Seven novel modulators of the analgesic target NaV1.7 uncovered using a high-throughput venom-based discovery approach

British Journal of Pharmacology

Volumn 172, Issue 10, 2015, Pages 2445-2458

  Klint, Julie K ^a   Smith, Jennifer J ^a   Vetter, Irina ^a   Rupasinghe, Darshani B ^a   Er, Sing Yan ^a   Senff, Sebastian ^a   Herzig, Volker ^a   Mobli, Mehdi ^a   Lewis, Richard J ^a   Bosmans, Frank ^b,c   King, Glenn F ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE MU TETRODOTOXIN CCY1A; PEPTIDE MU TETRODOTOXIN CCY1B; PEPTIDE MU TETRODOTOXIN EP1A; PEPTIDE MU TETRODOTOXIN HD1A; PEPTIDE MU TETRODOTOXIN OSP1A; PEPTIDE MU TETRODOTOXIN OSP1B; PEPTIDE MU TETRODOTOXIN SE1A; SODIUM CHANNEL NAV1.1; SODIUM CHANNEL NAV1.2; SODIUM CHANNEL NAV1.3; SODIUM CHANNEL NAV1.4; SODIUM CHANNEL NAV1.5; SODIUM CHANNEL NAV1.6; SODIUM CHANNEL NAV1.7; SODIUM CHANNEL NAV1.8; SPIDER VENOM; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL BLOCKING AGENT; ANALGESIC AGENT; PROTX-III PROTEIN, THRIXOPELMA PRURIENS;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CHROMATOPELMA CYANEOPUBESCENS; CONTROLLED STUDY; DOMAIN II VOLTAGE SENSOR; DRUG ACTIVITY; DRUG ISOLATION; DRUG PURIFICATION; DRUG SELECTIVITY; DRUG TARGETING; EUATHLUS PULCHERRIMAKLAASI; FEMALE; FLUORESCENCE ANALYSIS; HAPLOPELMA; HAPLOPELMA DORIAE; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IC50; INHIBITOR CYSTINE KNOT MOTIF; MOLECULAR STABILITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OOCYTE; ORPHNAECUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN STRUCTURE; S3B S4 PADDLE MOTIF; SELENOCOSMIA EFFERA; SPIDER; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; VOLTAGE CLAMP TECHNIQUE; XENOPUS; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DRUG DEVELOPMENT; METABOLISM; MOLECULAR GENETICS; PROCEDURES;

AMINO ACID SEQUENCE; ANALGESICS; ANIMALS; DRUG DISCOVERY; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MOLECULAR SEQUENCE DATA; NAV1.7 VOLTAGE-GATED SODIUM CHANNEL; SPIDER VENOMS; VOLTAGE-GATED SODIUM CHANNEL BLOCKERS;

EID: 84928342298     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13081     Document Type: Article

References (62)

1. + channel. Neuron 16: 1169-1177.
2. 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.
3. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013). The Concise Guide to PHARMACOLOGY 2013/14: Ion channels. Br J Pharmacol 170: 1607-1651.
4. Bosmans F, Swartz KJ, (2010). Targeting voltage sensors in sodium channels with spider toxins. Trends Pharmacol Sci 31: 175-182.
5. Bosmans F, Rash L, Zhu S, Diochot S, Lazdunski M, Escoubas P, et al. (2006). Four novel tarantula toxins as selective modulators of voltage-gated sodium channel subtypes. Mol Pharmacol 69: 419-429.
6. Bosmans F, Martin-Eauclaire MF, Swartz KJ, (2008). Deconstructing voltage sensor function and pharmacology in sodium channels. Nature 456: 202-208.
7. Bosmans F, Puopolo M, Martin-Eauclaire MF, Bean BP, Swartz KJ, (2011). Functional properties and toxin pharmacology of a dorsal root ganglion sodium channel viewed through its voltage sensors. J Gen Physiol 138: 59-72.
8. Cabrita LD, Dai W, Bottomley SP, (2006). A family of E. coli expression vectors for laboratory scale and high throughput soluble protein production. BMC Biotech 6: 12.
9. Catterall WA, Goldin AL, Waxman SG, (2005). International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57: 397-409.
10. Catterall WA, Cestele S, Yarov-Yarovoy V, Yu FH, Konoki K, Scheuer T, (2007). Voltage-gated ion channels and gating modifier toxins. Toxicon 49: 124-141.
11. Cestele S, Qu Y, Rogers JC, Rochat H, Scheuer T, Catterall WA, (1998). Voltage sensor-trapping: enhanced activation of sodium channels by β-scorpion toxin bound to the S3-S4 loop in domain II. Neuron 21: 919-931.
12. Chanda B, Bezanilla F, (2002). Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. J Gen Physiol 120: 629-645.
13. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, et al. (2010). MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21.
14. V1.7 in inherited erythromelalgia: enhanced slow inactivation modulates dorsal root ganglion neuron hyperexcitability. Brain 134: 1972-1986.
15. Cox JJ, Reimann F, Nicholas AK, Thornton G, Roberts E, Springell K, et al. (2006). An SCN9A channelopathy causes congenital inability to experience pain. Nature 444: 894-898.
16. Duan G, Xiang G, Zhang X, Yuan R, Zhan H, Qi D, (2013). A single-nucleotide polymorphism in SCN9A may decrease postoperative pain sensitivity in the general population. Anesthesiology 118: 436-442.
17. Escoubas P, Bosmans F, (2007). Spider peptide toxins as leads for drug development. Expert Opin Drug Discov 2: 823-835.
18. Escoubas P, Sollod B, King GF, (2006). Venom landscapes: mining the complexity of spider venoms via a combined cDNA and mass spectrometric approach. Toxicon 47: 650-663.
19. V1.7 gain-of-function mutations as a continuum: A1632E displays physiological changes associated with erythromelalgia and paroxysmal extreme pain disorder mutations and produces symptoms of both disorders. J Neurosci 28: 11079-11088.
20. Fertleman CR, Baker MD, Parker KA, Moffatt S, Elmslie FV, Abrahamsen B, et al. (2006). SCN9A mutations in paroxysmal extreme pain disorder: allelic variants underlie distinct channel defects and phenotypes. Neuron 52: 767-774.
21. Frech GC, Vandongen AM, Schuster G, Brown AM, Joho RH, (1989). A novel potassium channel with delayed rectifier properties isolated from rat brain by expression cloning. Nature 340: 642-645.
22. + channels from Leiurus quinquestriatus var. hebraeus venom. Biochemistry 33: 6834-6839.
23. Gaskin DJ, Richard P, (2012). The economic costs of pain in the United States. J Pain 13: 715-724.
24. Gilchrist J, Olivera BM, Bosmans F, (2014). Animal toxins influence voltage-gated sodium channel function. Handb Exp Pharmacol 221: 203-229.
25. Gui J, Liu B, Cao G, Lipchik AM, Perez M, Dekan Z, et al. (2014). A tarantula-venom peptide antagonizes the TRPA1 nociceptor ion channel by binding to the S1-S4 gating domain. Curr Biol 24: 473-483.
26. Gurevitz M, Karbat I, Cohen L, Ilan N, Kahn R, Turkov M, et al. (2007). The insecticidal potential of scorpion β-toxins. Toxicon 49: 473-489.
27. Güntert P, (2004). Automated NMR structure calculation with CYANA. Methods Mol Biol 278: 353-378.
28. Herzig V, Wood DL, Newell F, Chaumeil PA, Kaas Q, Binford GJ, et al. (2011). ArachnoServer 2.0, an updated online resource for spider toxin sequences and structures. Nucl Acids Res 39: D653-D657.
29. Horn R, Ding S, Gruber HJ, (2000). Immobilizing the moving parts of voltage-gated ion channels. J Gen Physiol 116: 461-476.
30. Kapust RB, Tozser J, Copeland TD, Waugh DS, (2002). The P1 specificity of tobacco etch virus protease. Biochem Biophys Res Commun 294: 949-955.
31. V channels by peptidic spider toxins. Toxicon 49: 513-530.
32. V1.7 as an analgesic target. ACS Chem Neurosci 5: 749-751.
33. V channels. Channels 2: 100-116.
34. King GF, Gentz MC, Escoubas P, Nicholson GM, (2008b). A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon 52: 264-276.
35. Klint JK, Senff S, Rupasinghe DB, Er SY, Herzig V, Nicholson GM, et al. (2012). Spider-venom peptides that target voltage-gated sodium channels: pharmacological tools and potential therapeutic leads. Toxicon 60: 478-491.
36. Klint JK, Senff S, Saez NJ, Seshadri R, Lau HY, Bende NS, et al. (2013). Production of recombinant disulfide-rich venom peptides for structural and functional analysis via expression in the periplasm of E. coli. PLoS ONE 8: e63865.
37. Kwan AH, Mobli M, Gooley PR, King GF, Mackay JP, (2011). Macromolecular NMR spectroscopy for the non-spectroscopist. FEBS J 278: 687-703.
38. Liu Y, Li D, Wu Z, Li J, Nie D, Xiang Y, et al. (2012). A positively charged surface patch is important for hainantoxin-IV binding to voltage-gated sodium channels. J Pept Sci 18: 643-649.
39. Minassian NA, Gibbs A, Shih AY, Liu Y, Neff RA, Sutton SW, et al. (2013). Analysis of the structural and molecular basis of voltage-sensitive sodium channel inhibition by the spider toxin huwentoxin-IV (μ-TRTX-Hh2a). J Biol Chem 288: 22707-22720.
40. Mobli M, Maciejewski MW, Gryk MR, Hoch JC, (2007). An automated tool for maximum entropy reconstruction of biomolecular NMR spectra. Nat Meth 4: 467-468.
41. Mobli M, Stern AS, Bermel W, King GF, Hoch JC, (2010). A non-uniformly sampled 4D HCC(CO)NH-TOCSY experiment processed using maximum entropy for rapid protein sidechain assignment. J Magn Reson 204: 160-164.
42. Nicholson GM, Little MJ, (2005). Spider neurotoxins targeting voltage-gated sodium channels. Toxin Rev 24: 315-345.
43. Pallaghy PK, Nielsen KJ, Craik DJ, Norton RS, (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.
44. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucl. Acids Res. 42 (Database Issue): D1098-1106.
45. Reeder JE, Byler TK, Foster DC, Landas SK, Okafor H, Stearns G, et al. (2013). Polymorphism in the SCN9A voltage-gated sodium channel gene associated with interstitial cystitis/bladder pain syndrome. Urology 81: 210, e1-210.e4.
46. Reimann F, Cox JJ, Belfer I, Diatchenko L, Zaykin DV, McHale DP, et al. (2010). Pain perception is altered by a nucleotide polymorphism in SCN9A. Proc Natl Acad Sci U S A 107: 5148-5453.
47. Renicke C, Spadaccini R, Taxis C, (2013). A tobacco etch virus protease with increased substrate tolerance at the P1 position. PLoS ONE 8: e67915.
48. V1.7: a neurotoxin TTX-S sodium-channel antagonist from the venom of the Chinese bird-eating spider Selenocosmia huwena. Peptides 44: 40-46.
49. + channels and related peptides: biodiversity, structure-function relationships and evolution. Toxicon 46: 831-844.
50. Ruta V, MacKinnon R, (2004). Localization of the voltage-sensor toxin receptor on KvAP. Biochemistry 43: 10071-10079.
51. + channel. Neuron 16: 1159-1167.
52. Sheets MF, Kyle JW, Kallen RG, Hanck DA, (1999). The Na channel voltage sensor associated with inactivation is localized to the external charged residues of domain IV, S4. Biophys J 77: 747-757.
53. Shen Y, Delaglio F, Cornilescu G, Bax A, (2009). TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biomol NMR 44: 213-223.
54. V channels in SH-SY5Y human neuroblastoma cells. PLoS ONE 8: e59293.
55. + channel through multiple binding sites. Neuron 18: 665-673.
56. Theile JW, Jarecki BW, Piekarz AD, Cummins TR, (2011). Nav1.7 mutations associated with paroxysmal extreme pain disorder, but not erythromelalgia, enhance Navβ4 peptide-mediated resurgent sodium currents. J Physiol 589: 597-608.
57. Vetter I, Davis JL, Rash LD, Anangi R, Mobli M, Alewood PF, et al. (2011). Venomics: a new paradigm for natural products-based drug discovery. Amino Acids 40: 15-28.
58. V types endogenously expressed in human SH-SY5Y neuroblastoma cells. Biochem Pharmacol 83: 1562-1571.
59. Xiao Y, Bingham JP, Zhu W, Moczydlowski E, Liang S, Cummins TR, (2008). Tarantula huwentoxin-IV inhibits neuronal sodium channels by binding to receptor site 4 and trapping the domain II voltage sensor in the closed configuration. J Biol Chem 283: 27300-27313.
60. + channel voltage-sensors in domains II and IV. J Biol Chem 286: 27301-27310.
61. Yang S, Liu Z, Xiao Y, Li Y, Rong M, Liang S, et al. (2012). Chemical punch packed in venoms makes centipedes excellent predators. Mol Cell Proteomics 11: 640-650.
62. Yang Y, Wang Y, Li S, Xu Z, Li H, Ma L, et al. (2004). Mutations in SCN9A, encoding a sodium channel alpha subunit, in patients with primary erythermalgia. J Med Genet 41: 171-174.