Molecular determinants of interactions between the N-terminal domain and the transmembrane core that modulate hERG K+ channel gating

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Fernández Trillo, Jorge ^a   Barros, Francisco ^a   Machín, Angeles ^a   Carretero, Luis ^a   Domínguez, Pedro ^a   de la Peña, Pilar ^a  

^a UNIVERSITY OF OVIEDO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL HERG; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL STRAIN HEK293; CHANNEL GATING; CHO CELL; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE DELETION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; NONHUMAN; POINT MUTATION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL PROCESSING; TOTAL INTERNAL REFLECTION FLUORESCENCE;

ANIMALS; CELL LINE; CHO CELLS; CRICETINAE; ELECTROPHYSIOLOGY; ETHER-A-GO-GO POTASSIUM CHANNELS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY;

EID: 80052861717     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024674     Document Type: Article

References (54)

1. Sanguinetti MC, Jiang C, Curran ME, Keating MT, (1995) A mechanistic link between an inherited and an adquired cardiac arrhythmia. 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. Viskin S, (1999) Long QT syndromes and torsade de pointes. Lancet 354: 1625-1633.
4. Chiang C, Roden DM, (2000) The long QT syndromes: Genetic basis and clinical implications. J Am Coll Cardiol 36: 1-12.
5. Keating MT, Sanguinetti MC, (2001) Molecular and cellular mechanisms of cardiac arrhythmias. Cell 104: 569-580.
6. Redfern WS, Carlsson L, Davis AS, Lynch WG, MacKenzie I, et al. (2002) Relationship between preclinical cardiac electrophysiology, clinical QT interval prolongation and torsade de pointes for a broad range of drugs: evidence for a provisional safety margin in drug development. Cardiovasc Res 58: 32-45.
7. Thomas D, Zhang W, Wu K, Wimmer A-B, Gut B, et al. (2003) Regulation of potassium channel activation by protein kinase C independent of direct phosphorylation of the channel protein. Cardiovasc Res 59: 14-26.
8. Finlayson K, Witchel HJ, McCulloch J, Sharkey J, (2004) Adquired QT interval prolongation and HERG: Implications for drug discovery and development. Eur J Pharmacol 500: 129-142.
9. Roden DM, Lazzara R, Rosen M, Schwartz PJ, Towbin J, Vincent GM, (1996) Multiple mechanisms in the long-QT syndrome. Current knowledge, gaps, and future directions. Circulation 94: 1996-2012.
10. Schwartz PJ, (2005) Management of the long QT syndrome. Nat Clin Pract Cardiovasc Med 2: 346-351.
11. Sanguinetti MC, Tristani-Firouzi M, (2006) hERG potassium channels and cardiac arrhythmia. Nature 440: 463-469.
12. Wanke E, Restano-Cassulini R, (2006) Toxins interacting with ether-a-go-go-related gene voltage-dependent potassium channels. Toxicon 49: 239-248.
13. + channel: target and antitarget strategies in drug development. Pharmacol Res 57: 181-195.
14. Arcangeli A, Crociani O, Lastraioli E, Masi A, Pilozzi S, Becchetti A, (2009) Targeting ion channels in cancer: A novel frontier in antineoplastic therapy. Curr Med Chem 16: 66-93.
15. Sanguinetti MC, (2010) HERG1 channelopathies. Pflügers Arch 460: 265-276.
16. Warmke JW, Ganetzky B, (1994) A family of potassium channel genes related to eag in Drosophila and mammals. Proc Natl Acad Sci USA 91: 3438-3442.
17. Smith PL, Baukrowitz T, Yellen G, (1996) The inward rectification mechanism of the HERG cardiac potassium channel. Nature 379: 833-836.
18. + channels. J Physiol 537: 843-851.
19. Schönherr R, Heinemann SH, (1996) Molecular determinants for activation and inactivation of HERG, a human inward rectifier potassium channel. J Physiol 493: 635-642.
20. 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.
21. Morais-Cabral JH, Lee A, Cohen SL, Chait BT, Li M, MacKinnon R, (1998) Crystal structure and functional analysis of the HERG potassium channel N terminus: a eukaryotic PAS domain. Cell 95: 649-655.
22. Wang J, Trudeau MC, Zappia AM, Robertson GA, (1998) Regulation of deactivation by an amino terminal domain in Human ether-a-go-go-related gene potassium channels. J Gen Physiol 112: 637-647.
23. + channels. Biophys J 115: 749-758.
24. + channel gating. Biophys J 79: 231-246.
25. 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.
26. Ng CA, Hunter MJ, Perry MD, Mobli M, Ke Y, et al. (2011) The N-terminal tail of hERG contains an amphipathic α-helix that regulates channel deactivation. PloS ONE 6: e16191.
27. + channel deactivation gating from the solution structure of the eag domain. J Biol Chem 286: 6184-6191.
28. Li Q, Gayen S, Chen AS, Huang Q, Raida M, Kang C, (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.
29. de la Peña P, Alonso-Ron C, Machín A, Fernández-Trillo J, Carretero L, et al. (2011) Demonstration of physical proximity between the amino terminus and the S4-S5 linker of the h-ERG potassium channel. J Biol Chem 286: 19065-19075.
30. Gustina AS, Trudeau MC, (2009) A recombinant N-terminal domain fully restores deactivation gating in N-truncated and long QT syndrome mutant hERG potassium channels. Proc Natl Acad Sci USA 106: 13082-13087.
31. Gustina AS, Trudeau MC, (2011) hERG potassium channel gating is mediated by N- and C-terminal region interactions. J Gen Physiol 137: 315-325.
32. de la Peña P, Delgado LM, del Camino D, Barros F, (1992) Cloning and expression of the thyrotropin-releasing hormone receptor from GH3 rat anterior pituitary cells. Biochem J 284: 891-899.
33. + channel gating by activation of a G protein-coupled receptor and protein kinase C. J Physiol 511: 333-346.
34. Alonso-Ron C, Barros F, Manso DG, Gómez-Varela D, Miranda P, et al. (2009) Participation of HERG channel cytoplasmic structures on regulation by the G protein-coupled TRH receptor. Pflügers Arch 457: 1237-1252.
35. + channels as a reporter of the in vivo coarse architecture of the cytoplasmic domains. Biochim Biophys Acta 1783: 1681-1699.
36. Fowler CE, Aryal P, Suen KF, Slesinger PA, (2007) Evidence for association of GABAB receptors with Kir3 channels and regulators of G protein signalling (RGS4) proteins. J Physiol 580: 51-65.
37. Gómez-Varela D, Barros F, Viloria CG, Giráldez T, Manso DG, et al. (2003) Relevance of the proximal domain in the amino-terminus of HERG channels for regulation by a phospholipase C-coupled hormone receptor. FEBS Lett 535: 125-130.
38. + channels in GH3 rat anterior pituitary cells. J Physiol 566: 717-736.
39. Subbiah RN, Clarke CE, Smith DJ, Zhao JT, Campbell TJ, Vandenberg JI, (2004) Molecular basis of slow activation of the human ether-á-go-go related gene potassium channel. J Physiol 558: 417-431.
40. 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.
41. + channel. J Biol Chem 281: 12858-12864.
42. Liu J, Zhang M, Jiang M, Tseng G-N, (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.
43. + channels. J Membrane Biol 187: 117-133.
44. Chen J, Zou A, Splawski I, Keating MT, Sanguinetti MC, (1999) Long QT syndrome-associated mutations in the Per-Arnt-sim (PAS) domain of HERG potassium channels accelerate deactivation. J Biol Chem 274: 10113-10118.
45. Sanguinetti MC, Xu QP, (1999) Mutations of the S4-S5 linker alter activation properties of HERG potassium channels expressed in Xenopus oocytes. J Physiol 514: 667-675.
46. + channels. Biophys J 99: 2841-2852.
47. Axelrod D, (2003) Total internal reflection fluorescence microscopy in cell biology. Meth Enzymol 361: 1-33.
48. Selvin PR, (1995) Fluorescence resonance energy transfer. Meth Enzymol 246: 300-334.
49. Uversky VN, Dunker AK, (2010) Understanding protein non-folding. Biochim Biophys Acta 1804: 1231-1264.
50. Chouard T, (2011) Breaking the protein rules. Nature 471: 151-153.
51. + channels. Science 289: 123-127.
52. + channel. Biochemistry 39: 10347-10352.
53. Wissmann R, Bildl W, Oliver D, Beyermann M, Kalbitzer H, et al. (2003) Solution structure and function of the "tandem inactivation domain" of the neuronal A-type potassium channel Kv1.4. J Biol Chem 278: 16142-16150.
54. Zagotta WN, Olivier NB, Black KD, Young EC, Olson R, Gouaux E, (2003) Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 425: 200-205.