On the structural basis of modal gating behavior in K+ channels

Nature Structural and Molecular Biology

Volumn 18, Issue 1, 2011, Pages 67-75

  Chakrapani, Sudha ^a,b   Cordero Morales, Julio F ^a,b,c   Jogini, Vishwanath ^a,b,d   Pan, Albert C ^a,b,e   Cortes, D Marien ^a,b,f   Roux, Benoît ^a   Perozo, Eduardo ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d D E Shaw Research   (India)

^e D E SHAW RESEARCH   (United States)

^f TEXAS TECH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; POTASSIUM CHANNEL;

ARTICLE; CHANNEL GATING; CHEMICAL INTERACTION; CRYSTAL STRUCTURE; HUMAN; POINT MUTATION; PRIORITY JOURNAL; REGULATORY MECHANISM;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; ION CHANNEL GATING; KINETICS; MODELS, MOLECULAR; MUTATION; POTASSIUM CHANNELS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, PROTEIN;

EID: 78650972577     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1968     Document Type: Article

References (60)

1. Hille, B. Ion Channels of Excitable Membranes (Sinauer Associates Inc., 2001).
2. Yellen, G. The moving parts of voltage-gated ion channels. Q. Rev. Biophys. 31, 239-295 (1998).
3. + conduction and selectivity. Science 280, 69-77 (1998).
4. Kuo, A. et al. Crystal structure of the potassium channel KirBac1.1 in the closed state. Science 300, 1922-1926 (2003).
5. + channel-Fab complex at 2.0 A resolution. Nature 414, 43-48 (2001).
6. Jiang, Y. et al. Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417, 515-522 (2002).
7. + channel. Science 309, 897-903 (2005).
8. + channel in a lipid membrane-like environment. Nature 450, 376-382 (2007).
9. + channels. Nature 466, 203-208 (2010).
10. Schoppa, N.E. & Sigworth, F.J. Activation of shaker potassium channels. I. Characterization of voltage-dependent transitions. J. Gen. Physiol. 111, 271-294 (1998).
11. Cordero-Morales, J.F. et al. Molecular determinants of gating at the potassium-channel selectivity flter. Nat. Struct. Mol. Biol. 13, 311-318 (2006).
12. Chakrapani, S., Cordero-Morales, J.F. & Perozo, E. A quantitative description of KcsA gating II: single-channel currents. J. Gen. Physiol. 130, 479-496 (2007).
13. Zagotta, W.N., Hoshi, T. & Aldrich, R.W. Shaker potassium channel gating. III: Evaluation of kinetic models for activation. J. Gen. Physiol. 103, 321-362 (1994).
14. Schrempf, H. et al. A prokaryotic potassium ion channel with two predicted transmembrane segments from Streptomyces lividans. EMBO J. 14, 5170-5178 (1995).
15. + channel. Biochemistry 37, 3229-3236 (1998).
16. Chapman, M.L. & VanDongen, A.M. K channel subconductance levels result from heteromeric pore conformations. J. Gen. Physiol. 126, 87-103 (2005).
17. Zheng, J. & Sigworth, F.J. Selectivity changes during activation of mutant Shaker potassium channels. J. Gen. Physiol. 110, 101-117 (1997).
18. Blunck, R., Cordero-Morales, J.F., Cuello, L.G., Perozo, E. & Bezanilla, F. Detection of the opening of the bundle crossing in KcsA with fuorescence lifetime spectroscopy reveals the existence of two gates for ion conduction. J. Gen. Physiol. 128, 569-581 (2006).
19. Chakrapani, S., Cordero-Morales, J.F. & Perozo, E. A quantitative description of KcsA gating I: macroscopic currents. J. Gen. Physiol. 130, 465-478 (2007).
20. Pusch, M., Bertorello, L. & Conti, F. Gating and fickery block differentially affected by rubidium in homomeric KCNQ1 and heteromeric KCNQ1/KCNE1 potassium channels. Biophys. J. 78, 211-226 (2000).
21. + channel correlate with occupancy of the pore. Biophys. J. 61, 639-648 (1992).
22. LeMasurier, M., Heginbotham, L. & Miller, C. KcsA: it's a potassium channel. J. Gen. Physiol. 118, 303-314 (2001).
23. Choe, H., Sackin, H. & Palmer, L.G. Gating properties of inward-rectifer potassium channels: effects of permeant ions. J. Membr. Biol. 184, 81-89 (2001).
24. Lu, T., Wu, L., Xiao, J. & Yang, J. Permeant ion-dependent changes in gating of Kir2.1 inward rectifer potassium channels. J. Gen. Physiol. 118, 509-522 (2001).
25. + channel with backbone mutations in the selectivity flter. Nat. Neurosci. 4, 239-246 (2001).
26. + channel with altered conduction properties and selectivity flter ion distribution. J. Mol. Biol. 338, 839-846 (2004).
27. + fow by a ring of negative charges in the outer pore of BKCa channels. Part II: Neutralization of aspartate 292 reduces long channel openings and gating current slow component. J. Gen. Physiol. 124, 185-197 (2004).
28. Proks, P., Capener, C.E., Jones, P. & Ashcroft, F.M. Mutations within the P-loop of Kir6.2 modulate the intraburst kinetics of the ATP-sensitive potassium channel. J. Gen. Physiol. 118, 341-353 (2001).
29. + selectivity flter. Nature 414, 37-42 (2001).
30. + channel switches between two distinct gating modes resulting in either inward-rectifying or 'leak' current. FEBS Lett. 505, 233-239 (2001).
31. v1.1. Pfugers Arch. 439, 18-26 (1999).
32. Cooper, E. & Shrier, A. Inactivation of A currents and A channels on rat nodose neurons in culture. J. Gen. Physiol. 94, 881-910 (1989).
33. Armstrong, C.M. & Gilly, W.F. Fast and slow steps in the activation of sodium channels. J. Gen. Physiol. 74, 691-711 (1979).
34. Howe, J.R. & Ritchie, J.M. Multiple kinetic components of sodium channel inactivation in rabbit Schwann cells. J. Physiol. (Lond.) 455, 529-566 (1992).
35. Lenaeus, M.J., Vamvouka, M., Focia, P.J. & Gross, A. Structural basis of TEA blockade in a model potassium channel. Nat. Struct. Mol. Biol. 12, 454-459 (2005).
36. Bockenhauer, D., Zilberberg, N. & Goldstein, S.A. KCNK2: reversible conversion of a hippocampal potassium leak into a voltage-dependent channel. Nat. Neurosci. 4, 486-491 (2001).
37. + channel alpha subunit modulates the inactivation conferred by a beta subunit. Involvement of cytoskeleton. J. Biol. Chem. 271, 29321-29328 (1996).
38. Cordero-Morales, J.F. et al. Molecular driving forces determining potassium channel slow inactivation. Nat. Struct. Mol. Biol. 14, 1062-1069 (2007).
39. Capener, C.E., Proks, P., Ashcroft, F.M. & Sansom, M.S. Filter fexibility in a mammalian K channel: models and simulations of Kir6.2 mutants. Biophys. J. 84, 2345-2356 (2003).
40. Domene, C., Klein, M.L., Branduardi, D., Gervasio, F.L. & Parrinello, M. Conformational changes and gating at the selectivity flter of potassium channels. J. Am. Chem. Soc. 130, 9474-9480 (2008).
41. + channel in a bilayer membrane. Biophys. J. 78, 2900-2917 (2000).
42. Shrivastava, I.H. & Sansom, M.S. Simulations of ion permeation through a potassium channel: molecular dynamics of KcsA in a phospholipid bilayer. Biophys. J. 78, 557-570 (2000).
43. + channel. FEBS Lett. 477, 37-42 (2000).
44. Bernèche, S. & Roux, B. A gate in the selectivity flter of potassium channels. Structure 13, 591-600 (2005).
45. Nishida, M., Cadene, M., Chait, B.T. & MacKinnon, R. Crystal structure of a Kir3.1-prokaryotic Kir channel chimera. EMBO J. 26, 4005-4015 (2007).
46. Delcour, A.H., Lipscombe, D. & Tsien, R.W. Multiple modes of N-type calcium channel activity distinguished by differences in gating kinetics. J. Neurosci. 13, 181-194 (1993).
47. Luvisetto, S. et al. Modal gating of human CaV2.1 (P/Q-type) calcium channels: I. The slow and the fast gating modes and their modulation by beta subunits. J. Gen. Physiol. 124, 445-461 (2004).
48. Yue, D.T., Herzig, S. & Marban, E. Beta-adrenergic stimulation of calcium channels occurs by potentiation of high-activity gating modes. Proc. Natl. Acad. Sci. USA 87, 753-757 (1990).
49. McManus, O.B. & Magleby, K.L. Kinetic states and modes of single large-conductance calcium-activated potassium channels in cultured rat skeletal muscle. J. Physiol. (Lond.) 402, 79-120 (1988).
50. 2+-independent long shut intervals in BK channels from rat muscle. J. Physiol. (Lond.) 493, 673-689 (1996).
51. Auerbach, A. & Lingle, C.J. Heterogeneous kinetic properties of acetylcholine receptor channels in Xenopus myocytes. J. Physiol. (Lond.) 378, 119-140 (1986).
52. Milone, M. et al. Mode switching kinetics produced by a naturally occurring mutation in the cytoplasmic loop of the human acetylcholine receptor epsilon subunit. Neuron 20, 575-588 (1998).
53. Naranjo, D. & Brehm, P. Modal shifts in acetylcholine receptor channel gating confer subunit-dependent desensitization. Science 260, 1811-1814 (1993).
54. Popescu, G. & Auerbach, A. Modal gating of NMDA receptors and the shape of their synaptic response. Nat. Neurosci. 6, 476-483 (2003).
55. Patlak, J.B., Gration, K.A. & Usherwood, P.N. Single glutamate-activated channels in locust muscle. Nature 278, 643-645 (1979).
56. Huganir, R.L., Delcour, A.H., Greengard, P. & Hess, G.P. Phosphorylation of the nicotinic acetylcholine receptor regulates its rate of desensitization. Nature 321, 774-776 (1986).
57. Levy, D.I. & Deutsch, C. Recovery from C-type inactivation is modulated by extracellular potassium. Biophys. J. 70, 798-805 (1996).
58. 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).
59. Brooks, B.R. et al. CHARMM: A program for macromolecular energy, minimization and dynamics calculations. J. Comput. Chem. 4, 187-217 (1983).
60. Phillips, J.C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005).