Tarantula toxins use common surfaces for interacting with Kv and ASIC ion channels

eLife

Volumn 4, Issue MAY, 2015, Pages

  Gupta, Kanchan ^a,b   Zamanian, Maryam ^a,b   Bae, Chanhyung ^a,b,d   Milescu, Mirela ^a,b,e   Krepkiy, Dmitriy ^a,b   Tilley, Drew C ^c   Sack, Jon T ^c   Yarov Yarovoy, Vladimir ^c   Kim, Jae Il ^d   Swartz, Kenton J ^a,b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

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

^c UNIVERSITY OF CALIFORNIA   (United States)

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

^e UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 1A; GUANGXITOXIN; KV2.1 POTASSIUM CHANNEL; PSALMOTOXIN; SPIDER VENOM; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; ACID SENSING ION CHANNEL BLOCKING AGENT; ARTHROPOD PROTEIN; ASIC1 PROTEIN, HUMAN; GXTX-1E, PLESIOPHRICTUS GUANGXIENSIS; HYBRID PROTEIN; KCNB1 PROTEIN, HUMAN; LIPOSOME; NEUROTOXIN; PCTX1 PROTEIN, PSALMOPOEUS CAMBRIDGEI; PEPTIDE; PROTEIN BINDING; SHAB POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOPHYSICS; CHIMERA; ELECTROPHYSIOLOGY; FLUORESCENCE SPECTROSCOPY; LIPID MEMBRANE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; OOCYTE; PEPTIDE SYNTHESIS; POLYMERASE CHAIN REACTION; PROTEIN BINDING; PROTEIN INTERACTION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SOLID PHASE SYNTHESIS; SURFACE AREA; TARANTULA; TOXIN STRUCTURE; X RAY ANALYSIS; XENOPUS LAEVIS; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; CHANNEL GATING; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; KINETICS; METABOLISM; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; SEQUENCE HOMOLOGY; SPIDER; SYNTHESIS;

ACID SENSING ION CHANNEL BLOCKERS; ACID SENSING ION CHANNELS; AMINO ACID SEQUENCE; ANIMALS; ARTHROPOD PROTEINS; GENE EXPRESSION; ION CHANNEL GATING; KINETICS; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; NEUROTOXINS; OOCYTES; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SHAB POTASSIUM CHANNELS; SPIDER VENOMS; SPIDERS; UNILAMELLAR LIPOSOMES; XENOPUS LAEVIS;

EID: 84930678031     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06774     Document Type: Article

References (73)

1. Alabi AA, Bahamonde MI, Jung HJ, Kim JI, Swartz KJ. 2007. Portability of paddle motif function and pharmacology in voltage sensors. Nature 450:370-375. doi: 10.1038/nature06266.
2. Axelrod D, Wang MD. 1994. Reduction-of-dimensionality kinetics at reaction-limited cell surface receptors. Biophysical Journal 66:588-600. doi: 10.1016/S0006-3495(94)80834-3.
3. Baconguis I, Bohlen CJ, Goehring A, Julius D, Gouaux E. 2014. X-ray structure of acid-sensing ion channel 1-snake toxin complex reveals open state of a Na(+)-selective channel. Cell 156:717-729. doi: 10.1016/j.cell.2014.01.011.
4. Baconguis I, Gouaux E. 2012. Structural plasticity and dynamic selectivity of acid-sensing ion channel-spider toxin complexes. Nature 489:400-405. doi: 10.1038/nature11375.
5. Banerjee A, Lee A, Campbell E, Mackinnon R. 2013. Structure of a pore-blocking toxin in complex with a eukaryotic voltage-dependent K(+) channel. eLife 2:e00594. doi: 10.7554/eLife.00594.
6. Ben-Tal N, Honig B, Miller C, McLaughlin S. 1997. Electrostatic binding of proteins to membranes. Theoretical predictions and experimental results with charybdotoxin and phospholipid vesicles. Biophysical Journal 73: 1717-1727. doi: 10.1016/S0006-3495(97)78203-1.
7. Bohlen CJ, Chesler AT, Sharif-Naeini R, Medzihradszky KF, Zhou S, King D, Sánchez EE, Burlingame AL, Basbaum AI, Julius D. 2011. A heteromeric Texas coral snake toxin targets acid-sensing ion channels to produce pain. Nature 479:410-414. doi: 10.1038/nature10607.
8. Bohlen CJ, Priel A, Zhou S, King D, Siemens J, Julius D. 2010. A bivalent tarantula toxin activates the capsaicin receptor, TRPV1, by targeting the outer pore domain. Cell 141:834-845. doi: 10.1016/j.cell.2010.03.052.
9. Bosmans F, Martin-Eauclaire MF, Swartz KJ. 2008. Deconstructing voltage sensor function and pharmacology in sodium channels. Nature 456:202-208. doi: 10.1038/nature07473.
10. Bosmans F, Milescu M, Swartz KJ. 2011a. Palmitoylation influences the function and pharmacology of sodium channels. Proceedings of the National Academy of Sciences of USA 108:20213-20218. doi: 10.1073/pnas.1108497108.
11. Bosmans F, Puopolo M, Martin-Eauclaire MF, Bean BP, Swartz KJ. 2011b. Functional properties and toxin pharmacology of a dorsal root ganglion sodium channel viewed through its voltage sensors. The Journal of General Physiology 138:59-72. doi: 10.1085/jgp.201110614.
12. Bradley P, Misura KM, Baker D. 2005. Toward high-resolution de novo structure prediction for small proteins. Science 309:1868-1871. doi: 10.1126/science.1113801.
13. Campos FV, Chanda B, Beirão PS, Bezanilla F. 2007. beta-Scorpion toxin modifies gating transitions in all four voltage sensors of the sodium channel. The Journal of General Physiology 130:257-268. doi: 10.1085/jgp. 200609719.
14. Campos FV, Chanda B, Beirão PS, Bezanilla F. 2008. Alpha-scorpion toxin impairs a conformational change that leads to fast inactivation of muscle sodium channels. The Journal of General Physiology 132:251-263. doi: 10. 1085/jgp.200809995.
15. Cestè le S, Qu Y, Rogers JC, Rochat H, Scheuer T, Catterall WA. 1998. Voltage sensor-trapping: enhanced activation of sodium channels by beta- scorpion toxin bound to the S3-S4 loop in domain II. Neuron 21:919-931. doi: 10.1016/S0896-6273(00)80606-6.
16. Chen X, Kalbacher H, Gründer S. 2005. The tarantula toxin psalmotoxin 1 inhibits acid-sensing ion channel (ASIC) 1a by increasing its apparent H+ affinity. The Journal of General Physiology 126:71-79. doi: 10.1085/jgp. 200509303.
17. Chen X, Kalbacher H, Gründer S. 2006. Interaction of acid-sensing ion channel (ASIC) 1 with the tarantula toxin psalmotoxin 1 is state dependent. The Journal of General Physiology 127:267-276. doi: 10.1085/jgp.200509409.
18. Conway P, Tyka MD, DiMaio F, Konerding DE, Baker D. 2014. Relaxation of backbone bond geometry improves protein energy landscape modeling. Protein Science 23:47-55. doi: 10.1002/pro.2389.
19. Dawson RJ, Benz J, Stohler P, Tetaz T, Joseph C, Huber S, Schmid G, Hügin D, Pflimlin P, Trube G, Rudolph MG Hennig M, Ruf A. 2012. Structure of the acid-sensing ion channel 1 in complex with the gating modifier Psalmotoxin 1. Nature Communications 3:936. doi: 10.1038/ncomms1917.
20. Escoubas P, Bernard C, Lambeau G, Lazdunski M, Darbon H. 2003. Recombinant production and solution structure of PcTx1, the specific peptide inhibitor of ASIC1a proton-gated cation channels. Protein Science 12:1332-1343. doi: 10.1110/ps.0307003. Escoubas P, De Weille JR, Lecoq A, Diochot S, Waldmann R, Champigny G, Moinier D, Ménez A, Lazdunski M. c2000. Isolation of a tarantula toxin specific for a class of proton-gated Na+ channels. The Journal of Biological Chemistry 275:25116-25121. doi: 10.1074/jbc.M003643200.
21. Gill SC, von Hippel PH. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Analytical Biochemistry 182:319-326. doi: 10.1016/0003-2697(89)90602-7.
22. Gray JJ, Moughon S, Wang C, Schueler-Furman O, Kuhlman B, Rohl CA, Baker D. 2003. Protein-protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations. Journal of Molecular Biology 331:281-299. doi: 10.1016/S0022-2836(03)00670-3.
23. Herrington J, Zhou YP, Bugianesi RM, Dulski PM, Feng Y,Warren VA, Smith MM, Kohler MG, Garsky VM, Sanchez M, Wagner M, Raphaelli K, Banerjee P, Ahaghotu C, Wunderler D, Priest BT, Mehl JT, Garcia ML, McManus OB Kaczorowski GJ, Slaughter RS. 2006. Blockers of the delayed-rectifier potassium current in pancreatic beta-cells enhance glucose-dependent insulin secretion. Diabetes 55:1034-1042. doi: 10.2337/diabetes.55.04.06.db05-0788.
24. Hessa T, Kim H, Bihlmaier K, Lundin C, Boekel J, Andersson H, Nilsson I, White SH, von Heijne G. 2005. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377-381. doi: 10.1038/nature03216.
25. Jones S. 2012. Computational and structural characterisation of protein associations. Advances in Experimental Medicine and Biology 747:42-54. doi: 10.1007/978-1-4614-3229-6_3.
26. Jung HH, Jung HJ, Milescu M, Lee CW, Lee S, Lee JY, Eu YJ, Kim HH, Swartz KJ, Kim JI. 2010. Structure and orientation of a voltage-sensor toxin in lipid membranes. Biophysical Journal 99:638-646. doi: 10.1016/j.bpj. 2010.04.061.
27. Jung HJ, Lee JY, Kim SH, Eu YJ, Shin SY, Milescu M, Swartz KJ, Kim JI. 2005. Solution structure and lipid membrane partitioning of VSTx1, an inhibitor of the KvAP potassium channel. Biochemistry 44:6015-6023. doi: 10.1021/ bi0477034.
28. Kalia J, Swartz KJ. 2013. Exploring structure-function relationships between TRP and Kv channels. Scientific Reports 3:1523. doi: 10.1038/srep01523.
29. Kortemme T, Baker D. 2002. A simple physical model for binding energy hot spots in protein-protein complexes. Proceedings of the National Academy of Sciences of USA 99:14116-14121. doi: 10.1073/pnas.202485799.
30. Kortemme T, Kim DE, Baker D. 2004. Computational alanine scanning of protein-protein interfaces. Science's STKE 2004:pl2. doi: 10.1126/stke.2192004pl2.
31. Ladokhin AS. 1997. Distribution analysis of depth-dependent fluorescence quenching in membranes: a practical guide. Methods in Enzymology 278:462-473. doi: 10.1016/S0076-6879(97)78024-8.
32. Ladokhin AS. 1999. Analysis of protein and peptide penetration into membranes by depth-dependent fluorescence quenching: theoretical considerations. Biophysical Journal 76:946-955. doi: 10.1016/S0006-3495 (99)77258-9.
33. Ladokhin AS. 2014. Measuring membrane penetration with depth-dependent fluorescence quenching: distribution analysis is coming of age. Biochimica Et Biophysica Acta 1838:2289-2295. doi: 10.1016/j.bbamem. 2014.02.019.
34. Ladokhin AS, Jayasinghe S, White SH. 2000. How to measure and analyze tryptophan fluorescence in membranes properly, and why bother? Analytical Biochemistry 285:235-245. doi: 10.1006/abio.2000.4773.
35. Lee CW, Kim S, Roh SH, Endoh H, Kodera Y, Maeda T, Kohno T, Wang JM, Swartz KJ, Kim JI. 2004. Solution structure and functional characterization of SGTx1, a modifier of Kv2.1 channel gating. Biochemistry 43:890-897. doi: 10.1021/bi0353373.
36. Lee HC, Wang JM, Swartz KJ. 2003. Interaction between extracellular Hanatoxin and the resting conformation of the voltage-sensor paddle in Kv channels. Neuron 40:527-536. doi: 10.1016/S0896-6273(03)00636-6.
37. Lee S, Milescu M, Jung HH, Lee JY, Bae CH, Lee CW, Kim HH, Swartz KJ, Kim JI. 2010. Solution structure of GxTX-1E, a high-affinity tarantula toxin interacting with voltage sensors in Kv2.1 potassium channels. Biochemistry 49: 5134-5142. doi: 10.1021/bi100246u.
38. Lee SY, MacKinnon R. 2004. A membrane-access mechanism of ion channel inhibition by voltage sensor toxins from spider venom. Nature 430:232-235. doi: 10.1038/nature02632.
39. Li-Smerin Y, Swartz KJ. 1998. Gating modifier toxins reveal a conserved structural motif in voltage- gated Ca2+ and K+ channels. Proceedings of the National Academy of Sciences of USA 95:8585-8589. doi: 10.1073/pnas.95.15.8585.
40. Li-Smerin Y, Swartz KJ. 2000. Localization and molecular determinants of the Hanatoxin receptors on the voltagesensing domain of a K+ channel. The Journal of General Physiology 115:673-684. doi: 10.1085/jgp.115.6.673.
41. Li-Smerin Y, Swartz KJ. 2001. Helical structure of the COOH terminus of S3 and its contribution to the gating modifier toxin receptor in voltage-gated ion channels. The Journal of General Physiology 117:205-218. doi: 10.1085/jgp.117.3.205.
42. 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. doi: 10.1038/nature06265.
43. MacKinnon R. 1991. Determination of the subunit stoichiometry of a voltage-activated potassium channel. Nature 350:232-235. doi: 10.1038/350232a0.
44. MacKinnon R, Aldrich RW, Lee AW. 1993. Functional stoichiometry of Shaker potassium channel inactivation. Science 262:757-759. doi: 10.1126/science.7694359.
45. MacKinnon R, Miller C. 1988. Mechanism of charybdotoxin block of the high-conductance, Ca2+- activated K+ channel. The Journal of General Physiology 91:335-349. doi: 10.1085/jgp.91.3.335.
46. MacKinnon R, Miller C. 1989. Mutant potassium channels with altered binding of charybdotoxin, a pore- blocking peptide inhibitor. Science 245:1382-1385. doi: 10.1126/science.2476850.
47. Mihailescu M, Krepkiy D, Milescu M, Gawrisch K, Swartz KJ, White S. 2014. Structural interactions of a voltage sensor toxin with lipid membranes. Proceedings of the National Academy of Sciences of USA 111:E5463-E5470. doi: 10.1073/pnas.1415324111.
48. Milescu M, Bosmans F, Lee S, Alabi AA, Kim JI, Swartz KJ. 2009. Interactions between lipids and voltage sensor paddles detected with tarantula toxins. Nature Structural & Molecular Biology 16:1080-1085. doi: 10.1038/nsmb.1679.
49. Milescu M, Lee HC, Bae CH, Kim JI, Swartz KJ. 2013. Opening the shaker K+ channel with hanatoxin. The Journal of General Physiology 141:203-216. doi: 10.1085/jgp.201210914.
50. Milescu M, Vobecky J, Roh SH, Kim SH, Jung HJ, Kim JI, Swartz KJ. 2007. Tarantula toxins interact with voltage sensors within lipid membranes. The Journal of General Physiology 130:497-511. doi: 10.1085/jgp.200709869.
51. Miller C. 1995. The charybdotoxin family of K+ channel-blocking peptides. Neuron 15:5-10. doi: 10.1016/0896- 6273(95)90057-8.
52. Morin TJ, Kobertz WR. 2008. Counting membrane-embedded KCNE beta-subunits in functioning K+ channel complexes. Proceedings of the National Academy of Sciences of USA 105:1478-1482. doi: 10.1073/pnas. 0710366105.
53. Norton RS, Pallaghy PK. 1998. The cystine knot structure of ion channel toxins and related polypeptides. Toxicon 36:1573-1583. doi: 10.1016/S0041-0101(98)00149-4.
54. Pallaghy PK, Nielsen KJ, Craik DJ, Norton RS. 1994. A common structural motif incorporating a cystine knot and a triple-stranded beta-sheet in toxic and inhibitory polypeptides. Protein Science 3:1833-1839. doi: 10.1002/pro. 5560031022.
55. Phillips LR, Milescu M, Li-Smerin Y, Mindell JA, Kim JI, Swartz KJ. 2005. Voltage-sensor activation with a tarantula toxin as cargo. Nature 436:857-860. doi: 10.1038/nature03873.
56. Posokhov YO, Gottlieb PA, Ladokhin AS. 2007. Quenching-enhanced fluorescence titration protocol for accurate determination of free energy of membrane binding. Analytical Biochemistry 362:290-292. doi: 10.1016/j.ab. 2006.11.022.
57. Raman S, Vernon R, Thompson J, Tyka M, Sadreyev R, Pei J, Kim D, Kellogg E, Dimaio F, Lange O, Kinch L, Sheffler W, Kim BH, Das R, Grishin NV, Baker D. 2009. Structure prediction for CASP8 with all-atom refinement using Rosetta. Proteins 77:89-99. doi: 10.1002/prot.22540.
58. Rogers JC, Qu Y, Tanada TN, Scheuer T, Catterall WA. 1996. Molecular determinants of high affinity binding of alpha-scorpion toxin and sea anemone toxin in the S3-S4 extracellular loop in domain IV of the Na+ channel alpha subunit. The Journal of Biological Chemistry 271:15950-15962. doi: 10.1074/jbc.271.27.15950.
59. Rohl CA, Strauss CE, Misura KM, Baker D. 2004. Protein structure prediction using Rosetta. Methods in Enzymology 383:66-93. doi: 10.1016/S0076-6879(04)83004-0.
60. Salinas M, Rash LD, Baron A, Lambeau G, Escoubas P, Lazdunski M. 2006. The receptor site of the spider toxin PcTx1 on the proton-gated cation channel ASIC1a. The Journal of Physiology 570:339-354. doi: 10.1113/ jphysiol.2005.095810.
61. Schmalhofer WA, Ratliff KS, Weinglass A, Kaczorowski GJ, Garcia ML, Herrington J. 2009. A KV2.1 gating modifier binding assay suitable for high throughput screening. Channels 3:437-447. doi: 10.4161/chan.3.6.10201.
62. Schmidt D, MacKinnon R. 2008. Voltage-dependent K+ channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane. Proceedings of the National Academy of Sciences of USA 105: 19276-19281. doi: 10.1073/pnas.0810187105.
63. Suchyna TM, Tape SE, Koeppe RE II, Andersen OS, Sachs F, Gottlieb PA. 2004. Bilayer-dependent inhibition of mechanosensitive channels by neuroactive peptide enantiomers. Nature 430:235-240. doi: 10.1038/nature02743.
64. Swartz KJ. 2007. Tarantula toxins interacting with voltage sensors in potassium channels. Toxicon 49:213-230. doi: 10.1016/j.toxicon.2006.09.024.
65. Swartz KJ, MacKinnon R. 1995. An inhibitor of the Kv2.1 potassium channel isolated from the venom of a Chilean tarantula. Neuron 15:941-949. doi: 10.1016/0896-6273(95)90184-1.
66. Swartz KJ, MacKinnon R. 1997a. Hanatoxin modifies the gating of a voltage-dependent K+ channel through multiple binding sites. Neuron 18:665-673. doi: 10.1016/S0896-6273(00)80306-2.
67. Swartz KJ, MacKinnon R. 1997b. Mapping the receptor site for hanatoxin, a gating modifier of voltage- dependent K+ channels. Neuron 18:675-682. doi: 10.1016/S0896-6273(00)80307-4.
68. Takahashi H, Kim JI, Min HJ, Sato K, Swartz KJ, Shimada I. 2000. Solution structure of hanatoxin1, a gating modifier of voltage-dependent K(+) channels: common surface features of gating modifier toxins. Journal of Molecular Biology 297:771-780. doi: 10.1006/jmbi.2000.3609
69. Tilley DC, Eum KS, Fletcher-Taylor S, Austin DC, DupréC, Patrón LA, Garcia RL, Lam K, Yarov-Yarovoy V, Cohen BE, Sack JT. 2014. Chemoselective tarantula toxins report voltage activation of wild-type ion channels in live cells. Proceedings of the National Academy of Sciences of USA 111:E4789-E4796. doi: 10.1073/pnas.1406876111.
70. Tyka MD, Keedy DA, AndréI, Dimaio F, Song Y, Richardson DC, Richardson JS, Baker D. 2011. Alternate states of proteins revealed by detailed energy landscape mapping. Journal of Molecular Biology 405: 607-618. doi: 10.1016/j.jmb.2010.11.008.
71. Wang C, Bradley P, Baker D. 2007. Protein-protein docking with backbone flexibility. Journal of Molecular Biology 373:503-519. doi: 10.1016/j.jmb.2007.07.050.
72. Wang JM, Roh SH, Kim S, Lee CW, Kim JI, Swartz KJ. 2004. Molecular surface of tarantula toxins interacting with voltage sensors in K(v) channels. The Journal of General Physiology 123:455-467. doi: 10.1085/jgp.200309005.
73. Xu Y, Ramu Y, Shin HG, Yamakaze J, Lu Z. 2013. Energetic role of the paddle motif in voltage gating of Shaker K(+) channels. Nature Structural & Molecular Biology 20:574-581. doi: 10.1038/nsmb.2535.