opin. Ther. Targets 2008, 12:647-661.
64. Mulryan K., et al. Reduced vas deferens contraction and male infertility in mice lacking P2X1 receptors. Nature 2000, 403:86-89.
65. Inscho E.W., et al. Physiological role for P2X1 receptors in renal microvascular autoregulatory behavior. J. Clin. Invest. 2003, 112:1895-1905.
66. Hechler B., et al. A role of the fast ATP-gated P2X1 cation channel in thrombosis of small arteries in vivo. J. Exp. Med. 2003, 198:661-667.
67. Lecut C., et al. P2X1 ion channels promote neutrophil chemotaxis through Rho kinase activation. J. Immunol. 2009, 183:2801-2809.
68. Cockayne D.A., et al. Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature 2000, 407:1011-1015.
69. Souslova V., et al. Warm-coding deficits and aberrant inflammatory pain in mice lacking P2X3 receptors. Nature 2000, 407:1015-1017.
70. Jarvis M.F., 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.
71. Bian X., et al. Peristalsis is impaired in the small intestine of mice lacking the P2X3 subunit. J. Physiol. 2003, 551:309-322.
72. Ren J., et al. P2X2 subunits contribute to fast synaptic excitation in myenteric neurons of the mouse small intestine. J. Physiol. 2003, 552:809-821.
73. Prasad M., et al. Expression of P2X2 and P2X3 receptor subunits in rat carotid body afferent neurones: role in chemosensory signalling. J. Physiol. 2001, 537:667-677.
74. Rong W., et al. Pivotal role of nucleotide P2X2 receptor subunit of the ATP-gated ion channel mediating ventilatory responses to hypoxia. J. Neurosci. 2003, 23:11315-11321.
75. Finger T.E., et al. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 2005, 310:1495-1499.
76. Tsuda M., et al. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 2003, 424:778-783.
77. Sim J.A., et al. Altered hippocampal synaptic potentiation in P2X4 knock-out mice. J. Neurosci. 2006, 26:9006-9009.
78. Yamamoto K., et al. Impaired flow-dependent control of vascular tone and remodeling in P2X4-deficient mice. Nat. Med. 2006, 12:133-137.
79. Solle M., et al. Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem. 2001, 276:125-132.
80. Ke K.Z., et al. Deletion of the P2X7 nucleotide receptor reveals its regulatory roles in bone formation and resorption. Mol. Endocrinol. 2003, 17:1356-1367.
81. Chessell I.P., et al. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 2005, 114:386-396.
82. Honore P., et al. A-740003 [N-(1-{[(cyanoimino)(5-quinolinylamino) methyl]amino}-2,2-dimethylpropyl)-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.
83. Goncalves R.G., et al. The role of purinergic P2X7 receptors in the inflammation and fibrosis of unilateral ureteral obstruction in mice. Kidney Int. 2006, 70:1599-1606.
84. Zhang X., et al. Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:9864-9869.
85. Chen Y., et al. Activation of P2X7 receptors in glial satellite cells reduces pain through downregulation of P2X3 receptors in nociceptive neurons. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16773-16778.
86. Ennion S., et al. The role of positively charged amino acids in ATP recognition by human P2X1 receptors. J. Biol. Chem. 2000, 275:29361-29367.
87. Roberts J.A., et al. 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.
88. Fischer W., et al. Conserved lysin and arginin residues in the extracellular loop of P2X3 receptors are involved in agonist binding. Eur. J. Pharmacol. 2007, 576:7-17.
89. Zemkova H., et al. Role of aromatic and charged ectodomain residues in the P2X4 receptor functions. J. Neurochem. 2007, 102:1139-1150.
90. Roberts J.A., Evans R.J. 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.
91. 200 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.
92. Roberts J.A., Evans R.J. 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.
93. Roberts J.A., Evans R.J. Cysteine substitution mutants give structural insight and identify ATP binding and activation sites at P2X receptors. J. Neurosci. 2007, 27:4072-4082.
94. 308. J. Neurosci. 2007, 27:12916-12923.
95. 298. Biochem. J. 2008, 416:137-143.
96. 333 sequence of the purinergic P2X4 receptor in agonist binding and transduction of signals to the channel gate. J. Biol. Chem. 2006, 281:32649-32659.