The S4-S5 linker acts as a signal integrator for hERG K + channel activation and deactivation gating

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Ng, Chai Ann ^a,b,c   Perry, Matthew D ^a   Tan, Peter S ^a   Hill, Adam P ^a,c   Kuchel, Philip W ^b,d   Vandenberg, Jamie I ^a,b,c  

^a VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ETHER A GO GO RELATED CHANNEL POTASSIUM; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; POTASSIUM CHANNEL HERG;

ANIMAL CELL; ARTICLE; BINDING SITE; CHANNEL GATING; CONTROLLED STUDY; MOLECULAR MODEL; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; STEADY STATE; STRUCTURE ANALYSIS; TRANSPORT KINETICS; CHEMISTRY; HUMAN; KINETICS; MUTATION; PROTEIN CONFORMATION;

ETHER-A-GO-GO POTASSIUM CHANNELS; HUMANS; ION CHANNEL GATING; KINETICS; MUTATION; PROTEIN CONFORMATION;

EID: 84857127272     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031640     Document Type: Article

References (50)

1. 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.
2. 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.
3. Sanguinetti MC, Tristani-Firouzi M, (2006) hERG potassium channels and cardiac arrhythmia. Nature 440: 463-469.
4. Spector PS, Curran ME, Zou A, Keating MT, Sanguinetti MC, (1996) Fast inactivation causes rectification of the IKr channel. J Gen Physiol 107: 611-619.
5. Smith PL, Baukrowitz T, Yellen G, (1996) The inward rectification mechanism of the HERG cardiac potassium channel. Nature 379: 833-836.
6. Lu Y, Mahaut-Smith MP, Varghese A, Huang CL, Kemp PR, et al. (2001) Effects of premature stimulation on HERG K(+) channels. J Physiol (Lond) 537: 843-851.
7. Curran ME, Splawski I, Timothy KW, Vincent GM, Green ED, et al. (1995) A molecular basis for cardiac arrhythmia: HERG mutations cause long QT syndrome. Cell 80: 795-803.
8. Long S, Campbell E, MacKinnon R, (2005) Voltage sensor of Kv1. 2: structural basis of electromechanical coupling. Science 309: 903-908.
9. 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 (Lond) 558: 417-431.
10. Piper D, (2005) Regional Specificity of Human ether-a'-go-go-related Gene Channel Activation and Inactivation Gating. J Biol Chem 280: 7206-7217.
11. 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.
12. Tristani-Firouzi M, Chen J, Sanguinetti MC, (2002) Interactions between S4-S5 linker and S6 transmembrane domain modulate gating on HERG K+ channels. J Biol Chem 277: 18994-19000.
13. Sanguinetti MC, Xu QP, (1999) Mutations of the S4-S5 linker alter activation properties of HERG potassium channels expressed in Xenopus oocytes. J Physiol (Lond) 514: 667-675.
14. Wynia-Smith S, Gillian-Daniel A, Satyshur K, Robertson G, (2008) hERG Gating Microdomains Defined by S6 Mutagenesis and Molecular Modeling. J Gen Physiol 132: 507-520.
15. Al-Owais M, Bracey K, Wray D, (2009) Role of intracellular domains in the function of the herg potassium channel. Eur Biophys J 38: 569-576.
16. Wang J, Myers C, Robertson G, (2000) Dynamic control of deactivation gating by a soluble amino-terminal domain in HERG K+ channels. J Gen Physiol 115: 749-758.
17. Wang J, Trudeau MC, Zappia AM, Robertson GA, (1998) Regulation of deactivation by an amino terminal domain in human ether-à-go-go-related gene potassium channels. J Gen Physiol 112: 637-647.
18. Morais Cabral JH, Lee A, Cohen S, Chait B, Li M, et al. (1998) Crystal structure and functional analysis of the HERG potassium channel N terminus: a eukaryotic PAS domain. Cell 95: 649-655.
19. Schonherr R, Heinemann S, (1996) Molecular determinants for activation and inactivation of HERG, a human inward rectifier potassium channel. J Physiol (Lond).
20. Ng CA, Hunter MJ, Perry MD, Mobli M, Ke Y, et al. (2011) The N-terminal tail of hERG contains an amphipathic alpha-helix that regulates channel deactivation. PLoS ONE 6: e16191.
21. Muskett FW, Thouta S, Thomson SJ, Bowen A, Stansfeld PJ, et al. (2011) Mechanistic insight into human ether-a-go-go-related gene (hERG) K+ channel deactivation gating from the solution structure of the EAG domain. J Biol Chem 286: 6184-6191.
22. Gustina AS, Trudeau MC, (2011) hERG potassium channel gating is mediated by N- and C-terminal region interactions. J Gen Physiol 137: 315-325.
23. Alonso-Ron C, de la Peña P, Miranda P, Domínguez P, Barros F, (2008) Thermodynamic and kinetic properties of amino-terminal and S4-S5 loop HERG channel mutants under steady-state conditions. Biophys J 94: 3893-3911.
24. Ferrer T, Rupp J, Piper DR, Tristani-Firouzi M, (2006) The S4-S5 Linker Directly Couples Voltage Sensor Movement to the Activation Gate in the Human Ether-a-go-go-related Gene (hERG) K+ Channel. J Biol Chem 281: 12858-12864.
25. Van Slyke AC, Rezazadeh S, Snopkowski M, Shi P, Allard CR, et al. (2010) Mutations within the S4-S5 linker alter voltage sensor constraints in hERG K+ channels. Biophys J 99: 2841-2852.
26. Wüthrich K, (1986) NMR of proteins and nucleic acids Wiley-Interscience, New York pp. 117-176.
27. Bax A, Davis DG, (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. Journal of Magnetic Resonance pp. 355-360.
28. Kumar A, Ernst RR, Wüthrich K, (1980) A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem Biophys Res Commun 95.
29. Shaka AJ, Shykind DN, Chingas GC, Pines A, (1988) Multiple pulse sequences for precise transmitter phase alignment. J Magn Res pp. 96-111.
30. Bartels C, Xia TH, Billeter M, Guntert P, Wuthrich K, (1995) The Program Xeasy for Computer-Supported Nmr Spectral-Analysis of Biological Macromolecules. J Biomol NMR 6: 1-10.
31. Güntert P, (2004) Automated NMR structure calculation with CYANA Methods in Molecular Biology pp. 353-378.
32. Case D, Darden T, Cheatham I, Simmerling C, Wang J, et al. (2010) AMBER 11 University of California, San Francisco.
33. Bhattacharya A, Tejero R, Montelione GT, (2007) Evaluating protein structures determined by structural genomics consortia. Proteins 66: 778-795.
34. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
35. Guex N, Peitsch MC, (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis pp. 2714-2723.
36. 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: 376-382.
37. Perry M, Sachse FB, Sanguinetti MC, (2007) Structural basis of action for a human ether-a-go-go-related gene 1 potassium channel activator. Proc Natl Acad Sci U S A 104: 13827-13832.
38. 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 (Lond) 573: 291-304.
39. Almers W, (1978) Gating currents and charge movements in excitable membranes. Reviews of physiology, biochemistry and pharmacology 82: 96-190.
40. Wang S, Liu S, Morales MJ, Strauss HC, Rasmusson RL, (1997) A quantitative analysis of the activation and inactivation kinetics of HERG expressed in Xenopus oocytes. J Physiol (Lond) 502 (Pt 1): 45-60.
41. Long S, Campbell E, MacKinnon R, (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309: 897-903.
42. Ju P, Pages G, Riek RP, Chen PC, Torres AM, et al. (2009) The pore domain outer helix contributes to both activation and inactivation of the HERG K+ channel. J Biol Chem 284: 1000-1008.
43. Gayen S, Li Q, Kang C, (2011) The solution structure of the S4-S5 linker of the hERG potassium channel. J Pept Sci.
44. McCormack K, Tanouye MA, Iverson LE, Lin JW, Ramaswami M, et al. (1991) A role for hydrophobic residues in the voltage-dependent gating of Shaker K+ channels. Proc Natl Acad Sci U S A 88: 2931-2935.
45. Piper D, Varghese A, Sanguinetti M, Tristani-Firouzi M, (2003) Gating currents associated with intramembrane charge displacement in HERG potassium channels. Proc Natl Acad Sci U S A 100: 10534-10539.
46. Zou A, Curran ME, Keating MT, Sanguinetti MC, (1997) Single HERG delayed rectifier K+ channels expressed in Xenopus oocytes. Am J Physiol 272: H1309-1314.
47. de la Pena P, Alonso-Ron C, Machin A, Fernandez-Trillo J, Carretero L, et al. (2011) Demonstration of Physical Proximity between the N Terminus and the S4-S5 Linker of the Human ether-a-go-go-related Gene (hERG) Potassium Channel. J Biol Chem 286: 19065-19075.
48. Li Q, Gayen S, Chen AS, Huang Q, Raida M, et al. (2010) NMR solution structure of the N-terminal domain of hERG and its interaction with the S4-S5 linker. Biochem Biophys Res Commun 403: 126-132.
49. Saenen JB, Labro AJ, Raes A, Snyders DJ, (2006) Modulation of HERG gating by a charge cluster in the N-terminal proximal domain. Biophys J 91: 4381-4391.
50. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041.