Selection of inhibitor-resistant viral potassium channels identifies a selectivity filter site that affects barium and amantadine block

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Chatelain, Franck C ^a   Gazzarrini, Sabrina ^b   Fujiwara, Yuichiro ^a   Arrigoni, Cristina ^b   Domigan, Courtney ^a   Ferrara, Giuseppina ^b   Pantoja, Carlos ^c   Thiel, Gerhard ^d   Moroni, Anna ^b   Minor Jr , Daniel L ^a,c,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^e LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMANTADINE; BARIUM; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL KCV; SERINE; THYMINE; UNCLASSIFIED DRUG; KCV POTASSIUM CHANNEL, CHLORELLA VIRUS; POTASSIUM; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG BINDING; DRUG SELECTIVITY; DRUG STABILITY; FILTER; MUTANT; MUTATION; NONHUMAN; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; ELECTROPHYSIOLOGY; METABOLISM; METHODOLOGY; OOCYTE; PHYSIOLOGY; PICHIA; XENOPUS LAEVIS;

MAMMALIA;

AMANTADINE; ANIMALS; BARIUM; BINDING SITES; ELECTROPHYSIOLOGY; MODELS, GENETIC; MUTATION; OOCYTES; PICHIA; POTASSIUM; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS; VIRAL PROTEINS; XENOPUS LAEVIS;

EID: 70449372669     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007496     Document Type: Article

References (65)

1. Hille B (2001) Ion Channels of Excitable Membranes. Sunderland, MA: Sinauer Associates, Inc. (Total pages 814).
2. Kaczorowski GJ, McManus OB, Priest BT, Garcia ML (2008) Ion channels as drug targets: the next GPCRs. J Gen Physiol 131: 399-405.
3. Lu Q, An WF (2008) Impact of novel screening technologies on ion channel drug discovery. Comb Chem High Throughput Screen 11: 185-194.
4. Minor DL Jr (2009) Searching for interesting channels: pairing selection and molecular evolution methods to study ion channel structure and function. Mol Biosyst 5: 802-810.
5. Bulaj G (2008) Integrating the discovery pipeline for novel compounds targeting ion channels. Curr Opin Chem Biol 12: 441-447.
6. Dunlop J, Bowlby M, Peri R, Vasilyev D, Arias R (2008) High-throughput electrophysiology: an emerging paradigm for ion-channel screening and physiology. Nat Rev Drug Discov 7: 358-368.
7. Zaks-Makhina E, Kim Y, Aizenman E, Levitan ES (2004) Novel neuroprotective K+ channel inhibitor identified by high-throughput screening in yeast. Mol Pharmacol 65: 214-219.
8. Zaks-Makhina E, Li H, Grishin A, Salvador-Recatala V, Levitan ES (2009) Specific and slow inhibition of the kir2.1 K+ channel by gambogic acid. J Biol Chem 284: 15432-15438.
9. Chatelain FC, Alagem N, Xu Q, Pancaroglu R, Reuveny E, et al. (2005) The pore helix dipole has a minor role in inward rectifier channel function. Neuron 47: 833-843.
10. Kwok TC, Hui K, Kostelecki W, Ricker N, Selman G, et al. (2008) A genetic screen for dihydropyridine (DHP)-resistant worms reveals new residues required for DHP-blockage of mammalian calcium channels. PLoS Genet 4: e1000067.
11. Kwok TC, Ricker N, Fraser R, Chan AW, Burns A, et al. (2006) A small-molecule screen in C. elegans yields a new calcium channel antagonist. Nature 441: 91-95.
12. Burns AR, Kwok TC, Howard A, Houston E, Johanson K, et al. (2006) High-throughput screening of small molecules for bioactivity and target identification in Caenorhabditis elegans. Nat Protoc 1: 1906-1914.
13. Kang M, Moroni A, Gazzarrini S, DiFrancesco D, Thiel G, et al. (2004) Small potassium ion channel proteins encoded by chlorella viruses. Proc Natl Acad Sci U S A 101: 5318-5324.
14. Shim JW, Yang M, Gu LQ (2007) In vitro synthesis, tetramerization and single channel characterization of virus-encoded potassium channel Kcv. FEBS Lett 581: 1027-1034.
15. Pagliuca C, Goetze TA, Wagner R, Thiel G, Moroni A, et al. (2007) Molecular properties of Kcv, a virus encoded K+ channel. Biochemistry 46: 1079-1090.
16. Plugge B, Gazzarrini S, Nelson M, Cerana R, Van Etten JL, et al. (2000) A potassium channel protein encoded by chlorella virus PBCV-1. Science 287: 1641-1644.
17. Syeda R, Holden MA, Hwang WL, Bayley H (2008) Screening blockers against a potassium channel with a droplet interface bilayer array. J Am Chem Soc 130: 15543-15548.
18. Pinto LH, Lamb RA (2007) Controlling influenza virus replication by inhibiting its proton channel. Mol Biosyst 3: 18-23.
19. Bichet D, Lin YF, Ibarra CA, Huang CS, Yi BA, et al. (2004) Evolving potassium channels by means of yeast selection reveals structural elements important for selectivity. Proc Natl Acad Sci U S A 101: 4441-4446.
20. Grabe M, Lai HC, Jain M, Jan YN, Jan LY (2007) Structure prediction for the down state of a potassium channel voltage sensor. Nature 445: 550-553.
21. Lai HC, Grabe M, Jan YN, Jan LY (2005) The S4 voltage sensor packs against the pore domain in the KAT1 voltage-gated potassium channel. Neuron 47: 395-406.
22. Minor DL Jr, Masseling SJ, Jan YN, Jan LY (1999) Transmembrane structure of an inwardly rectifying potassium channel. Cell 96: 879-891.
23. Yi BA, Lin YF, Jan YN, Jan LY (2001) Yeast screen for constitutively active mutant G protein-activated potassium channels. Neuron 29: 657-667.
24. Sadja R, Smadja K, Alagem N, Reuveny E (2001) Coupling Gbetagamma-dependent activation to channel opening via pore elements in inwardly rectifying potassium channels. Neuron 29: 669-680.
25. + channels in Saccharomyces cerevisiae:strategies for molecular analysis of structure and function. Soc Exper Biol. pp 85-97.
26. + channel pore. J Biol Chem 272: 1011-1018.
27. + channel in yeast. Mol Biol Cell 6: 1231-1240.
28. Balss J, Papatheodorou P, Mehmel M, Baumeister D, Hertel B, et al. (2008) Transmembrane domain length of viral K+ channels is a signal for mitochondria targeting. Proc Natl Acad Sci U S A 105: 12313-12318.
29. Stemmer WP (1994) Rapid evolution of a protein in vitro by DNA shuffling. Nature 370: 389-391.
30. Heginbotham L, Lu Z, Abramson T, MacKinnon R (1994) Mutations in the K+ channel signature sequence. Biophys J 66: 1061-1067.
31. Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R (2001) Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A resolution. Nature 414: 43-48.
32. Jiang Y, MacKinnon R (2000) The barium site in a potassium channel by x-ray crystallography. J Gen Physiol 115: 269-272.
33. Lockless SW, Zhou M, MacKinnon R (2007) Structural and thermodynamic properties of selective ion binding in a K+ channel. PLoS Biol 5: e121.
34. Abenavoli A, DiFrancesco ML, Schroeder I, Epimashko S, Gazzarrini S, et al. (2009) Fast and slow gating are inherent properties of the pore module of the K+ channel Kcv. J Gen Physiol 134: 219-229.
35. Krishnan MN, Trombley P, Moczydlowski EG (2008) Thermal stability of the K+ channel tetramer: cation interactions and the conserved threonine residue at the innermost site (S4) of the KcsA selectivity filter. Biochemistry 47: 5354-5367.
36. Krishnan MN, Bingham JP, Lee SH, Trombley P, Moczydlowski E (2005) Functional role and affinity of inorganic cations in stabilizing the tetrameric structure of the KcsA K+ channel. J Gen Physiol 126: 271-283.
37. Wang S, Alimi Y, Tong A, Nichols CG, Enkvetchakul D (2009) Differential roles of blocking ions in KirBac1.1 tetramer stability. J Biol Chem 284: 2854-2860.
38. Rath A, Glibowicka M, Nadeau VG, Chen G, Deber CM (2009) Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proc Natl Acad Sci U S A 106: 1760-1765.
39. Dornmair K, Kiefer H, Jahnig F (1990) Refolding of an integral membrane protein. OmpA of Escherichia coli. J Biol Chem 265: 18907-18911.
40. Cortes DM, Perozo E (1997) Structural dynamics of the Streptomyces lividans K+ channel (SKC1): oligomeric stoichiometry and stability. Biochemistry 36: 10343-10352.
41. Heginbotham L, Odessey E, Miller C (1997) Tetrameric stoichiometry of a prokaryotic K+ channel. Biochemistry 36: 10335-10342.
42. Hidalgo P, MacKinnon R (1995) Revealing the architecture of a K+ channel pore through mutant cycles with a peptide inhibitor. Science 268: 307-310.
43. Carter PJ, Winter G, Wilkinson AJ, Fersht AR (1984) The use of double mutants to detect structural changes in the active site of the tyrosyl-tRNA synthetase (Bacillus stearothermophilus). Cell 38: 835-840.
44. Roux B (2005) The art of dissecting the function of a potassium channel. Neuron 47: 777-778.
45. Zhou M, MacKinnon R (2004) A mutant KcsA K(+) channel with altered conduction properties and selectivity filter ion distribution. J Mol Biol 338: 839-846.
46. Stouffer AL, Acharya R, Salom D, Levine AS, Di Costanzo L, et al. (2008) Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451: 596-599.
47. Schnell JR, Chou JJ (2008) Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451: 591-595.
48. Chen J, Cassar SC, Zhang D, Gopalakrishnan M (2005) A novel potassium channel encoded by Ectocarpus siliculosus virus. Biochem Biophys Res Commun 326: 887-893.
49. Ashcroft FM, Kerr AJ, Gibson JS, Williams BA (1991) Amantadine and sparteine inhibit ATP-regulated K-currents in the insulin-secreting beta-cell line, HIT-T15. Br J Pharmacol 104: 579-584.
50. Roux B (2005) Ion conduction and selectivity in K(+) channels. Annu Rev Biophys Biomol Struct 34: 153-171.
51. Lenaeus MJ, Vamvouka M, Focia PJ, Gross A (2005) Structural basis of TEA blockade in a model potassium channel. Nat Struct Mol Biol 12: 454-459.
52. Yohannan S, Hu Y, Zhou Y (2007) Crystallographic study of the tetrabutylammonium block to the KcsA K+ channel. J Mol Biol 366: 806-814.
53. Sanguinetti MC, Tristani-Firouzi M (2006) hERG potassium channels and cardiac arrhythmia. Nature 440: 463-469.
54. Sanguinetti MC, Mitcheson JS (2005) Predicting drug-hERG channel interactions that cause acquired long QT syndrome. Trends Pharmacol Sci 26: 119-124.
55. + conduction and selectivity. Science 280: 69-77.
56. Long SB, Campbell EB, Mackinnon R (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309: 897-903.
57. Duff KC, Cudmore AJ, Bradshaw JP (1993) The location of amantadine hydrochloride and free base within phospholipid multilayers: a neutron and X-ray diffraction study. Biochim Biophys Acta 1145: 149-156.
58. Wang J, Schnell JR, Chou JJ (2004) Amantadine partition and localization in phospholipid membrane: a solution NMR study. Biochem Biophys Res Commun 324: 212-217.
59. Subczynski WK, Wojas J, Pezeshk V, Pezeshk A (1998) Partitioning and localization of spin-labeled amantadine in lipid bilayers: an EPR study. J Pharm Sci 87: 1249-1254.
60. Stemmer PC (1994) DNA shuffling by random fragmentation and reassembly: In vitro recombination for molecular evolution. Proc Natl Acad Sci USA 91: 10747-10751.
61. Sigworth FJ, Sine SM (1987) Data transformations for improved display and fitting of single-channel dwell time histograms. Biophys J 52: 1047-1054.
62. Alagem N, Yesylevskyy S, Reuveny E (2003) The pore helix is involved in stabilizing the open state of inwardly rectifying K+ channels. Biophys J 85: 300-312.
63. Woodhull AM (1973) Ionic blockage of sodium channels in nerve. J Gen Physiol 61: 687-708.
64. Guizouarn H, Gabillat N, Motais R, Borgese F (2001) Multiple transport functions of a red blood cell anion exchanger, tAE1: its role in cell volume regulation. J Physiol 535: 497-506.
65. Gazzarrini S, Kang M, Abenavoli A, Romani G, Olivari C, et al. (2009) Chlorella virus ATCV-1 encodes a functional potassium channel of 82 amino acids. Biochem J 420: 295-303.