An NMR investigation of the structure, function and role of the hERG channel selectivity filter in the long QT syndrome

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 6, 2013, Pages 1494-1502

  Gravel, Andrée E ^a   Arnold, Alexandre A ^a   Dufourc, Erick J ^b   Marcotte, Isabelle ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Cardiotoxic drugs; Human ether a go go related gene; Lipid bicelle; Multilamellar vesicle; Nuclear magnetic resonance; Phosphatidylcholine model membrane

Indexed keywords

BEPRIDIL; CETIRIZINE; DIPHENHYDRAMINE; FLUVOXAMINE; POTASSIUM CHANNEL HERG; POTASSIUM ION; PROMETHAZINE;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DRUG PROTEIN BINDING; HEART MUSCLE FIBER MEMBRANE POTENTIAL; HYDROPHOBICITY; LONG QT SYNDROME; MEMBRANE CHANNEL; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTON NUCLEAR MAGNETIC RESONANCE; SOLID STATE; STRUCTURE ACTIVITY RELATION;

BEPRIDIL; CETIRIZINE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIPHENHYDRAMINE; ETHER-A-GO-GO POTASSIUM CHANNELS; FLUVOXAMINE; HUMANS; ION CHANNEL GATING; LONG QT SYNDROME; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANES, ARTIFICIAL; PHOSPHATIDYLCHOLINES; POTASSIUM; PROMETHAZINE; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84875078496     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.02.012     Document Type: Article

References (76)

1. M.C. Sanguinetti, and M. Tristani-Firouzi hERG potassium channels and cardiac arrhythmia Nature 440 2006 463 469
2. R.R. Shah Drug-induced QT interval prolongation - regulatory guidance and perspectives on hERG channel studies D.J. Chadwick, J. Goode, The hERG Cardiac Potassium Channel: Structure, Function, and Long QT Syndrome 2005 John Wiley & Sons Ltd Chichester 251 285
3. P.K. Mason, and J.P. Mounsey Drug-induced long QT syndrome: molecular mechanisms for congenital and acquired QT prolongation Drug Discov. Today 4 2007 159 163
4. S.Y. Noskov, S. Berneche, and B. Roux Control of ion selectivity in potassium channels by electrostatic and dynamic properties of carbonyl ligands Nature 431 2004 830 834
5. D.A. Doyle, J.M. Cabral, R.A. Pfuetzner, A. Kuo, J.M. Gulbis, S.L. Cohen, B.T. Chait, and R. MacKinnon The structure of the potassium channel: molecular basis of K1 conduction and selectivity Science 280 1998 69 77
6. J.H. Morais Cabral, A. Lee, S.L. Cohen, B.T. Chait, M. Li, and R. Mackinnon Crystal structure and functional analysis of the HERG potassium channel N terminus: a eukaryotic PAS domain Cell 95 1998 649 655
7. + channels J. Gen. Physiol. 115 2000 749 758
8. M. Zhang, J. Liu, and G.-N. Tseng Gating charges in the activation and inactivation processes of the hERG channel J. Gen. Physiol. 124 2004 703 718
9. M. Jiang, M. Zhang, I.V. Maslennikov, J. Liu, D.-M. Wu, Y.V. Korolkova, A.S. Arseniev, E.V. Grishin, and G.-N. Tseng Dynamic conformational changes of extracellular S5-P linkers in the hERG channel J. Physiol. 569 2005 75 89
10. G.-N. Tseng, K.D. Sonawane, Y.V. Korolkova, M. Zhang, J. Liu, E.V. Grishin, and H.R. Guy Probing the outer mouth structure of the hERG channel with peptide toxin footprinting and molecular modeling Biophys. J. 92 2007 3524 3540
11. É. Chartrand, A.A. Arnold, A. Gravel, S. Jenna, and I. Marcotte Potential role of the membrane in hERG channel functioning and drug-induced long QT syndrome Biochim. Biophys. Acta 1798 2010 1651 1662
12. + channel structure and function from NMR studies Eur. Biophys. J. 42 2012 71 79
13. L. Pardo-Lopez, M. Zhang, J. Liu, M. Jiang, L.D. Possani, and G.-N. Tseng Mapping the binding site of a human ether-a-gogo-related gene-specific peptide toxin (ErgTx) to the channel's outer vestibule J. Biol. Chem. 277 2002 16403 16411
14. + channel-Fab complex at 2.0 Å resolution Nature 414 2001 43 48
15. L. Guidoni, and P. Carloni Potassium permeation through the KcsA channel: a density functional study Biochim. Biophys. Acta 1563 2002 1 6
16. + channel in a bilayer membrane Biophys. J. 78 2000 2900 2917
17. + channel Biophys. J. 82 2002 772 780
18. M.S.P. Sansom, I.H. Shrivastava, J.N. Bright, J. Tate, C.E. Capener, and P.C. Biggin Potassium channels: structures, models, simulations Biochim. Biophys. Acta 1565 2002 294 307
19. + ions in a K channel selectivity filter: a simulation study Biophys. J. 83 2002 633 645
20. C. Domene, M.L. Klein, D. Branduardi, F.L. Gervasio, and M. Parrinello Conformational changes and gating at the selectivity filter of potassium channels J. Am. Chem. Soc. 130 2008 9474 9480
21. G.V. Miloshevsky, and P.C. Jordan Conformational changes in the selectivity filter of the open-state KcsA channel: an energy minimization study Biophys. J. 95 2008 3239 3251
22. + channels J. Biol. Chem. 277 2002 18994 19000
23. + channel S5P extracellular linker J. Biol. Chem. 278 2003 42136 42148
24. Q. Li, S. Gayen, A.S. Chen, Q. Huang, M. Raida, and C. Kang NMR solution structure of the N-terminal domain of hERG and its interaction with the S4-S5 linker Biochem. Biophys. Res. Commun. 403 2010 126 132
25. S. Gayen, Q. Li, and C. Kang The solution structure of the S4-S5 linker of the hERG potassium channel J. Pept. Sci. 18 2012 140 145
26. + channels Biochemistry 51 2012 3982 3992
27. J. Liu, M. Jiang, and G.-N. Tseng Structural and functional role of the extracellular S5-P linker in the HERG potassium channel J. Gen. Physiol. 120 2002 723 737
28. A.M. Aronov Predictive in silico modeling for hERG channel blockers DDT 10 2005 149 155
29. K. Kamiya, R. Niwa, J.S. Mitcheson, and M.C. Sanguinetti Molecular determinants of hERG channel block Mol. Pharmacol. 69 2006 1709 1716
30. A. Gill, S.F. Flaim, B.P. Damiano, S.P. Sit, and M.D. Brannan Pharmacology of bepridil Am. J. Cardiol. 69 1992 11D 16D
31. E.N. Prystowsky Effects of bepridil on cardiac electrophysiologic properties Am. J. Cardiol. 69 1992 63D 67D
32. J.D. Gilbert, S.A. Cahill, D.G. McCartney, A. Lukas, and G.J. Gross Predictors of torsades de pointes in rabbit ventricles perfused with sedating and nonsedating histamine H1-receptor antagonists Can. J. Physiol. Pharmacol. 78 2000 407 414
33. W. Zareba, A.J. Moss, S.Z. Rosero, R. Hajj-Ali, J. Konecki, and M. Andrews Electrocardiographic findings in patients with diphenhydramine overdose Am. J. Cardiol. 80 1997 1168 1173
34. J.S. Mitcheson, J. Chen, M. Lin, C. Culberson, and M.C. Sanguinetti A structural basis for drug-induced long QT syndrome Proc. Natl. Acad. Sci. U. S. A. 97 2000 12329 12333
35. J.T. Milnes, O. Crociani, A. Arcangeli, J.C. Hancox, and H.J. Witchel Blockade of HERG potassium currents by floxamine: incomplete attenuation by S6 mutations F656 or Y652 Br. J. Pharmacol. 139 2003 887 898
36. L. Pardo-Lopez, J. García-Valdez, G.B. Gurrola, G.A. Robertson, and L.D. Possani Mapping the receptor site for ergotoxin, a specific blocker of ERG channels FEBS Lett. 510 2002 45 49
37. +-ATPase activity Mol. Pharmacol. 44 1993 129 141
38. D.H. Wu, A.D. Chen, and C.S. Johnson An improved diffusion-ordered spectroscopy experiment incorporating bipolar-gradient pulses J. Magn. Reson. A115 1995 260 264
39. A.S. Altieri, D.P. Hinton, and R.A. Byrd Association of biomolecular systems via pulsed field gradient NMR self-diffusion measurements J. Am. Chem. Soc. 117 1995 7566 7567
40. J. Wang, J.R. Schnell, and J.J. Chou Amantadine partition and localization in phospholipid membrane: a solution NMR study Biochem. Biophys. Res. Commun. 324 2004 212 217
41. M. Mayer, and B. Meyer Characterization of ligand binding by saturation transfer difference NMR spectroscopy Angew. Chem. Int. Ed. 38 1999 1784 1788
42. A. Bax, and D.G. Davis MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy J. Magn. Reson. 65 1985 355 360
43. M. Rance, and R.A. Byrd Obtaining high-fidelity spin-1/2 powder spectra in anisotropic media: phase-cycled Hahn echo spectroscopy J. Magn. Reson. 52 1983 221 240
44. J.H. Davis, K.R. Jeffrey, M. Bloom, M.I. Valic, and T.P. Higgs Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains Chem. Phys. Lett. 42 1976 390 394
45. J.D. van Beek matNMR: A flexible toolbox for processing, analyzing and visualizing magnetic resonance data in Matlab® J. Magn. Reson. 187 2007 19 26
46. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
47. B.A. Johnson, and R.A. Blevins NMRView: a computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
48. + channel. A model for bad behavior J. Med. Chem. 46 2003 2017 2022
49. + channel using docking and molecular dynamics methods FEBS Lett. 579 2005 2939 2944
50. + channel: application to ligand binding Bioorg. Med. Chem. Lett. 15 2005 1737 1741
51. J.A. Post, A.J. Verkleij, and G.A. Langer Organization and function of sarcolemmal phospholipids in control and ischemic/reperfused cardiomyocytes J. Mol. Cell. Cardiol. 27 1995 749 760
52. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes Biochim. Biophys. Acta 515 1978 105 140
53. J. Seelig Deuterium magnetic resonance: theory and application to lipid membranes Q. Rev. Biophys. 10 1977 353 418
54. 2H-NMR Biochim. Biophys. Acta 737 1983 117 171
55. 31P-NMR lineshapes Biochim. Biophys. Acta 603 1980 63 69
56. H. Binder, and O. Zschörnig The effect of metal cations on the phase behavior and hydration characteristics of phospholipid membranes Chem. Phys. Lipids 115 2002 39 61
57. A.A. Gurtovenko, and I. Vattulainen Effect of NaCl and KCl on phosphatidylcholine and phosphatidylethanolamine lipid membranes: insight from atomic-scale simulations for understanding salt-induced effects in the plasma membrane J. Phys. Chem. B 112 2008 1953 1962
58. + distributions in the headgroup region of binary membranes of phosphatidylcholine and phosphatidylserine as seen by deuterium NMR Biochemistry 29 1990 7077 7089
59. J. Lind, A. Graslund, and L. Maler Membrane interactions of dynorphins Biochemistry 45 2006 15931 15940
60. U.M. Joshi, P.R.S. Kodavanti, B. Coudert, T.M. Dwyer, and H.M. Mehendale Types of interaction of amphiphilic drugs with phospholipid vesicles J. Pharmacol. Exp. Ther. 246 1988 150 157
61. J.S. Mitcheson Drug binding to hERG channels: evidence for a 'non-aromatic' binding site for fluvoxamine Br. J. Pharmacol. 139 2003 883 884
62. + channel Pharmacol. Res. 60 2009 429 437
63. 31P-NMR study J. Chem. Phys. 98 1993 1712 1720
64. 2H-NMR Biochim. Biophys. Acta 778 1984 435 442
65. S. Bernèche, and B. Roux A gate in the selectivity filter of potassium channels Structure 13 2005 591 600
66. + channel J. Mol. Biol. 366 2007 806 814
67. + channel: models and simulations of Kir6.2 mutants Biophys. J. 84 2003 2345 2356
68. R.L. Woosley Cardiac actions of antihistamines Annu. Rev. Pharmacol. Toxicol. 36 1996 233 252
69. + channel block-related cardiotoxicity by the H1 receptor blocker cetirizine compared with other second-generation antihistamines Mol. Pharmacol. 54 1998 113 121
70. P. Hoffmann, and B. Warner Are hERG channel inhibition and QT interval prolongation all there is in drug-induced torsadogenesis? A review of emerging trends J. Pharmacol. Toxicol. Methods 53 2006 87 105
71. G.P. van Balen, G. Caron, G. Ermondi, A. Pagliara, T. Grandi, G. Bouchard, R. Fruttero, P.A. Carrupt, and B. Testa Lipophilicity behaviour of the zwitterionic antihistamine cetirizine in phosphatidylcholine liposomes/water systems Pharm. Res. 18 2001 694 701
72. 1H NMR investigation of the conformation of methionine-enkephalin in fast-tumbling bicelles Biophys. J. 86 2004 1587 1600
73. D.E. Warschawski, A.A. Arnold, M. Beaugrand, A. Gravel, É. Chartrand, and I. Marcotte Choosing membrane mimetics for NMR structural studies of transmembrane proteins Biochim. Biophys. Acta 1808 2011 1957 1974
74. D.S. Cafiso Dipole potentials and spontaneous curvature: membrane properties that could mediate anesthesia Toxicol. Lett. 100-101 1998 431 439
75. O.G. Mouritsen, and K. Jorgensen A new look at lipid-membrane structure in relation to drug research Pharm. Res. 15 1998 1507 1519
76. + channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane Proc. Natl. Acad. Sci. U. S. A. 105 2008 19276 19281