An integrated catch-and-hold mechanism activates nicotinic acetylcholine receptors

Journal of General Physiology

Volumn 140, Issue 1, 2012, Pages 17-28

  Jadey, Snehal ^a   Auerbach, Anthony ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CARBACHOL; NICOTINIC AGENT; NICOTINIC RECEPTOR;

ANIMAL; APLYSIA; ARTICLE; CELL STRAIN HEK293; CHANNEL GATING; CHEMISTRY; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; MOUSE; PROTEIN DOMAIN; SITE DIRECTED MUTAGENESIS; SPECIES DIFFERENCE; STRUCTURE ACTIVITY RELATION;

ACETYLCHOLINE; ANIMALS; APLYSIA; CARBACHOL; HEK293 CELLS; HUMANS; ION CHANNEL GATING; MICE; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; NICOTINIC AGONISTS; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, NICOTINIC; SPECIES SPECIFICITY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84864009008     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201210801     Document Type: Article

References (49)

1. Armstrong, N., Y. Sun, G.Q. Chen, and E. Gouaux. 1998. Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature. 395:913-917. http://dx.doi.org/10.1038/27692
2. Auerbach, A. 2005. Gating of acetylcholine receptor channels: brownian motion across a broad transition state. Proc. Natl. Acad. Sci. USA. 102:1408-1412. http://dx.doi.org/10.1073/pnas.0406787102
3. Auerbach, A. 2010. The gating isomerization of neuromuscular acetylcholine receptors. J. Physiol. 588:573-586. http://dx.doi.org/ 10.1113/jphysiol.2009.182774
4. Auerbach, A. 2012. Thinking in cycles: MWC is a good model for acetylcholine receptor-channels. J. Physiol. 590:93-98.
5. Bafna, P.A., P.G. Purohit, and A. Auerbach. 2008. Gating at the mouth of the acetylcholine receptor channel: energetic consequences of mutations in the alphaM2-cap. PLoS ONE. 3:e2515. http://dx.doi.org/10.1371/journal.pone.0002515
6. Bafna, P.A., A. Jha, and A. Auerbach. 2009. Aromatic residues epsilonTrp-55 and deltaTrp-57 and the activation of acetylcholine receptor channels. J. Biol. Chem. 284:8582-8588. http://dx.doi .org/10.1074/jbc.M807152200
7. Berg, O.G., and P.H. von Hippel. 1985. Diffusion-controlled macromolecular interactions. Annu. Rev. Biophys. Biophys. Chem. 14:131-160. http://dx.doi.org/10.1146/annurev.bb.14.060185.001023
8. Bocquet, N., H. Nury, M. Baaden, C. Le Poupon, J.P. Changeux, M. Delarue, and P.J. Corringer. 2009. X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature. 457:111-114. http://dx.doi.org/10.1038/ nature07462
9. Brams, M., E.A. Gay, J.C. Sáez, A. Guskov, R. van Elk, R.C. van der Schors, S. Peigneur, J. Tytgat, S.V. Strelkov, A.B. Smit, et al. 2011a. Crystal structures of a cysteine-modified mutant in loop D of acetylcholine-binding protein. J. Biol. Chem. 286:4420-4428. http://dx.doi.org/10.1074/jbc.M110.188730
10. Brams, M., A. Pandya, D. Kuzmin, R. van Elk, L. Krijnen, J.L. Yakel, V. Tsetlin, A.B. Smit, and C. Ulens. 2011b. A structural and mutagenic blueprint for molecular recognition of strychnine and d-tubocurarine by different cys-loop receptors. PLoS Biol. 9:e1001034. http://dx.doi.org/10.1371/journal.pbio.1001034
11. Burnham, K.P., and D.R. Anderson. 2002. Model Selection and Inference: A Practical Information-Theoretic Approach. Second edition. Springer, New York. 488 pp.
12. Cadugan, D.J., and A. Auerbach. 2010. Linking the acetylcholine receptor-channel agonist-binding sites with the gate. Biophys. J. 99:798-807. http://dx.doi.org/10.1016/j.bpj.2010.05.008
13. Celie, P.H., I.E. Kasheverov, D.Y. Mordvintsev, R.C. Hogg, P. van Nierop, R. van Elk, S.E. van Rossum-Fikkert, M.N. Zhmak, D. Bertrand, V. Tsetlin, et al. 2005. Crystal structure of nicotinic acetylcholine receptor homolog AChBP in complex with an alphaconotoxin PnIA variant. Nat. Struct. Mol. Biol. 12:582-588.
14. Chang, Y., D.F. Covey, and D.S. Weiss. 2000. Correlation of the apparent affinities and efficacies of gamma-aminobutyric acid(C) receptor agonists. Mol. Pharmacol. 58:1375-1380.
15. Changeux, J.P., A. Devillers-Thiéry, and P. Chemouilli. 1984. Acetylcholine receptor: an allosteric protein. Science. 225:1335-1345. http://dx.doi.org/10.1126/science.6382611
16. Del Castillo, J., and B. Katz. 1957. The identity of intrinsic and extrinsic acetylcholine receptors in the motor end-plate. Proc. R. Soc. Lond. B Biol. Sci. 146:357-361. http://dx.doi.org/10.1098/rspb.1957.0016
17. Fenwick, M.K., and R.E. Oswald. 2010. On the mechanisms of alphaamino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptor binding to glutamate and kainate. J. Biol. Chem. 285:12334-12343. http://dx.doi.org/10.1074/jbc.M109.086371
18. Fersht, A.R., R.J. Leatherbarrow, and T.N. Wells. 1987. Structureactivity relationships in engineered proteins: analysis of use of binding energy by linear free energy relationships. Biochemistry. 26:6030-6038. http://dx.doi.org/10.1021/bi00393a013
19. Grosman, C., and A. Auerbach. 2000. Kinetic, mechanistic, and structural aspects of unliganded gating of acetylcholine receptor channels: a single-channel study of second transmembrane segment 12' mutants. J. Gen. Physiol. 115:621-635. http://dx.doi .org/10.1085/jgp.115.5.621
20. Grosman, C., and A. Auerbach. 2001. The dissociation of acetylcholine from open nicotinic receptor channels. Proc. Natl. Acad. Sci. USA. 98:14102-14107. http://dx.doi.org/10.1073/pnas.251402498
21. Grosman, C., M. Zhou, and A. Auerbach. 2000. Mapping the conformational wave of acetylcholine receptor channel gating. Nature. 403:773-776. http://dx.doi.org/10.1038/35001586
22. Gupta, S., and A. Auerbach. 2011. Temperature dependence of acetylcholine receptor channels activated by different agonists. Biophys. J. 100:895-903. http://dx.doi.org/10.1016/j.bpj.2010.12.3727
23. Hansen, S.B., G. Sulzenbacher, T. Huxford, P. Marchot, P. Taylor, and Y. Bourne. 2005. Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations. EMBO J. 24:3635-3646. http:// dx.doi.org/10.1038/sj.emboj.7600828
24. Hibbs, R.E., G. Sulzenbacher, J. Shi, T.T. Talley, S. Conrod, W.R. Kem, P. Taylor, P. Marchot, and Y. Bourne. 2009. Structural determinants for interaction of partial agonists with acetylcho line binding protein and neuronal alpha7 nicotinic acetylcholine receptor. EMBO J. 28:3040-3051. http://dx.doi.org/10.1038/emboj.2009.227
25. Hilf, R.J., and R. Dutzler. 2008. X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature. 452:375-379. http://dx.doi.org/10.1038/nature06717
26. Jackson, M.B. 1986. Kinetics of unliganded acetylcholine receptor channel gating. Biophys. J. 49:663-672. http://dx.doi.org/10.1016/ S0006-3495(86)83693-1
27. Jackson, M.B., K. Imoto, M. Mishina, T. Konno, S. Numa, and B. Sakmann. 1990. Spontaneous and agonist-induced openings of an acetylcholine receptor channel composed of bovine muscle alpha-, beta-and delta-subunits. Pflugers Arch. 417:129-135. http:// dx.doi.org/10.1007/BF00370689
28. Jadey, S.V., P. Purohit, I. Bruhova, T.M. Gregg, and A. Auerbach. 2011. Design and control of acetylcholine receptor conformational change. Proc. Natl. Acad. Sci. USA. 108:4328-4333. http:// dx.doi.org/10.1073/pnas.1016617108
29. Jha, A., and A. Auerbach. 2010. Acetylcholine receptor channels activated by a single agonist molecule. Biophys. J. 98:1840-1846. http://dx.doi.org/10.1016/j.bpj.2010.01.025
30. Jha, A., P. Purohit, and A. Auerbach. 2009. Energy and structure of the M2 helix in acetylcholine receptor-channel gating. Biophys. J. 96:4075-4084. http://dx.doi.org/10.1016/j.bpj.2009.02.030
31. Jin, R., T.G. Banke, M.L. Mayer, S.F. Traynelis, and E. Gouaux. 2003. Structural basis for partial agonist action at ionotropic glutamate receptors. Nat. Neurosci. 6:803-810. http://dx.doi.org/10.1038/ nn1091
32. Jones, M.V., P. Jonas, Y. Sahara, and G.L. Westbrook. 2001. Microscopic kinetics and energetics distinguish GABA(A) receptor agonists from antagonists. Biophys. J. 81:2660-2670. http:// dx.doi.org/10.1016/S0006-3495(01)75909-7
33. Karlin, A. 1967. On the application of "a plausible model" of allosteric proteins to the receptor for acetylcholine. J. Theor. Biol. 16:306-320. http://dx.doi.org/10.1016/0022-5193(67)90011-2
34. Lape, R., D. Colquhoun, and L.G. Sivilotti. 2008. On the nature of partial agonism in the nicotinic receptor superfamily. Nature. 454:722-727.
35. MacKay, D. 2003. Information Theory, Inference and Learning Algorithms. Fourth edition. Cambridge University Press, Cambridge. 631 pp.
36. Mukhtasimova, N., W.Y. Lee, H.L. Wang, and S.M. Sine. 2009. Detection and trapping of intermediate states priming nicotinic receptor channel opening. Nature. 459:451-454. http://dx.doi .org/10.1038/nature07923
37. Nayak, T.K., P.G. Purohit, and A. Auerbach. 2012. The intrinsic energy of the gating isomerization of a neuromuscular acetylcholine receptor channel. J. Gen. Physiol. 139:349-358. http://dx.doi .org/10.1085/jgp.201110752
38. Purohit, P., and A. Auerbach. 2009. Unliganded gating of acetylcholine receptor channels. Proc. Natl. Acad. Sci. USA. 106:115-120. http://dx.doi.org/10.1073/pnas.0809272106
39. Purohit, Y., and C. Grosman. 2006. Estimating binding affinities of the nicotinic receptor for low-efficacy ligands using mixtures of agonists and two-dimensional concentration-response relationships. J. Gen. Physiol. 127:719-735. http://dx.doi.org/10.1085/ jgp.200509438
40. Qin, F. 2004. Restoration of single-channel currents using the segmental k-means method based on hidden Markov modeling. Biophys. J. 86:1488-1501. http://dx.doi.org/10.1016/S0006-3495(04) 74217-4
41. Qin, F., A. Auerbach, and F. Sachs. 1997. Maximum likelihood estimation of aggregated Markov processes. Proc. Biol. Sci. 264:375-383. http://dx.doi.org/10.1098/rspb.1997.0054
42. Robert, A., N. Armstrong, J.E. Gouaux, and J.R. Howe. 2005. AMPA receptor binding cleft mutations that alter affinity, efficacy, and recovery from desensitization. J. Neurosci. 25:3752-3762. http:// dx.doi.org/10.1523/JNEUROSCI.0188-05.2005
43. Rucktooa, P., A.B. Smit, and T.K. Sixma. 2009. Insight in nAChR subtype selectivity from AChBP crystal structures. Biochem. Pharmacol. 78:777-787. http://dx.doi.org/10.1016/j.bcp.2009.06.098
44. Talley, T.T., M. Harel, R.E. Hibbs, Z. Radic, M. Tomizawa, J.E. Casida, and P. Taylor. 2008. Atomic interactions of neonicotinoid agonists with AChBP: molecular recognition of the distinctive electronegative pharmacophore. Proc. Natl. Acad. Sci. USA. 105:7606-7611. http://dx.doi.org/10.1073/pnas.0802197105
45. Trautmann, A. 1982. Curare can open and block ionic channels associated with cholinergic receptors. Nature. 298:272-275. http://dx.doi.org/10.1038/298272a0
46. Ulens, C., A. Akdemir, A. Jongejan, R. van Elk, S. Bertrand, A. Perrakis, R. Leurs, A.B. Smit, T.K. Sixma, D. Bertrand, and I.J. de Esch. 2009. Use of acetylcholine binding protein in the search for novel alpha7 nicotinic receptor ligands. In silico docking, pharmacological screening, and X-ray analysis. J. Med. Chem. 52:2372-2383. http://dx.doi.org/10.1021/jm801400g
47. Unwin, N. 2005. Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 346:967-989. http://dx.doi .org/10.1016/j.jmb.2004.12.031
48. Zhang, Y., J. Chen, and A. Auerbach. 1995. Activation of recombinant mouse acetylcholine receptors by acetylcholine, carbamylcholine and tetramethylammonium. J. Physiol. 486:189-206.
49. Zhou, Y., J.E. Pearson, and A. Auerbach. 2005. Phi-value analysis of a linear, sequential reaction mechanism: theory and application to ion channel gating. Biophys. J. 89:3680-3685. http://dx.doi .org/10.1529/biophysj.105.067215