Size matters in activation/inhibition of ligand-gated ion channels

Trends in Pharmacological Sciences

Volumn 33, Issue 9, 2012, Pages 482-493

  Du, Juan ^a   Dong, Hao ^a   Zhou, Huan Xiang ^a  

^a Florida State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CHLORIDE CHANNEL; CYSTEINE LOOP LIGAND GATED ION CHANNEL RECEPTOR; GLUTAMATE GATED CHLORIDE CHANNEL; GLUTAMATE RECEPTOR; GLYCINE RECEPTOR; KAINIC ACID RECEPTOR; LIGAND GATED ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID; NICOTINIC RECEPTOR; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; SEROTONIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; DRUG DESIGN; DRUG TARGETING; LIGAND SIZE; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION;

EID: 84865253138     PISSN: 01656147     EISSN: 18733735     Source Type: Journal    
DOI: 10.1016/j.tips.2012.06.005     Document Type: Review

References (106)

1. N. Unwin Refined structure of the nicotinic acetylcholine receptor at 4 resolution J. Mol. Biol. 346 2005 967 989 (Pubitemid 40215523)
2. A.I. Sobolevsky X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor Nature 462 2009 745 756
3. T. Kawate Crystal structure of the ATP-gated P2X4 ion channel in the closed state Nature 460 2009 592 598
4. J. Du Gating mechanism of a P2X4 receptor developed from normal mode analysis and molecular dynamics simulations Proc. Natl. Acad. Sci. U.S.A. 109 2012 4140 4145
5. K. Brejc Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors Nature 411 2001 269 276 (Pubitemid 32467026)
6. N. Armstrong Structure of a glutamate-receptor ligand-binding core in complex with kainate Nature 395 1998 913 917 (Pubitemid 28503434)
7. N. Armstrong, and E. Gouaux Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: crystal structures of the GluR2 ligand binding core Neuron 28 2000 165 181
8. S.B. Hansen Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations EMBO J. 24 2005 3635 3646 (Pubitemid 41509370)
9. M. Brams A structural and mutagenic blueprint for molecular recognition of strychnine and d-tubocurarine by different Cys-loop receptors PLoS Biol. 9 2011 e1001034
10. M. Yi Spontaneous conformational change and toxin binding in α7 acetylcholine receptor: insight into channel activation and inhibition Proc. Natl. Acad. Sci. U.S.A. 105 2008 8280 8285 (Pubitemid 351904747)
11. A. Akdemir Acetylcholine binding protein (AChBP) as template for hierarchical in silico screening procedures to identify structurally novel ligands for the nicotinic receptors Bioorg. Med. Chem. 19 2011 6107 6119
12. A receptors Br. J. Pharmacol. 136 2002 965 974
13. D. Bertrand Unconventional pharmacology of a neuronal nicotinic receptor mutated in the channel domain Proc. Natl. Acad. Sci. U.S.A. 89 1992 1261 1265
14. S. Bertrand Paradoxical allosteric effects of competitive inhibitors on neuronal α7 nicotinic receptor mutants Neuroreport 8 1997 3591 3596 (Pubitemid 27497489)
15. P.H.N. Celie Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures Neuron 41 2004 907 914 (Pubitemid 38429734)
16. R.J. Hilf, and R. Dutzler X-ray structure of a prokaryotic pentameric ligand-gated ion channel Nature 452 2008 375 379 (Pubitemid 351430790)
17. R.J.C. Hilf, and R. Dutzler Structure of a potentially open state of a proton-activated pentameric ligand-gated ion channel Nature 457 2009 115 118
18. N. Bocquet X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation Nature 457 2009 111 114
19. I. Zimmermann, and R. Dutzler Ligand activation of the prokaryotic pentameric ligand-gated ion channel ELIC PLoS Biol. 9 2011 e1001101
20. W. Zheng, and A. Auerbach Decrypting the sequence of structural events during the gating transition of pentameric ligand-gated ion channels based on an interpolated elastic network model PLoS Comput. Biol. 7 2011 e1001046
21. A. Taly Normal mode analysis suggests a quaternary twist model for the nicotinic receptor gating mechanism Biophys. J. 88 2005 3954 3965 (Pubitemid 40991108)
22. R.J. Law A gating mechanism proposed from a simulation of a human α7 nicotinic acetylcholine receptor Proc. Natl. Acad. Sci. U.S.A. 102 2005 6813 6818 (Pubitemid 40675398)
23. X. Cheng Targeted molecular dynamics study of C-loop closure and channel gating in nicotinic receptors PLoS Comput. Biol. 2 2006 1173 1184 (Pubitemid 44495729)
24. X. Cheng Nanosecond-timescale conformational dynamics of the human α7 nicotinic acetylcholine receptor Biophys. J. 93 2007 2622 2634 (Pubitemid 47607800)
25. F. Zhu, and G. Hummer Gating transition of pentameric ligand-gated ion channels Biophys. J. 97 2009 2456 2463
26. H. Nury One-microsecond molecular dynamics simulation of channel gating in a nicotinic receptor homologue Proc. Natl. Acad. Sci. U.S.A. 107 2010 6275 6280
27. G.D. Cymes Probing ion-channel pores one proton at a time Nature 438 2005 975 980 (Pubitemid 43093964)
28. Y. Paas Pore conformations and gating mechanism of a Cys-loop receptor Proc. Natl. Acad. Sci. U.S.A. 102 2005 15877 15882 (Pubitemid 41552836)
29. R.E. Hibbs, and E. Gouaux Principles of activation and permeation in an anion-selective Cys-loop receptor Nature 474 2011 54 60
30. M. Bartos Structural basis of activation of Cys-loop receptors: the extracellular-transmembrane interface as a coupling region Mol. Neurobiol. 40 2009 236 252
31. P.S. Miller, and T.G. Smart Binding, activation and modulation of Cys-loop receptors Trends Pharmacol. Sci. 31 2010 161 174
32. Y. Sun Mechanism of glutamate receptor desensitization Nature 417 2002 245 253 (Pubitemid 34534700)
33. H. Dong, and H.-X. Zhou Atomistic mechanism for the activation and desensitization of an AMPA-subtype glutamate receptor Nat. Commun. 2 2011 354
34. R. Jin Structural basis for partial agonist action at ionotropic glutamate receptors Nat. Neurosci. 6 2003 803 810 (Pubitemid 36929700)
35. Y. Stern-Bach A point mutation in the glutamate binding site blocks desensitization of AMPA receptors Neuron 21 1998 907 918 (Pubitemid 28498797)
36. N. Armstrong Measurement of conformational changes accompanying desensitization in an ionotropic glutamate receptor Cell 127 2006 85 97 (Pubitemid 44466635)
37. J. Gonzalez Role of dimer interface in activation and desensitization in AMPA receptors Proc. Natl. Acad. Sci. U.S.A. 107 2010 9891 9896
38. L.E. Browne New structure enlivens interest in P2X receptors Trends Pharmacol. Sci. 31 2010 229 237
39. M.T. Young P2X receptors: dawn of the post-structure era Trends Biochem. Sci. 35 2010 83 90
40. S. Ennion The role of positively charged amino acids in ATP recognition by human P2X1 receptors J. Biol. Chem. 275 2000 29361 29367 (Pubitemid 32043808)
41. L.-H. Jiang Identification of amino acid residues contributing to the ATP-binding site of a purinergic P2X receptor J. Biol. Chem. 275 2000 34190 34196
42. W.J. Wilkinson Role of ectodomain lysines in the subunits of the heteromeric P2X2/3 receptor Mol. Pharmacol. 70 2006 1159 1163 (Pubitemid 44435966)
43. H. Zemkova Role of aromatic and charged ectodomain residues in the P2X4 receptor functions J. Neurochem. 102 2007 1139 1150 (Pubitemid 47174228)
44. W. Fischer Conserved lysin and arginin residues in the extracellular loop of P2X3 receptors are involved in agonist binding Eur. J. Pharmacol. 576 2007 7 17 (Pubitemid 47588249)
45. J.A. Roberts 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 2008 20126 20136
46. M. Li Pore-opening mechanism in trimeric P2X receptor channels Nat. Commun. 1 2010 44
47. S. Kracun Gated access to the pore of a P2X receptor J. Biol. Chem. 285 2010 10110 10121
48. T. Kawate Ion access pathway to the transmembrane pore in P2X receptor channels J. Gen. Physiol. 137 2011 579 590
49. D.S.K. Samways 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. U.S.A. 108 2011 13800 13805
50. R. Jiang Agonist trapped in ATP-binding sites of the P2X2 receptor Proc. Natl. Acad. Sci. U.S.A. 108 2011 9066 9071
51. M. Tomizawa Atypical nicotinic agonist bound conformations conferring subtype selectivity Proc. Natl. Acad. Sci. U.S.A. 105 2008 1728 1732 (Pubitemid 351346582)
52. M. Hattori, and E. Gouaux Molecular mechanism of ATP binding and ion channel activation in P2X receptors Nature 485 2012 207 212
53. R.J. Evans Structural interpretation of P2X receptor mutagenesis studies on drug action Br. J. Pharmacol. 161 2010 961 971
54. C. Coddou Activation and regulation of purinergic P2X receptor channels Pharmacol. Rev. 63 2011 641 683
55. N-i-H. Syed, and C. Kennedy Pharmacology of P2X receptors WIREs Membr. Transp. Signal. 1 2012 16 30
56. J.A. Sim Ectodomain lysines and suramin block of P2X1 receptors J. Biol. Chem. 283 2008 29841 29846
57. C. Ulens Use of acetylcholine binding protein in the search for novel α7 nicotinic receptor ligands. In silico docking, pharmacological screening, and X-ray analysis J. Med. Chem. 52 2009 2372 2383
58. E. Edink Fragment growing induces conformational changes in acetylcholine-binding protein: a structural and thermodynamic analysis J. Am. Chem. Soc. 133 2011 5363 5371
59. C. Grosman Mapping the conformational wave of acetylcholine receptor channel gating Nature 403 2000 773 776 (Pubitemid 30111838)
60. A receptor Nature 421 2003 272 275 (Pubitemid 36139131)
61. A. Miyazawa Structure and gating mechanism of the acetylcholine receptor pore Nature 423 2003 949 955 (Pubitemid 36806903)
62. C. Bouzat Coupling of agonist binding to channel gating in an ACh-binding protein linked to an ion channel Nature 430 2004 896 900 (Pubitemid 39119217)
63. S. Chakrapani Gating dynamics of the acetylcholine receptor extracellular domain J. Gen. Physiol. 123 2004 341 356 (Pubitemid 38469279)
64. W.Y. Lee, and S.M. Sine Principal pathway coupling agonist binding to channel gating in nicotinic receptors Nature 438 2005 243 247 (Pubitemid 41599878)
65. T. Grutter Molecular tuning of fast gating in pentameric ligand-gated ion channels Proc. Natl. Acad. Sci. U.S.A. 102 2005 18207 18212 (Pubitemid 41798526)
66. 3 receptors J. Neurosci. 25 2005 9358 9366 (Pubitemid 41464748)
67. X. Xiu A unified view of the role of electrostatic interactions in modulating the gating of Cys loop receptors J. Biol. Chem. 280 2005 41655 41666 (Pubitemid 41832228)
68. A. Jha Acetylcholine receptor gating at extracellular transmembrane domain interface: the Cys-loop and M2-M3 linker J. Gen. Physiol. 130 2007 547 558 (Pubitemid 350179573)
69. W.Y. Lee Nicotinic receptor interloop proline anchors β1-β2 and Cys loops in coupling agonist binding to channel gating J. Gen. Physiol. 132 2008 265 278
70. W.Y. Lee Binding to gating transduction in nicotinic receptors: Cys-loop energetically couples to pre-M1 and M2-M3 regions J. Neurosci. 29 2009 3189 3199
71. J.T. McLaughlin Agonist-driven conformational changes in the inner β-sheet of α7 nicotinic receptors Mol. Pharmacol. 71 2007 1312 1318 (Pubitemid 46658684)
72. + channels J. Neurosci. 23 2003 7559 7568 (Pubitemid 37034072)
73. A.I. Sobolevsky The outer pore of the glutamate receptor channel has 2-fold rotational symmetry Neuron 41 2004 367 378 (Pubitemid 38221041)
74. M.V. Yelshansky Block of AMPA receptor desensitization by a point mutation outside the ligand-binding domain J. Neurosci. 24 2004 4728 4736 (Pubitemid 38668197)
75. M. Li Gating the pore of P2X receptor channels Nat. Neurosci. 11 2008 883 887
76. R. Jiang 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 2010 15805 15815
77. S.D. Silberberg Ivermectin interaction with transmembrane helices reveals widespread rearrangements during opening of P2X receptor channels Neuron 54 2007 263 274 (Pubitemid 46561201)
78. 4 receptor transmembrane residues contributing to channel gating and interaction with ivermectin Pflugers Arch. 456 2008 939 950
79. A. Priel, and S.D. Silberberg Mechanism of ivermectin facilitation of human P2X4 receptor channels J. Gen. Physiol. 123 2004 281 293 (Pubitemid 38282976)
80. M. Brams Crystal structures of a cysteine-modified mutant in loop D of acetylcholine-binding protein J. Biol. Chem. 286 2011 4420 4428
81. R.E. Hibbs Structural determinants for interaction of partial agonists with acetylcholine binding protein and neuronal α7 nicotinic acetylcholine receptor EMBO J. 28 2009 3040 3051
82. P.H.N. Celie Crystal structure of acetylcholine-binding protein from Bulinus truncatus reveals the conserved structural scaffold and sites of variation in nicotinic acetylcholine receptors J. Biol. Chem. 280 2005 26457 26466 (Pubitemid 41022242)
83. M. Ihara Crystal structures of Lymnaea stagnalis AChBP in complex with neonicotinoid insecticides imidacloprid and clothianidin Invert. Neurosci. 8 2008 71 81
84. T.T. Talley Atomic interactions of neonicotinoid agonists with AChBP: molecular recognition of the distinctive electronegative pharmacophore Proc. Natl. Acad. Sci. U.S.A. 105 2008 7606 7611 (Pubitemid 351830065)
85. Y. Bourne Structural determinants in phycotoxins and AChBP conferring high affinity binding and nicotinic AChR antagonism Proc. Natl. Acad. Sci. U.S.A. 107 2010 6076 6081
86. A. Nemecz, and P.W. Taylor Creating an α7 nicotinic acetylcholine recognition domain from the acetylcholine binding protein: crystallographic and ligand selectivity analyses J. Biol. Chem. 286 2011 42555 42565
87. P.H.N. Celie Crystal structure of nicotinic acetylcholine receptor homolog AChBP in complex with an α-conotoxin PnIA variant Nat. Struct. Mol. Biol. 12 2005 582 588 (Pubitemid 40980807)
88. Y. Bourne Crystal structure of a Cbtx-AChBP complex reveals essential interactions between snake α-neurotoxins and nicotinic receptors EMBO J. 24 2005 1512 1522 (Pubitemid 40646442)
89. 7-nicotinic receptor chimera and its complex with agonist Nat. Neurosci. 14 2011 1253 1259
90. M.C. Weston Interdomain interactions in AMPA and kainate receptors regulate affinity for glutamate J. Neurosci. 26 2006 7650 7658 (Pubitemid 44315184)
91. C. Kasper GluR2 ligand-binding core complexes: importance of the isoxazolol moiety and 5-substituent for the binding mode of AMPA-type agonists FEBS Lett. 531 2002 173 178 (Pubitemid 35345144)
92. K. Frydenvang Biostructural and pharmacological studies of bicyclic analogues of the 3-isoxazolol glutamate receptor agonist ibotenic acid J. Med. Chem. 53 2010 8354 8361
93. N. Armstrong Tuning activation of the AMPA-sensitive GluR2 ion channel by genetic adjustment of agonist-induced conformational changes Proc. Natl. Acad. Sci. U.S.A. 100 2003 5736 5741 (Pubitemid 36576877)
94. R. Jin Mechanism of activation and selectivity in a ligand-gated ion channel: structural and functional studies of GluR2 and quisqualate Biochemistry 41 2002 15635 15643 (Pubitemid 36062468)
95. M. Beich-Frandsen Structures of the ligand-binding core of iGluR2 in complex with the agonists (R)- and (S)-2-amino-3-(4-hydroxy-1,2,5-thiadiazol-3- yl)propionic acid explain their unusual equipotency J. Med. Chem. 51 2008 1459 1463 (Pubitemid 351484800)
96. A. Hogner Structural basis for AMPA receptor activation and ligand selectivity: crystal structures of five agonist complexes with the GluR2 ligand-binding core J. Mol. Biol. 322 2002 93 109 (Pubitemid 36138726)
97. M.-L. Lunn Three-dimensional structure of the ligand-binding core of GluR2 in complex with the agonist (S)-ATPA: implications for receptor subunit selectivity J. Med. Chem. 46 2003 872 875 (Pubitemid 36261990)
98. K. Poon Mechanisms of modal activation of GluA3 receptors Mol. Pharmacol. 80 2011 49 59
99. B.B. Nielsen Exploring the GluR2 ligand-binding core in complex with the bicyclical AMPA analogue (S)-4-AHCP FEBS J. 272 2005 1639 1648 (Pubitemid 40516214)
100. A. Frandsen Tyr702 is an important determinant of agonist binding and domain closure of the ligand-binding core of GluR2 Mol. Pharmacol. 67 2005 703 713 (Pubitemid 40372239)
101. M.M. Holm Structural determinants of agonist-specific kinetics at the ionotropic glutamate receptor 2 Proc. Natl. Acad. Sci. U.S.A. 102 2005 12053 12058 (Pubitemid 41291127)
102. R. Jin, and E. Gouaux Probing the function, conformational plasticity, and dimer-dimer contacts of the GluR2 ligand-binding core: studies of 5-substituted willardiines and GluR2 S1S2 in the crystal Biochemistry 42 2003 5201 5213 (Pubitemid 36560416)
103. A. Hogner Competitive antagonism of AMPA receptors by ligands of different classes: crystal structure of ATPO bound to the GluR2 ligand-binding core, in comparison with DNQX J. Med. Chem. 46 2002 214 221 (Pubitemid 36082867)
104. S.B. Vogensen A tetrazolyl-substituted subtype-selective AMPA receptor agonist J. Med. Chem. 50 2007 2408 2414 (Pubitemid 46799252)
105. M. Koller Quinazolinedione sulfonamides: a novel class of competitive AMPA receptor antagonists with oral activity Bioorg. Med. Chem. Lett. 21 2011 3358 3361
106. C. Kasper The structure of a mixed GluR2 ligand-binding core dimer in complex with (S)-glutamate and the antagonist (S)-NS1209 J. Mol. Biol. 357 2006 1184 1201 (Pubitemid 43357980)