Charge substitution for a deep-pore residue reveals structural dynamics during BK channel gating

Journal of General Physiology

Volumn 138, Issue 2, 2011, Pages 137-154

  Chen, Xixi ^a   Aldrich, Richard W ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; METHIONINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CELL CULTURE; CELL MEMBRANE POTENTIAL; CELL STRAIN HEK293; CHANNEL GATING; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PH; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARGININE; CELLS, CULTURED; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; ION CHANNEL GATING; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MEMBRANE POTENTIALS; METHIONINE; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 79961119376     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201110632     Document Type: Article

References (51)

1. Barrett, J.N., K.L. Magleby, and B.S. Pallotta. 1982. Properties of single calcium-activated potassium channels in cultured rat muscle. J. Physiol. 331:211-230.
2. + and contribute to the limits of unitary currents at high voltages. J. Gen. Physiol. 123:305-319.
3. Brelidze, T.I., and K.L. Magleby. 2005. Probing the geometry of the inner vestibule of BK channels with sugars. J. Gen. Physiol. 126:105-121.
4. + channels. Proc. Natl. Acad. Sci. USA. 88:5092-5095.
5. Contreras, J.E., and M. Holmgren. 2006. Access of quaternary ammonium blockers to the internal pore of cyclic nucleotide-gated channels: implications for the location of the gate. J. Gen. Physiol. 127:481-494.
6. Contreras, J.E., D. Srikumar, and M. Holmgren. 2008. Gating at the selectivity filter in cyclic nucleotide-gated channels. Proc. Natl. Acad. Sci. USA. 105:3310-3314.
7. + channel. J. Gen. Physiol. 110:257-281.
8. Cuello, L.G., V. Jogini, D.M. Cortes, A.C. Pan, D.G. Gagnon, O. Dalmas, J.F. Cordero-Morales, S. Chakrapani, B. Roux, and E. Perozo. 2010a. Structural basis for the coupling between activation and inactivation gates in K(+) channels. Nature. 466:272-275.
9. Cuello, L.G., V. Jogini, D.M. Cortes, and E. Perozo. 2010b. Structural mechanism of C-type inactivation in K(+) channels. Nature. 466:203-208.
10. Cui, J., and R.W. Aldrich. 2000. Allosteric linkage between voltage and Ca(2+)-dependent activation of BK-type mslo1 K(+) channels. Biochemistry. 39:15612-15619.
11. + channels. J. Gen. Physiol. 109:647-673.
12. Cymes, G.D., and C. Grosman. 2008. Pore-opening mechanism of the nicotinic acetylcholine receptor evinced by proton transfer. Nat. Struct. Mol. Biol. 15:389-396.
13. Cymes, G.D., and C. Grosman. 2011. Tunable pK(a) values and the basis of opposite charge selectivities in nicotinic-type receptors. Nature.
14. Cymes, G.D., C. Grosman, and A. Auerbach. 2002. Structure of the transition state of gating in the acetylcholine receptor channel pore: a phi-value analysis. Biochemistry. 41:5548-5555.
15. Cymes, G.D., Y. Ni, and C. Grosman. 2005. Probing ion-channel pores one proton at a time. Nature. 438:975-980.
16. del Camino, D., and G. Yellen. 2001. Tight steric closure at the intracellular activation gate of a voltage-gated K(+) channel. Neuron. 32:649-656.
17. + channel and its structural implications. Nature. 403:321-325.
18. + conduction and selectivity. Science. 280:69-77.
19. Flynn, G.E., and W.N. Zagotta. 2001. Conformational changes in S6 coupled to the opening of cyclic nucleotide-gated channels. Neuron. 30:689-698.
20. Flynn, G.E., J.P. Johnson Jr., and W.N. Zagotta. 2001. Cyclic nucleotide-gated channels: shedding light on the opening of a channel pore. Nat. Rev. Neurosci. 2:643-651.
21. Grosman, C., M. Zhou, and A. Auerbach. 2000. Mapping the conformational wave of acetylcholine receptor channel gating. Nature. 403:773-776.
22. + channels: evidence for a trap door mechanism of activation gating. J. Gen. Physiol. 109:527-535.
23. + channel can be trapped in the open state by an intersubunit metal bridge. Neuron. 21:617-621.
24. 2+). J. Gen. Physiol. 114:305-336.
25. 2+ binding and channel opening in large conductance (BK) potassium channels. J. Gen. Physiol. 120:267-305.
26. 2+). J. Gen. Physiol. 114:277-304.
27. + channels: effects of alterations in the carboxyterminal region. Neuron. 7:547-556.
28. Hou, S., R. Xu, S.H. Heinemann, and T. Hoshi. 2008. Reciprocal regulation of the Ca2+ and H+ sensitivity in the SLO1 BK channel conferred by the RCK1 domain. Nat. Struct. Mol. Biol. 15:403-410.
29. Hou, S., F.T. Horrigan, R. Xu, S.H. Heinemann, and T. Hoshi. 2009. Comparative effects of H+ and Ca2+ on large-conductance Ca2+and voltage-gated Slo1 K+ channels. Channels (Austin). 3:249-258.
30. Jiang, Y., A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon. 2002. Crystal structure and mechanism of a calcium-gated potassium channel. Nature. 417:515-522.
31. Johnson, J.P. Jr., and W.N. Zagotta. 2001. Rotational movement during cyclic nucleotide-gated channel opening. Nature. 412:917-921.
32. Kollewe, A., A.Y. Lau, A. Sullivan, B. Roux, and S.A. Goldstein. 2009. A structural model for K2P potassium channels based on 23 pairs of interacting sites and continuum electrostatics. J. Gen. Physiol. 134:53-68.
33. Li, W., and R.W. Aldrich. 2004. Unique inner pore properties of BK channels revealed by quaternary ammonium block. J. Gen. Physiol. 124:43-57.
34. Li, W., and R.W. Aldrich. 2006. State-dependent block of BK channels by synthesized shaker ball peptides. J. Gen. Physiol. 128:423-441.
35. Liu, Y., M.E. Jurman, and G. Yellen. 1996. Dynamic rearrangement of the outer mouth of a K+ channel during gating. Neuron. 16:859-867.
36. Liu, Y., M. Holmgren, M.E. Jurman, and G. Yellen. 1997. Gated access to the pore of a voltage-dependent K+ channel. Neuron. 19:175-184.
37. Long, S.B., E.B. Campbell, and R. Mackinnon. 2005. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science. 309:897-903.
38. Marty, A., and E. Neher. 1985. Potassium channels in cultured bovine adrenal chromaffin cells. J. Physiol. 367:117-141.
39. Piskorowski, R.A., and R.W. Aldrich. 2006. Relationship between pore occupancy and gating in BK potassium channels. J. Gen. Physiol. 127:557-576.
40. + channels described by a two-tiered allosteric gating mechanism. J. Gen. Physiol. 116:75-99.
41. Tang, Q.Y., X.H. Zeng, and C.J. Lingle. 2009. Closed-channel block of BK potassium channels by bbTBA requires partial activation. J. Gen. Physiol. 134:409-436.
42. Tang, X.D., H. Daggett, M. Hanner, M.L. Garcia, O.B. McManus, N. Brot, H. Weissbach, S.H. Heinemann, and T. Hoshi. 2001. Oxidative regulation of large conductance calcium-activated potassium channels. J. Gen. Physiol. 117:253-274.
43. Wilkens, C.M., and R.W. Aldrich. 2006. State-independent block of BK channels by an intracellular quaternary ammonium. J. Gen. Physiol. 128:347-364.
44. Wu, Y., Y. Yang, S. Ye, and Y. Jiang. 2010. Structure of the gating ring from the human large-conductance Ca(2+)-gated K(+) channel. Nature. 466:393-397.
45. Xia, X.M., X. Zeng, and C.J. Lingle. 2002. Multiple regulatory sites in large-conductance calcium-activated potassium channels. Nature. 418:880-884.
46. Yellen, G., D. Sodickson, T.Y. Chen, and M.E. Jurman. 1994. An engineered cysteine in the external mouth of a K+ channel allows inactivation to be modulated by metal binding. Biophys. J. 66:1068-1075.
47. 2+-activation apparatus at 3.0 A resolution. Science. 329:182-186.
48. Zeng, X.H., X.M. Xia, and C.J. Lingle. 2005. Divalent cation sensitivity of BK channel activation supports the existence of three distinct binding sites. J. Gen. Physiol. 125:273-286.
49. 2+)-dependent gating of large conductance (BK) potassium channels. J. Gen. Physiol. 125:213-236.
50. Zhou, Y., and R. MacKinnon. 2003. The occupancy of ions in the K+ selectivity filter: charge balance and coupling of ion binding to a protein conformational change underlie high conduction rates. J. Mol. Biol. 333:965-975.
51. Zhou, Y., X. Xia, and C.J. Lingle. 2010. Inhibition of large-conductance Ca2+-activated K+ channels by nanomolar concentrations of Ag+. Mol. Pharmacol. 78:952-960.