Fluorescence-tracking of activation gating in human ERG channels reveals rapid S4 movement and slow pore opening

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Es Salah Lamoureux, Zeineb ^a   Fougere, Robert ^a   Xiong, Ping Yu ^a   Robertson, Gail A ^b   Fedida, David ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; FLUORESCENT DYE; POTASSIUM CHANNEL HERG; TETRAMETHYLRHODAMINE 5 MALEIMIDE; UNCLASSIFIED DRUG; VALINE; VOLTAGE GATED POTASSIUM CHANNEL;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRIC POTENTIAL; FEMALE; FLUORESCENCE ANALYSIS; MEMBRANE POLARIZATION AND DEPOLARIZATION; MEMBRANE POTENTIAL; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; POTASSIUM CONDUCTANCE; POTASSIUM CURRENT; PROTEIN FUNCTION; SIGNAL DETECTION; SIGNAL TRANSDUCTION; TRANSPORT KINETICS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CYSTEINE; ETHER-A-GO-GO POTASSIUM CHANNELS; FLUORESCENCE; HUMANS; ION CHANNEL GATING; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; RHODAMINES; TIME FACTORS; XENOPUS;

MAMMALIA;

EID: 77956274149     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010876     Document Type: Article

References (47)

1. Warmke J, Drysdale R, Ganetzky B (1991) A distinct potassium channel polypeptide encoded by the Drosophila eag locus. Science 252: 1560-1562.
2. Sanguinetti MC, Jiang C, Curran ME, Keating MT (1995) A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell 81: 299-307.
3. Trudeau MC, Warmke JW, Ganetzky B, Robertson GA (1995) HERG, a human inward rectifier in the voltage-gated potassium channel family. Science 269: 92-95.
4. Piper DR, Varghese A, Sanguinetti MC, Tristani-Firouzi M (2003) Gating currents associated with intramembrane charge displacement in HERG potassium channels. Proc Natl Acad Sci USA 100: 10534-10539.
5. + channel voltage sensor. Proc Natl Acad Sci USA 102: 18718-18723.
6. + channel. Neuron 14: 1293-1301.
7. Wynia-Smith SL, Gillian-Daniel AL, Satyshur KA, Robertson GA (2008) hERG gating microdomains defined by S6 mutagenesis and molecular modeling. J Gen Physiol 132: 507-520.
8. + channels. J Biol Chem 277: 18994-19000.
9. Liu J, Zhang M, Jiang M, Tseng GN (2003) Negative charges in the transmembrane domains of the HERG K channel are involved in the activation- and deactivation-gating processes. J Gen Physiol 121: 599-614.
10. Piper DR, Hinz WA, Tallurri CK, Sanguinetti MC, Tristani-Firouzi M (2005) Regional specificity of human ether-a9-go-go-related gene channel activation and inactivation gating. J Biol Chem 280: 7206-7217.
11. Smith PL, Yellen G (2002) Fast and slow voltage sensor movements in HERG potassium channels. J Gen Physiol 119: 275-293.
12. + channel with fluorescence. Neuron 19: 1127-1140.
13. Mannuzzu LM, Moronne MM, Isacoff EY (1996) Direct physical measurement of conformational rearrangement underlying potassium channel gating. Science 271: 213-216.
14. Bezanilla F (2000) The voltage sensor in voltage-dependent ion channels. Physiological Reviews 80: 555-592.
15. + channel, Kv1.5, incorporates Q1 and Q2 charge components. Am J Physiol Heart Circ Physiol 277: H1956-H1966.
16. Claydon TW, Vaid M, Rezazadeh S, Kehl SJ, Fedida D (2007) 4-aminopyridine prevents the conformational changes associated with P/C-type inactivation in Shaker channels. J Pharmacol Exp Ther 320: 162-172.
17. Vaid M, Claydon TW, Rezazadeh S, Fedida D (2008) Voltage clamp fluorimetry reveals a novel outer pore instability in a mammalian voltage-gated potassium channel. J Gen Physiol 132: 209-222.
18. + channels at low pH. J Gen Physiol 129: 437-455.
19. Zhuang X, Ha T, Kim HD, Centner T, Labeit S, et al. (2000) Fluorescence quenching: A tool for single-molecule protein-folding study. Proc Natl Acad Sci USA 97: 14241-14244.
20. Johnson JP, Jr., Balser JR, Bennett PB (2001) A novel extracellular calcium sensing mechanism in voltage-gated potassium ion channels. J Neurosci 21: 4143-4153.
21. Nakajima T, Furukawa T, Hirano Y, Tanaka T, Sakurada H, et al. (1999) Voltage-shift of the current activation in HERG S4 mutation (R534C) in LQT2. Cardiovasc Res 44: 283-293.
22. Horne AJ, Fedida D (2009) Use of voltage clamp fluorimetry in understanding potassium channel gating: a review of Shaker fluorescence data. Can J Physiol Pharmacol 87: 411-418.
23. Zagotta WN, Hoshi T, Aldrich RW (1994) Shaker potassium channel gating. III: Evaluation of kinetic models for activation. J Gen Physiol 103: 321-362.
24. 2+ binding and channel opening in large conductance (BK) potassium channels. J Gen Physiol 120: 267-305.
25. + channels. Circ Res 82: 386-395.
26. Anumonwo JMB, Horta J, Delmar M, Taffet SM, Jalife J (1999) Proton and zinc effects on HERG currents. Biophys J 77: 282-298.
27. Jiang M, Dun W, Tseng GN (1999) Mechanism for the effects of extracellular acidification on HERG-channel function. Am J Physiol 277: H1283-H1292.
28. + channel. Neuron 27: 585-595.
29. + channel. Neuron 56: 124-140.
30. Claydon TW, Fedida D (2007) Voltage clamp fluorimetry studies of mammalian voltage-gated K(+) channel gating. Biochem Soc Trans 35: 1080-1082.
31. Zhang M, Liu J, Tseng GN (2004) Gating charges in the activation and inactivation processes of the HERG channel. J Gen Physiol 124: 703-718.
32. Elliott DJ, Dondas NY, Munsey TS, Sivaprasadarao A (2009) Movement of the S4 segment in the hERG potassium channel during membrane depolarization. Mol Membr Biol 26: 435-447.
33. Clarke CE, Hill AP, Zhao J, Kondo M, Subbiah RN, et al. (2006) Effect of S5P alpha-helix charge mutants on inactivation of hERG K+ channels. J Physiol 573: 291-304.
34. + channel by the scorpion toxin CnErg1. Biophys J 92: 3915-3929.
35. + channel. J Biol Chem 284: 1000-1008.
36. Zhao JT, Hill AP, Varghese A, Cooper AA, Swan H, et al. (2009) Not All hERG pore domain mutations have a severe phenotype: G584S has an inactivation gating defect with mild phenotype compared to G572S, which has a dominant negative trafficking defect and a severe phenotype. J Cardiovasc Electrophysiol 20: 923-930.
37. Smith PL, Baukrowitz T, Yellen G (1996) The inward rectification mechanism of the HERG cardiac potassium channel. Nature 379: 833-836.
38. Furutani M, Trudeau MC, Hagiwara N, Seki A, Gong QM, et al. (1999) Novel mechanism associated with an inherited cardiac arrhythmia - Defective protein trafficking by the mutant HERG (G601S) potassium channel. Circulation 99: 2290-2294.
39. Thomas D, Hammerling BC, Wu K, Wimmer AB, Ficker EK, et al. (2004) Inhibition of cardiac HERG currents by the DNA topoisomerase II inhibitor amsacrine: mode of action. Br J Pharmacol 142: 485-494.
40. + channels expressed in Xenopus oocytes reduces rectification by shifting the voltage dependence of inactivation. J Physiol (Camb) 509: 129-137.
41. Choveau FS, El Harchi A, Rodriguez N, Louerat-Oriou B, Baro I, et al. (2009) Transfer of rolf S3-S4 linker to HERG eliminates activation gating but spares inactivation. Biophys J 97: 1323-1334.
42. 2+ - Evidence for two distinct voltage sensors. J Gen Physiol 113: 565-580.
43. Perrin MJ, Kuchel PW, Campbell TJ, Vandenberg JI (2008) Drug binding to the inactivated state is necessary but not sufficient for high-affinity binding to human ether-a-go-go-related gene channels. Mol Pharmacol 74: 1443-1452.
44. Lee SY, Banerjee A, MacKinnon R (2009) Two separate interfaces between the voltage sensor and pore are required for the function of voltage-dependent K(+) channels. PLoS Biol 7: e47.
45. Subbiah RN, Clarke CE, Smith DJ, Zhao J, Campbell TJ, et al. (2004) Molecular basis of slow activation of the human ether-a-go-go related gene potassium channel. J Physiol 558: 417-431.
46. Zhang M, Liu J, Jiang M, Wu DM, Sonawane K, et al. (2005) Interactions between charged residues in the transmembrane segments of the voltagesensing domain in the hERG channel. J Membrane Biol 207: 169-181.
47. + channel with its specific BeKm-1 peptide: insights into the selectivity of molecular recognition. J Proteome Res 6: 611-620.