The gating isomerization of neuromuscular acetylcholine receptors

Journal of Physiology

Volumn 588, Issue 4, 2010, Pages 573-586

  Auerbach, Anthony ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR; ACETYLCHOLINE; CHOLINE; PROLINE; SERINE;

ADAPTATION; BINDING AFFINITY; BINDING SITE; DESENSITIZATION; ENZYME ACTIVATION; ENZYME INACTIVATION; EQUILIBRIUM CONSTANT; GENE MUTATION; ISOMERIZATION; KINETICS; NERVE CONDUCTION; NEUROMUSCULAR SYNAPSE; NEUROMUSCULAR TRANSMISSION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; REVIEW; AMINO ACID SUBSTITUTION; ARTICLE; ASSOCIATION RATE CONSTANT; CHANNEL GATING; CONFORMATIONAL TRANSITION; ENERGY; ENERGY COUPLING; HUMAN; ION CONDUCTANCE; MOLECULAR MODEL; TRANSPORT KINETICS;

ANIMALS; ION CHANNEL GATING; MEMBRANE POTENTIALS; MICE; NEUROMUSCULAR JUNCTION; PATCH-CLAMP TECHNIQUES; RECEPTORS, CHOLINERGIC;

EID: 77949497067     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.182774     Document Type: Review

References (50)

1. Akk G. Aromatics at the murine nicotinic receptor agonist binding site: mutational analysis of the αY93 and αW149 residues. J Physiol 2001, 535:729-740.
2. Auerbach A. Kinetic behaviour of cloned mouse acetylcholine receptors. A semi-autonomous, stepwise model of gating. Biophys J 1992, 62:72-73.
3. Auerbach A. A statistical analysis of acetylcholine receptor activation in Xenopus myocytes: stepwise versus concerted models of gating. J Physiol 1993, 461:339-378.
4. Auerbach A. Gating of acetylcholine receptor channels: brownian motion across a broad transition state. Proc Natl Acad Sci U S A 2005, 102:1408-1412.
5. Auerbach A. How to turn the reaction coordinate into time. J Gen Physiol 2007, 130:543-546.
6. Auerbach A, Akk G. Desensitization of mouse nicotinic acetylcholine receptor channels. A two-gate mechanism. J Gen Physiol 1998, 112:181-197.
7. Bafna PA, Jha A, Auerbach A. Aromatic residues e{open}Trp-55 and δTrp-57 and the activation of acetylcholine receptor channels. J Biol Chem 2009, 284:8582-8588.
8. Bafna PA, Purohit PG, Auerbach A. Gating at the mouth of the acetylcholine receptor channel: energetic consequences of mutations in the αM2-cap. PLoS One 2008, 3:e2515.
9. Beckstein O, Sansom MS. A hydrophobic gate in an ion channel: the closed state of the nicotinic acetylcholine receptor. Phys Biol 2006, 3:147-159.
10. Bocquet N, Nury H, Baaden M, Le Poupon C, Changeux JP, Delarue M, Corringer PJ. X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 2009, 457:111-114.
11. Brejc K, van Dijk WJ, Klaassen RV, Schuurmans M, Van Der Oost J, Smit AB, Sixma TK. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 2001, 411:269-276.
12. Cadugan DJ, Auerbach A. Conformational dynamics of the αM3 transmembrane helix during acetylcholine receptor channel gating. Biophys J 2007, 93:859-865.
13. Celie PH, van Rossum-Fikkert SE, van Dijk WJ, Brejc K, Smit AB, Sixma TK. Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron 2004, 41:907-914.
14. Chakrapani S, Auerbach A. A speed limit for conformational change of an allosteric membrane protein. Proc Natl Acad Sci U S A 2005, 102:87-92.
15. Chakrapani S, Bailey TD, Auerbach A. Gating dynamics of the acetylcholine receptor extracellular domain. J Gen Physiol 2004a, 123:341-356.
16. Chakrapani S, Bailey TD, Auerbach A. Gating dynamics of the acetylcholine receptor extracellular domain. J Gen Physiol 2004b, 123:341-356.
17. Cymes GD, Grosman C, Auerbach A. Structure of the transition state of gating in the acetylcholine receptor channel pore: a Φ-value analysis. Biochemistry 2002, 41:5548-5555.
18. Dellisanti CD, Yao Y, Stroud JC, Wang ZZ, Chen L. Crystal structure of the extracellular domain of nAChR α1 bound to α-bungarotoxin at 1.94 Å resolution. Nat Neurosci 2007, 10:953-962.
19. Elenes S, Auerbach A. Desensitization of diliganded mouse muscle nicotinic acetylcholine receptor channels. J Physiol 2002, 541:367-383.
20. Frauenfelder H, Parak F, Young RD. Conformational substates in proteins. Annu Rev Biophys Biophys Chem 1988, 17:451-479.
21. Grosman C, Auerbach A. The dissociation of acetylcholine from open nicotinic receptor channels. Proc Natl Acad Sci U S A 2001, 98:14102-14107.
22. Grosman C, Salamone FN, Sine SM, Auerbach A. The extracellular linker of muscle acetylcholine receptor channels is a gating control element. J Gen Physiol 2000a, 116:327-340.
23. Grosman C, Zhou M, Auerbach A. Mapping the conformational wave of acetylcholine receptor channel gating. Nature 2000b, 403:773-776.
24. Hansen SB, Sulzenbacher G, Huxford T, Marchot P, Taylor P, Bourne Y. Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations. EMBO J 2005, 24:3635-3646.
25. Hilf RJ, Dutzler R. X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 2008, 452:375-379.
26. Hilf RJ, Dutzler R. Structure of a potentially open state of a proton-activated pentameric ligand-gated ion channel. Nature 2009, 457:115-118.
27. Jackson MB. Spontaneous openings of the acetylcholine receptor channel. Proc Natl Acad Sci U S A 1984, 81:3901-3904.
28. Jackson MB. Kinetics of unliganded acetylcholine receptor channel gating. Biophys J 1986, 49:663-672.
29. Jha A, Cadugan DJ, Purohit P, Auerbach A. Acetylcholine receptor gating at extracellular transmembrane domain interface: the cys-loop and M2-M3 linker. J Gen Physiol 2007, 130:547-558.
30. Jha A, Purohit P, Auerbach A. Energy and structure of the M2 helix in acetylcholine receptor-channel gating. Biophys J 2009, 96:4075-4084.
31. Katz B, Miledi R. Transmitter leakage from motor nerve endings. Proc R Soc Lond B Biol Sci 1977, 196:59-72.
32. Katz B, Thesleff S. A study of the desensitization produced by acetylcholine at the motor end-plate. J Physiol 1957, 138:63-80.
33. Lape R, Colquhoun D, Sivilotti LG. On the nature of partial agonism in the nicotinic receptor superfamily. Nature 2008, 454:722-727.
34. Lauger P. Internal motions in proteins and gating kinetics of ionic channels. Biophys J 1988, 53:877-884.
35. Lee WY, Free CR, Sine SM. Nicotinic receptor interloop proline anchors β1-β2 and Cys loops in coupling agonist binding to channel gating. J Gen Physiol 2008, 132:265-278.
36. Lee WY, Sine SM. Principal pathway coupling agonist binding to channel gating in nicotinic receptors. Nature 2005, 438:243-247.
37. Lummis SC, Beene DL, Lee LW, Lester HA, Broadhurst RW, Dougherty DA. Cis-trans isomerization at a proline opens the pore of a neurotransmitter-gated ion channel. Nature 2005, 438:248-252.
38. Mitra A, Bailey TD, Auerbach AL. Structural dynamics of the M4 transmembrane segment during acetylcholine receptor gating. Structure 2004, 12:1909-1918.
39. Miyazawa A, Fujiyoshi Y, Unwin N. Structure and gating mechanism of the acetylcholine receptor pore. Nature 2003, 423:949-955.
40. Mukhtasimova N, Lee WY, Wang HL, Sine SM. Detection and trapping of intermediate states priming nicotinic receptor channel opening. Nature 2009, 459:451-454.
41. Paulsen IM, Martin IL, Dunn SM. Isomerization of the proline in the M2-M3 linker is not required for activation of the human 5-HT3A receptor. J Neurochem 2009, 110:870-878.
42. Purohit P, Auerbach A. Acetylcholine receptor gating at extracellular transmembrane domain interface: the 'pre-M1' linker. J Gen Physiol 2007, 130:559-568.
43. Purohit P, Auerbach A. Unliganded gating of acetylcholine receptor channels. Proc Natl Acad Sci U S A 2009, 106:115-120.
44. Revah F, Bertrand D, Galzi JL, Devillers-Thiery A, Mulle C, Hussy N, Bertrand S, Ballivet M, Changeux JP. Mutations in the channel domain alter desensitization of a neuronal nicotinic receptor. Nature 1991, 353:846-849.
45. Taly A, Delarue M, Grutter T, Nilges M, Le Novere N, Corringer PJ, Changeux JP. Normal mode analysis suggests a quaternary twist model for the nicotinic receptor gating mechanism. Biophys J 2005, 88:3954-3965.
46. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution. J Mol Biol 2005, 346:967-989.
47. Zhang Y, Chen J, Auerbach A. Activation of recombinant mouse acetylcholine receptors by acetylcholine, carbamylcholine and tetramethylammonium. J Physiol 1995a, 486:189-206.
48. Zhong W, Gallivan JP, Zhang Y, Li L, Lester HA, Dougherty DA. From ab initio quantum mechanics to molecular neurobiology: a cation-π binding site in the nicotinic receptor. Proc Natl Acad Sci U S A 1998, 95:12088-12093.
49. Zhou M, Engel AG, Auerbach A. Serum choline activates mutant acetylcholine receptors that cause slow channel congenital myasthenic syndromes. Proc Natl Acad Sci U S A 1999, 96:10466-10471.
50. Zhou Y, Pearson JE, Auerbach A. Φ-value analysis of a linear, sequential reaction mechanism: theory and application to ion channel gating. Biophys J 2005, 89:3680-3685.