Hydrogen bonds as molecular timers for slow inactivation in voltage-gated potassium channels

eLife

Volumn 2013, Issue 2, 2013, Pages

  Pless, Stephan A ^a   Galpin, Jason D ^a,b   Niciforovic, Ana P ^a   Kurata, Harley T ^a   Ahern, Christopher A ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; VOLTAGE GATED POTASSIUM CHANNEL;

ARTICLE; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; DEPOLARIZATION; ELECTROPHYSIOLOGY; HYDROGEN BOND; KINETICS; MOLECULAR BIOLOGY; SITE DIRECTED MUTAGENESIS;

EID: 84890380408     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01289.001     Document Type: Article

References (61)

1. Aldrich RW Jnr, Getting PA, Thompson SH. 1979. Mechanism of frequency-dependent broadening of molluscan neurone soma spikes. J Physiol 291:531-44.
2. Almers W, Armstrong CM. 1980. Survival of K+ permeability and gating currents in squid axons perfused with K+-free media. J Gen Physiol 75:61-78. doi: 10.1085/jgp.75.1.61.
3. Banerjee A, Lee A, Campbell E, Mackinnon R. 2013. Structure of a pore-blocking toxin in complex with a eukaryotic voltage-dependent K(+) channel. eLife 2:e00594. doi: 10.7554/eLife.00594.
4. Baukrowitz T, Yellen G. 1996. Use-dependent blockers and exit rate of the last ion from the multi-ion pore of a K+ channel. Science 271:653-6. doi: 10.1126/science.271.5249.653.
5. Bean BP. 2007. The action potential in mammalian central neurons. Nat Rev Neurosci 8:451-65. doi: 10.1038/nrn2148.
6. Choi KL, Aldrich RW, Yellen G. 1991. Tetraethylammonium blockade distinguishes two inactivation mechanisms in voltage-activated K+ channels. Proc Natl Acad Sci USA 88:5092-5. doi: 10.1073/pnas.88.12.5092.
7. Cordero-Morales JF, Cuello LG, Zhao Y, Jogini V, Cortes DM, Roux B, et al. 2006. Molecular determinants of gating at the potassium-channel selectivity filter. Nat Struct Mol Biol 13:311-8. doi: 10.1038/nsmb1069.
8. Cordero-Morales JF, Jogini V, Chakrapani S, Perozo E. 2011. A multipoint hydrogen-bond network underlying KcsA C-type inactivation. Biophys J 100:2387-93. doi: 10.1016/j.bpj.2011.01.073.
9. Cordero-Morales JF, Jogini V, Lewis A, Vasquez V, Cortes DM, Roux B, et al. 2007. Molecular driving forces determining potassium channel slow inactivation. Nat Struct Mol Biol 14:1062-9. doi: 10.1038/nsmb1309.
10. Cuello LG, Jogini V, Cortes DM, Pan AC, Gagnon DG, Dalmas O, et al. 2010a. Structural basis for the coupling between activation and inactivation gates in K(+) channels. Nature 466:272-5. doi: 10.1038/nature09136.
11. Cuello LG, Jogini V, Cortes DM, Perozo E. 2010b. Structural mechanism of C-type inactivation in K(+) channels. Nature 466:203-8. doi: 10.1038/nature09153.
12. Deutsch CJ, Taylor JS. 1987. Intracellular pH as measured by 19F NMR. Ann N Y Acad Sci 508:33-47. doi: 10.1111/j.1749-6632.1987.tb32892.x.
13. Deutsch CJ, Taylor JS. 1989. New class of 19F pH indicators: fluoroanilines. Biophys J 55:799-804. doi: 10.1016/S0006-3495(89)82879-6.
14. Dougherty DA. 1996. Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271:163-8. doi: 10.1126/science.271.5246.163.
15. Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, et al. 1998. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69-77. doi: 10.1126/science.280.5360.69.
16. Eriksson MA, Roux B. 2002. Modeling the structure of agitoxin in complex with the Shaker K+ channel: a computational approach based on experimental distance restraints extracted from thermodynamic mutant cycles. Biophys J 83:2595-609. doi: 10.1016/S0006-3495(02)75270-3.
17. Grissmer S, Cahalan M. 1989. TEA prevents inactivation while blocking open K+ channels in human T lymphocytes. Biophys J 55:203-6. doi: 10.1016/S0006-3495(89)82793-6.
18. Harris RE, Larsson HP, Isacoff EY. 1998. A permanent ion binding site located between two gates of the Shaker K+ channel. Biophys J 74:1808-20. doi: 10.1016/S0006-3495(98)77891-9.
19. Heginbotham L, Lu Z, Abramson T, MacKinnon R. 1994. Mutations in the K+ channel signature sequence. BiophysJ 66:1061-7. doi: 10.1016/S0006-3495(94)80887-2.
20. Hille B. 2001. Ion channels of excitable membranes, (3rd edition). Sunderland, Mass: Sinauer. p. 814.
21. Hoshi T, Armstrong CM. 2013. C-type inactivation of voltage-gated K+ channels: pore constriction or dilation? J Gen Physiol 141:151-60. doi: 10.1085/jgp.201210888.
22. Hoshi T, Zagotta WN, Aldrich RW. 1990. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science 250:533-8. doi: 10.1126/science.2122519.
23. Hoshi T, Zagotta WN, Aldrich RW. 1991. Two types of inactivation in Shaker K+ channels: effects of alterations in the carboxy-terminal region. Neuron 7:547-56. doi: 10.1016/0896-6273(91)90367-9.
24. Hurst RS, North RA, Adelman JP. 1995. Potassium channel assembly from concatenated subunits: effects of proline substitutions in S4 segments. Receptors Channels 3:263-72.
25. Hurst RS, Toro L, Stefani E. 1996. Molecular determinants of external barium block in Shaker potassium channels. FEBS Lett 388:59-65. doi: 10.1016/0014-5793(96)00516-9.
26. Kiss L, LoTurco J, Korn SJ. 1999. Contribution of the selectivity filter to inactivation in potassium channels. Biophys J 76:253-63. doi: 10.1016/S0006-3495(99)77194-8.
27. Kitaguchi T, Sukhareva M, Swartz KJ. 2004. Stabilizing the closed S6 gate in the Shaker Kv channel through modification of a hydrophobic seal. J Gen Physiol 124:319-32. doi: 10.1085/jgp.200409098.
28. Kurata HT, Fedida D. 2006. A structural interpretation of voltage-gated potassium channel inactivation. Prog Biophys Mol Biol 92:185-208. doi: 10.1016/j.pbiomolbio.2005.10.001.
29. Lacroix JJ, Pless SA, Maragliano L, Campos FV, Galpin JD, Ahern CA, et al. 2012. Intermediate state trapping of a voltage sensor. J Gen Physiol 140:635-52. doi: 10.1085/jgp.201210827.
30. Larsson HP, Elinder F. 2000. A conserved glutamate is important for slow inactivation in K+ channels. Neuron 27:573-83. doi: 10.1016/S0896-6273(00)00067-2.
31. Liu Y, Jurman ME, Yellen G. 1996. Dynamic rearrangement of the outer mouth of a K+ channel during gating. Neuron 16:859-67. doi: 10.1016/S0896-6273(00)80106-3.
32. Liu Y, Holmgren M, Jurman ME, Yellen G. 1997. Gated access to the pore of a voltage-dependent K+ channel. Neuron 19:175-84. doi: 10.1016/S0896-6273(00)80357-8.
33. Loboda A, Melishchuk A, Armstrong C. 2001. Dilated and defunct K channels in the absence of K+. Biophys J 80:2704-14. doi: 10.1016/S0006-3495(01)76239-X.
34. Long SB, Campbell EB, Mackinnon R. 2005. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309:897-903. doi: 10.1126/science.1116269.
35. Long SB, Tao X, Campbell EB, MacKinnon R. 2007. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 450:376-82. doi: 10.1038/nature06265.
36. Loots E, Isacoff EY. 1998. Protein rearrangements underlying slow inactivation of the Shaker K+ channel. J Gen Physiol 112:377-89. doi: 10.1085/jgp.112.4.377.
37. Loots E, Isacoff EY. 2000. Molecular coupling of S4 to a K(+) channel's slow inactivation gate. J Gen Physiol 116:623-36. doi: 10.1085/jgp.116.5.623.
38. Lopez-Barneo J, Hoshi T, Heinemann SH, Aldrich RW. 1993. Effects of external cations and mutations in the pore region on C-type inactivation of Shaker potassium channels. Receptors Channels 1:61-71.
39. McCormack K, Lin L, Iverson LE, Tanouye MA, Sigworth FJ. 1992. Tandem linkage of Shaker K+ channel subunits does not ensure the stoichiometry of expressed channels. Biophys J 63:1406-11. doi: 10.1016/S0006-3495(92)81703-4.
40. Molina A, Castellano AG, Lopez-Barneo J. 1997. Pore mutations in Shaker K+ channels distinguish between the sites of tetraethylammonium blockade and C-type inactivation. J Physiol 499:361-7.
41. Molina A, Ortega-Saenz P, Lopez-Barneo J. 1998. Pore mutations alter closing and opening kinetics in Shaker K+ channels. J Physiol 509:327-37. doi: 10.1111/j.1469-7793.1998.327bn.x.
42. Ogielska EM, Zagotta WN, Hoshi T, Heinemann SH, Haab J, Aldrich RW. 1995. Cooperative subunit interactions in C-type inactivation of K channels. Biophys J 69:2449-57. doi: 10.1016/S0006-3495(95)80114-1.
43. Ostmeyer J, Chakrapani S, Pan AC, Perozo E, Roux B. 2013. Recovery from slow inactivation in K channels is controlled by water molecules. Nature 501:121-4. doi: 10.1038/nature12395.
44. Panyi G, Sheng Z, Deutsch C. 1995. C-type inactivation of a voltage-gated K+ channel occurs by a cooperative mechanism. Biophys J 69:896-903. doi: 10.1016/S0006-3495(95)79963-5.
45. Peng Y, Scarsdale JN, Kellogg GE. 2007. Hydropathic analysis and comparison of KcsA and Shaker potassium channels. Chem Biodivers 4:2578-92. doi: 10.1002/cbdv.200790211.
46. Perozo E, MacKinnon R, Bezanilla F, Stefani E. 1993. Gating currents from a nonconducting mutant reveal open-closed conformations in Shaker K+ channels. Neuron 11:353-8. doi: 10.1016/0896-6273(93)90190-3.
47. Pless SA, Ahern CA. 2013. Unnatural amino acids as probes of ligand-receptor interactions and their conformational consequences. Annu Rev Pharmacol Toxicol 53:211-29. doi: 10.1146/annurev-pharmtox-011112-140343.
48. Pless SA, Galpin JD, Niciforovic AP, Ahern CA. 2011. Contributions of counter-charge in a potassium channel voltage-sensor domain. Nat Chem Biol 7:617-23. doi: 10.1038/nchembio.622.
49. Pless SA, Niciforovic AP, Galpin JD, Nunez JJ, Kurata HT, Ahern CA. 2013. A novel mechanism for fine-tuning open-state stability in a voltage-gated potassium channel. Nat Commun 4:1784. doi: 10.1038/ncomms2761.
50. Rossi M, Tkatchenko A, Rempe SB, Varma S. 2013. Role of methyl-induced polarization in ion binding. Proc Natl Acad Sci USA 110:12978-83. doi: 10.1073/pnas.1302757110.
51. Sanguinetti MC, Tristani-Firouzi M. 2006. hERG potassium channels and cardiac arrhythmia. Nature 440:463-9. doi: 10.1038/nature04710.
52. Shoichet BK, Baase WA, Kuroki R, Matthews BW. 1995. A relationship between protein stability and protein function. Proc Natl Acad Sci USA 92:452-6. doi: 10.1073/pnas.92.2.452.
53. Smith PL, Baukrowitz T, Yellen G. 1996. The inward rectification mechanism of the HERG cardiac potassium channel. Nature 379:833-6. doi: 10.1038/379833a0.
54. Spector PS, Curran ME, Zou A, Keating MT, Sanguinetti MC. 1996. Fast inactivation causes rectification of the IKr channel. J Gen Physiol 107:611-9. doi: 10.1085/jgp.107.5.611.
55. Starkus JG, Kuschel L, Rayner MD, Heinemann SH. 1997. Ion conduction through C-type inactivated Shaker channels. J Gen Physiol 110:539-50. doi: 10.1085/jgp.110.5.539.
56. van der Cruijsen EA, Nand D, Weingarth M, Prokofyev A, Hornig S, Cukkemane AA, et al. 2013. Importance of lipid-pore loop interface for potassium channel structure and function. Proc Natl Acad Sci USA 110:13008-13. doi: 10.1073/pnas.1305563110.
57. Yang Y, Yan Y, Sigworth FJ. 1997. How does the W434F mutation block current in Shaker potassium channels? J Gen Physiol 109:779-89. doi: 10.1085/jgp.109.6.779.
58. Yellen G, Sodickson D, Chen TY, Jurman ME. 1994. An engineered cysteine in the external mouth of a K+ channel allows inactivation to be modulated by metal binding. Biophys J 66:1068-75. doi: 10.1016/S0006-3495(94)80888-4.
59. Yool AJ, Schwarz TL. 1991. Alteration of ionic selectivity of a K+ channel by mutation of the H5 region. Nature 349:700-4. doi: 10.1038/349700a0.
60. Zheng J, Sigworth FJ. 1997. Selectivity changes during activation of mutant Shaker potassium channels. J Gen Physiol 110:101-17. doi: 10.1085/jgp.110.2.101.
61. Zhou M, Morais-Cabral JH, Mann S, MacKinnon R. 2001. Potassium channel receptor site for the inactivation gate and quaternary amine inhibitors. Nature 411:657-61. doi: 10.1038/35079500.