Solution structure of GxTX-1E, a high-affinity tarantula toxin interacting with voltage sensors in Kv2.1 potassium channels

Biochemistry

Volumn 49, Issue 25, 2010, Pages 5134-5142

  Lee, Seungkyu ^a   Milescu, Mirela ^b   Jung, Hyun Ho ^a   Lee, Ju Yeon ^a   Bae, Chan Hyung ^a   Lee, Chul Won ^c   Kim, Ha Hyung ^d   Swartz, Kenton J ^b   Kim, Jae Il ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d Chung Ang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL REGIONS; HIGH AFFINITY; HYDROPHOBIC RESIDUES; MECHANISTIC STUDIES; NMR SPECTROSCOPY; POLAR RESIDUES; POTASSIUM CHANNELS; SOLUTION STRUCTURES; STRUCTURAL ARCHITECTURE; STRUCTURAL DIFFERENCES; TARGET VOLTAGE; THREE-DIMENSIONAL SOLUTIONS; VOLTAGE SENSOR;

METABOLITES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POTASSIUM; SENSORS;

TOXIC MATERIALS;

CYSTEINE; GXTX 1E; JZTX III; POTASSIUM CHANNEL; POTASSIUM CHANNEL KV2.1; SGTX1; SPIDER VENOM; TOXIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CHEMICAL STRUCTURE; CONTROLLED STUDY; MOLECULAR INTERACTION; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN MOTIF; SPIDER; TARANTULA;

AMINO ACID SEQUENCE; ANIMALS; HYDROGEN BONDING; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; SHAB POTASSIUM CHANNELS; SPIDER VENOMS; XENOPUS LAEVIS;

TARANTULA;

EID: 77953903460     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100246u     Document Type: Article

References (58)

1. + channel in a lipid membrane-like environment Nature 450, 376-382
2. Swartz, K. J. (2008) Sensing voltage across lipid membranes Nature 456, 891-897
3. + channel-blocking peptides Neuron 15, 5-10
4. Swartz, K. J. (2007) Tarantula toxins interacting with voltage sensors in potassium channels Toxicon 49, 213-230
5. Alabi, A. A., Bahamonde, M. I., Jung, H. J., Kim, J. I., and Swartz, K. J. (2007) Portability of paddle motif function and pharmacology in voltage sensors Nature 450, 370-375
6. Bosmans, F., Martin-Eauclaire, M. F., and Swartz, K. J. (2008) Deconstructing voltage sensor function and pharmacology in sodium channels Nature 456, 202-208
7. Lee, S. Y. and MacKinnon, R. (2004) A membrane-access mechanism of ion channel inhibition by voltage sensor toxins from spider venom Nature 430, 232-235
8. MacKinnon, R. (1991) Determination of the subunit stoichiometry of a voltage-activated potassium channel Nature 350, 232-235
9. MacKinnon, R., Cohen, S. L., Kuo, A., Lee, A., and Chait, B. T. (1998) Structural conservation in prokaryotic and eukaryotic potassium channels Science 280, 106-109
10. MacKinnon, R. and Miller, C. (1989) Mutant potassium channels with altered binding of charybdotoxin, a pore-blocking peptide inhibitor Science 245, 1382-1385
11. + channel complexes Proc. Natl. Acad. Sci. U.S.A. 105, 1478-1482
12. Phillips, L. R., Milescu, M., Li-Smerin, Y., Mindell, J. A., Kim, J. I., and Swartz, K. J. (2005) Voltage-sensor activation with a tarantula toxin as cargo Nature 436, 857-860
13. Frech, G. C., VanDongen, A. M., Schuster, G., Brown, A. M., and Joho, R. H. (1989) A novel potassium channel with delayed rectifier properties isolated from rat brain by expression cloning Nature 340, 642-645
14. + channels in pancreatic beta cells: Role, regulation and potential as therapeutic targets Diabetologia 46, 1046-1062
15. + channel critical to dynamic control of neuronal excitability Neurotoxicology 26, 743-752
16. Lee, H. C., Wang, J. M., and Swartz, K. J. (2003) Interaction between extracellular Hanatoxin and the resting conformation of the voltage-sensor paddle in Kv channels Neuron 40, 527-536
17. + channel J. Gen. Physiol. 115, 673-684
18. Li-Smerin, Y. and Swartz, K. J. (2001) Helical structure of the COOH terminus of S3 and its contribution to the gating modifier toxin receptor in voltage-gated ion channels J. Gen. Physiol. 117, 2 5-218
19. Liao, Z., Yuan, C., Peng, K., Xiao, Y., and Liang, S. (2007) Solution structure of Jingzhaotoxin-III, a peptide toxin inhibiting both Nav1.5 and Kv2.1 channels Toxicon 50, 135-143
20. + channel through multiple binding sites Neuron 18, 665-673
21. + channels Neuron 18, 675-682
22. Wang, J. M., Roh, S. H., Kim, S., Lee, C. W., Kim, J. I., and Swartz, K. J. (2004) Molecular surface of tarantula toxins interacting with voltage sensors in kv channels J. Gen. Physiol. 123, 455-467
23. Xiao, Y., Tang, J., Yang, Y., Wang, M., Hu, W., Xie, J., Zeng, X., and Liang, S. (2004) Jingzhaotoxin-III, a novel spider toxin inhibiting activation of voltage-gated sodium channel in rat cardiac myocytes J. Biol. Chem. 279, 26220-26226
24. Yuan, C., Yang, S., Liao, Z., and Liang, S. (2007) Effects and mechanism of Chinese tarantula toxins on the Kv2.1 potassium channels Biochem. Biophys. Res. Commun. 352, 799-804
25. Jung, H. J., Lee, J. Y., Kim, S., Eu, Y. J., Shin, S. Y., Milescu, M., Swartz, K. J., and Kim, J. I. (2005) Solution Structure and Lipid Membrane Partitioning of VSTx1, an Inhibitor of the KvAP Potassium Channel Biochemistry 44, 6015-6023
26. Milescu, M., Vobecky, J., Roh, S. H., Kim, S. H., Jung, H. J., Kim, J. I., and Swartz, K. J. (2007) Tarantula toxins interact with voltage sensors within lipid membranes J. Gen. Physiol. 130, 497-511
27. Tombola, F., Pathak, M. M., and Isacoff, E. Y. (2005) How far will you go to sense voltage? Neuron 48, 719-725
28. Swartz, K. J. and MacKinnon, R. (1995) An inhibitor of the Kv2.1 potassium channel isolated from the v nom of a Chilean tarantula Neuron 15, 941-949
29. + channels: Common surface features of gating modifier toxins J. Mol. Biol. 297, 771-780
30. + channels Proc. Natl. Acad. Sci. U.S.A. 95, 8585-8589
31. Herrington, J. (2007) Gating modifier peptides as probes of pancreatic β-cell physiology Toxicon 49, 231-238
32. Herrington, J., Zhou, Y. P., Bugianesi, R. M., Dulski, P. M., Feng, Y., Warren, V. A., Smith, M. M., Kohler, M. G., Garsky, V. M., Sanchez, M., Wagner, M., Raphaelli, K., Banerjee, P., Ahaghotu, C., Wunderler, D., Priest, B. T., Mehl, J. T., Garcia, M. L., McManus, O. B., Kaczorowski, G. J., and Slaughter, R. S. (2006) Blockers of the delayed-rectifier potassium current in pancreatic β-cells enhance glucose-dependent insulin secretion Diabetes 55, 1034-1042
33. Schmalhoefer, W. A., Ratliff, K. S., Weinglass, A. B., Kaczorowski, G. J., Garcia, M. L., and Herrington, J. (2009) A Kv2.1 gating modifier binding assay suitable for high throughput screening Channels 3, 1-11
34. Milescu, M., Bosmans, F., Lee, S., Alabi, A. A., Kim, J. I., and Swartz, K. J. (2009) Interactions between lipids and voltage sensor paddles detected with tarantula toxins Nat. Struct. Mol. Biol. 16, 1080-1085
35. Middleton, R. E., Warren, V. A., Kraus, R. L., Hwang, J. C., Liu, C. J., Dai, G., Brochu, R. M., Kohler, M. G., Gao, Y. D., Garsky, V. M., Bogusky, M. J., Mehl, J. T., Cohen, C. J., and Smith, M. M. (2002) Two tarantula peptides inhibit activation of multiple sodium channels Biochemistry 41, 14734-14747
36. Bax, A. and Davis, D. G. (1985) LEV-17-Based Two-Dimensional Homonuclear Magnetization Transfer Spectroscopy J. Magn. Reson. 65, 355-360
37. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions J. Biomol. NMR 2, 661-665
38. 1H NMR spectra of proteins via double quantum filtering Biochem. Biophys. Res. Commun. 117, 479-485
39. Goddard, T. D. and Kneller, D. G. (2004) SPARKY 3, University of California, San Francisco.
40. Guntert, P. (2004) Automated NMR structure calculation with CYANA Methods Mol. Biol. 278, 353-378
41. Herrmann, T., Guntert, P., and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA J. Mol. Biol. 319, 209-227
42. Linge, J. P., Williams, M. A., Spronk, C. A., Bonvin, A. M., and Nilges, M. (2003) Refinement of protein structures in explicit solvent Proteins 50, 496-506
43. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D54, 905-921
44. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8, 477-486
45. Hutchinson, E. G. and Thornton, J. M. (1996) PROMOTIF: A program to identify and analyze structural motifs in proteins Protein Sci. 5, 212-220
46. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures J. Mol. Graphics 14, 29-32, 5155
47. Wüthrich, K. (1986) NMR of proteins and nucleic acids, Wiley, New York.
48. Lee, C. W., Kim, S., Roh, S. H., Endoh, H., Kodera, Y., Maeda, T., Kohno, T., Wang, J. M., Swartz, K. J., and Kim, J. I. (2004) Solution Structure and Functional Characterization of SGTx1, a Modifier of Kv2.1 Channel Gating Biochemistry 43, 890-897
49. Takeuchi, K., Kim, J. I., Takahashi, H., Swartz, K., and Shimada, I. (2002) Solution structure of ω-grammotoxin SIA, a gating modifier of P/Q and N type calcium channels J. Mol. Biol. 321, 517-526
50. Sibanda, B. L., Blundell, T. L., and Thornton, J. M. (1989) Conformation of β-hairpins in protein structures. A systematic classification with applications to modeling by homology, electron density fitting and protein engineering J. Mol. Biol. 206, 759-777
51. Norton, R. S. and Pallaghy, P. K. (1998) The cystine knot structure of ion channel toxins and related polypeptides Toxicon 36, 1573-1583
52. Pallaghy, P. K., Nielsen, K. J., Craik, D. J., and Norton, R. S. (1994) A common structural motif incorporating a cystine knot and a triple-stranded β-sheet in toxic and inhibitory polypeptides Protein Sci. 3, 1833-1839
53. Richardson, J. S. (1981) The anatomy and taxonomy of protein structure Adv. Protein Chem. 34, 167-339
54. Oswald, R. E., Suchyna, T. M., McFeeters, R., Gottlieb, P., and Sachs, F. (2002) Solution structure of peptide toxins that block mechanosensitive ion channels J. Biol. Chem. 277, 34443-34450
55. Suchyna, T. M., Johnson, J. H., Hamer, K., Leykam, J. F., Gage, D. A., Clemo, H. F., Baumgarten, C. M., and Sachs, F. (2000) Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels J. Gen. Physiol. 115, 583-598
56. Suchyna, T. M., Tape, S. E., Koeppe, R. E., II, Andersen, O. S., Sachs, F., and Gottlieb, P. A. (2004) Bilayer-dependent inhibition of mechanosensitive channels by neuroactive peptide enantiomers Nature 430, 235-240
57. + channel pore through mutant cycles with a peptide inhibitor Science 268, 307-310
58. + channel selectivity filter by mutant cycle-based structure analysis Neuron 16, 131-139