Pore-opening mechanism of the nicotinic acetylcholine receptor evinced by proton transfer

Nature Structural and Molecular Biology

Volumn 15, Issue 4, 2008, Pages 389-396

  Cymes, Gisela D ^a   Grosman, Claudio ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTRANSMITTER; NICOTINIC RECEPTOR;

ALPHA HELIX; ARTICLE; CONFORMATIONAL TRANSITION; EMBRYO; HUMAN; HUMAN CELL; MUSCLE; NANOPORE; PRIORITY JOURNAL; PROTON TRANSPORT; SYNAPSE;

AMINO ACID SEQUENCE; CELL LINE; HUMANS; ION CHANNEL GATING; ION TRANSPORT; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTONS; RECEPTORS, NICOTINIC; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 41649119572     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1407     Document Type: Article

References (52)

1. Unwin, N. Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution. J. Mol. Biol. 346, 967-989 (2005).
2. Dilger, J.P. & Liu, Y. Desensitization of acetylcholine receptors in BC3H-1 cells. Pflugers Arch. 420, 479-485 (1992).
3. Unwin, N. Acetylcholine receptor channel imaged in the open state. Nature 373, 37-43 (1995).
4. Arévalo, E., Chiara, D.C., Forman, S.A., Cohen, J.B. & Miller, K.W. Gating-enhanced accessibility of hydrophobic sites within the transmembrane region of the nicotinic acetylcholine receptor's δ-subunit. A time-resolved photolabeling study. J. Biol. Chem. 280, 13631-13640 (2005).
5. Sansom, M.S.P. Twist to open. Curr. Biol. 5, 373-375 (1995).
6. Miyazawa, A., Fujiyoshi, Y. & Unwin, N. Structure and gating mechanism of the acetylcholine receptor pore. Nature 423, 949-955 (2003).
7. Law, R.J., Henchman, R.H. & McCammon, J.A. A gating mechanism proposed from a simulation of a human α7 nicotinic acetylcholine receptor. Proc. Natl. Acad. Sci. USA 102, 6813-6818 (2005).
8. Paas, Y. et al. Pore conformations and gating mechanism of a Cys-loop receptor. Proc. Natl. Acad. Sci. USA 102, 15877-15882 (2005).
9. Cheng, X., Ivanov, I., Wang, H., Sine, S.M. & McCammon, J.A. Nanosecond time scale conformational dynamics of the human α7 nicotinic acetylcholine receptor. Biophys. J. 93, 2622-2634 (2007).
10. Cheng, X., Wang, H., Grant, B., Sine, S.M. & McCammon, J.A. Targeted molecular dynamics study of C-loop closure and channel gating in nicotinic receptors. PLOS Comput. Biol. 2, e134 (2006).
11. Cymes, G.D., Ni, Y. & Grosman, C. Probing ion-channel pores one proton at a time. Nature 438, 975-980 (2005).
12. a, proton transfer reactions, and general catalysis reactions in enzymes. Biochemistry 20, 3167-3177 (1981).
13. Dao-Pin, S., Anderson, D.E., Baase, W.A., Dahlquist, F.W. & Matthews, B.W. Structural and thermodynamic consequences of burying a charged residue within the hydrophobic core of T4 lysozyme. Biochemistry 30, 11521-11529 (1991).
14. Schutz, C.N. & Warshel, A. What are the dielectric "constants" of proteins and how to validate electrostatic models? Proteins 44, 400-417 (2001).
15. a values of buried residues: analysis with continuum methods and role of water penetration. Biophys. J. 82, 3289-3304 (2002).
16. a shifts in proteins. Proteins 48, 283-292 (2002).
17. Guillén Schlippe, Y.V. & Hedstrom, L. A twisted base? The role of arginine in enzyme-catalyzed proton abstractions. Arch. Biochem. Biophys. 433, 266-278 (2005).
18. Kim, J., Mao, J. & Gunner, M.R. Are acidic and basic groups in buried proteins predicted to be ionized? J. Mol. Biol. 348, 1283-1298 (2005).
19. + channel. Proc. Natl. Acad. Sci. USA 104, 666-671 (2007).
20. A and acetylcholine receptor M3 segments. J. Neurosci. 26, 4492-4499 (2006).
21. Norberg, J., Foloppe, N. & Nilsson, L. Intrinsic relative stabilities of the neutral tautomers of arginine side-chain models. J. Chem. Theory Comput. 1, 986-993 (2005).
22. Blanton, M.P. & Cohen, J.B. Identifying the lipid-protein interface of the Torpedo nicotinic acetylcholine receptor: secondary structure implications. Biochemistry 33, 2859-2872 (1994).
23. 3H]azicholesterol. Biochemistry 45, 976-986 (2006).
24. Tamamizu, S. et al. Functional effects of periodic tryptophan substitutions in the α M4 transmembrane domain of the Torpedo californica nicotinic acetylcholine receptor. Biochemistry 39, 4666-4673 (2000).
25. Dwyer, T.M., Adams, D.J. & Hille, B. The permeability of the endplate channel to organic cations in frog muscle. J. Gen. Physiol. 75, 469-492 (1980).
26. Cohen, B.N., Labarca, C., Davidson, N. & Lester, H.A. Mutations in M2 alter the selectivity of the mouse nicotinic acetylcholine receptor for organic and alkali metal cations. J. Gen. Physiol. 100, 373-400 (1992).
27. Smart, O.S., Neduvelil, J.G., Wang, X., Wallace, B.A. & Sansom, M.S.P. HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph. 14, 354-360 (1996).
28. Varma, S., Chiu, S.W. & Jakobsson, E. The influence of amino acid protonation states on molecular dynamics simulations of the bacterial porin OmpF. Biophys. J. 90, 112-123 (2006).
29. Beckstein, O. & Sansom, M.S.P. A hydrophobic gate in an ion channel: the closed state of the nicotinic acetylcholine receptor. Phys. Biol. 3, 147-159 (2006).
30. Corry, B. An energy-efficient gating mechanism in the acetylcholine receptor channel suggested by molecular and Brownian dynamics. Biophys. J. 90, 799-810 (2006).
31. White, B.H. & Cohen, J.B. Agonist-induced changes in the structure of the acetylcholine receptor M2 regions revealed by photoincorporation of an uncharged nicotinic noncompetitive antagonist. J. Biol. Chem. 267, 15770-15783 (1992).
32. Beckstein, O., Biggin, P.C. & Sansom, M.S.P. A hydrophobic gating mechanism for nanopores. J. Phys. Chem. B 105, 12902-12905 (2001).
33. Lynden-Bell, R.M. & Rasaiah, J.C. Mobility and solvation of ions in channels. J. Chem. Phys. 105, 9266-9280 (1996).
34. Beckstein, O. & Sansom, M.S.P. The influence of geometry, surface character, and flexibility on the permeation of ions and water through biological pores. Phys. Biol. 1, 42-52 (2004).
35. Peter, C. & Hummer, G. Ion transport through membrane-spanning nanopores studied by molecular dynamics simulations and continuum electrostatics calculations. Biophys. J. 89, 2222-2234 (2005).
36. Sotomayor, M., van der Straaten, T.A., Ravaioli, U. & Schulten, K. Electrostatic properties of the mechanosensitive channel of small conductance MscS. Biophys. J. 90, 3496-3510 (2006).
37. Vora, T., Corry, B. & Chung, S.H. Brownian dynamics investigation into the conductance state of the MscS channel crystal structure. Biochim. Biophys. Acta 1758, 730-737 (2006).
38. + channel. Neuron 56, 124-140 (2007).
39. Qin, F. Restoration of single-channel currents using the segmental k-means method based on hidden Markov modeling. Biophys. J. 86, 1488-1501 (2004).
40. Schwarz, G. Estimating the dimension of a model. Ann. Statist. 6, 461-464 (1978).
41. Qin, F., Auerbach, A. & Sachs, F. Estimating single-channel kinetic parameters from idealized patch-clamp data containing missed events. Biophys. J. 70, 264-280 (1996).
42. Grosman, C., Salamone, F.N., Sine, S.M. & Auerbach, A. The extracellular linker of muscle acetylcholine receptor channels is a gating control element. J. Gen. Physiol. 116, 327-339 (2000).
43. Engel, A.G. et al. New mutations in acetylcholine receptor subunit genes reveal heterogeneity in the slow-channel congenital myasthenic syndrome. Hum. Mol. Genet. 5, 1217-1227 (1996).
44. Grosman, C. & Auerbach, A. Asymmetric and independent contribution of the second transmembrane segment 12′ residues to diliganded gating of acetylcholine receptor channels. A single-channel study with choline as the agonist. J. Gen. Physiol. 115, 637-651 (2000).
45. Ohno, K. et al. Congenital myasthenic syndrome caused by prolonged acetylcholine receptor channel openings due to a mutation in the M2 domain of the e subunit. Proc. Natl. Acad. Sci. USA 92, 758-762 (1995).
46. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 (1996).
47. Frishman, D. & Argos, P. Knowledge-based protein secondary structure assignment. Proteins 23, 566-579 (1995).
48. 125I]TIDPC/16. Biochemistry 37, 14545-14555 (1998).
49. 1H-NMR study on the tautomerism of the imidazole ring of histidine residues. I. Microscopic pK values and molar ratios of tautomers in histidine-containing peptides. Biochim. Biophys. Acta 742, 576-585 (1983).
50. Thurlkill, R.L., Grimsley, G.R., Scholtz, J.M. & Pace, C.N. pK values of the ionizable groups of proteins. Protein Sci. 15, 1214-1218 (2006).
51. a calculations through flexibility based sampling of a water-dominated interaction scheme. Protein Sci. 13, 2793-2805 (2004).
52. Hilf, R.J.C. & Dutzler, R. X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature advance online publication, doi:10.1038/nature06717 (5 March 2008).