The insecticidal neurotoxin Aps III is an atypical knottin peptide that potently blocks insect voltage-gated sodium channels

Biochemical Pharmacology

Volumn 85, Issue 10, 2013, Pages 1542-1554

  Bende, Niraj S ^a   Kang, Eunji ^b   Herzig, Volker ^a   Bosmans, Frank ^c   Nicholson, Graham M ^b   Mobli, Mehdi ^a   King, Glenn F ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

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

Author keywords

Gating modifier; Inhibitor cystine knot; Neurotoxin; Pore blocker; Spider venom peptide; Voltage gated sodium channel

Indexed keywords

DISULFIDE; INSECTICIDE; KNOTTIN; NEUROTOXIN; PROTEIN APS III; RECOMBINANT PROTEIN; SPIDER VENOM; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG POTENCY; ESCHERICHIA COLI; INSECTICIDAL ACTIVITY; NONHUMAN; PEST CONTROL; PHARMACOPHORE; PRIORITY JOURNAL; STEADY STATE; VESTIBULE;

AMINO ACID SEQUENCE; ANIMALS; CYSTINE-KNOT MINIPROTEINS; DIPTERA; DISULFIDES; ESCHERICHIA COLI; INSECT PROTEINS; KINETICS; MEMBRANE POTENTIALS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEURONS; NEUROTOXINS; PATCH-CLAMP TECHNIQUES; PERIPLANETA; PRIMARY CELL CULTURE; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SODIUM CHANNEL BLOCKERS; SPIDER VENOMS; SPIDERS; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84876666595     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2013.02.030     Document Type: Article

References (79)

1. H.W. Tedford, B.L. Sollod, F. Maggio, and G.F. King Australian funnel-web spiders: master insecticide chemists Toxicon 43 2004 601 618
2. World Health Organization. World Malaria Report 2009. Geneva, Switzerland: WHO Press; 2009.
3. E.C. Oerke Crop losses to pests J Agric Sci 144 2006 31 43
4. D. Pimental Pesticides and pest control R. Peshin, A.K. Dhawan, Integrated pest management: innovation-development process 2009 Springer Verlag Dordrecht 83 87
5. H.W. Tedford, N. Gilles, A. Ménez, C.J. Doering, G.W. Zamponi, and G.F. King Scanning mutagenesis of ω-atracotoxin-Hv1a reveals a spatially restricted epitope that confers selective activity against invertebrate calcium channels J Biol Chem 279 2004 44133 44140
6. C. Bass, and L.M. Field Gene amplification and insecticide resistance Pest Manag Sci 67 2011 886 890
7. G.F. King, and M.C. Hardy Spider-venom peptides: structure, pharmacology, and potential for control of insect pests Annu Rev Entomol 58 2013 475 496
8. A.M. Gatehouse, N. Ferry, M.G. Edwards, and H.A. Bell Insect-resistant biotech crops and their impacts on beneficial arthropods Philos Trans R Soc Lond B: Biol Sci 366 2011 1438 1452
9. S.L. Bates, J.Z. Zhao, R.T. Roush, and A.M. Shelton Insect resistance management in GM crops: past, present and future Nat Biotechnol 23 2005 57 62
10. F. Maggio, B.L. Sollod, H.W. Tedford, V. Herzig, and G.F. King Spider toxins and their potential for insect control L.I. Gilbert, S.S. Gill, Insect pharmacology: channels, receptors, toxins and enzymes 2010 Academic Press London 101 123
11. L. Kuhn-Nentwig, R. Stöcklin, and W. Nentwig Venom composition and strategies in spiders: is everything possible? J. Casas, Spider physiology and behaviour - physiology 2011 Elsevier 1 86
12. M.J. Windley, V. Herzig, S.A. Dziemborowicz, M.C. Hardy, G.F. King, and G.M. Nicholson Spider-venom peptides as bioinsecticides Toxins 4 2012 191 227
13. P.K. Pallaghy, K.J. Nielsen, D.J. Craik, and R.S. Norton A common structural motif incorporating a cystine knot and a triple-stranded β-sheet in toxic and inhibitory polypeptides Protein Sci 3 1994 1833 1839
14. G.F. King, H.W. Tedford, and F. Maggio Structure and function of insecticidal neurotoxins from Australian funnel-web spiders J Toxicol Toxin Rev 21 2002 359 389
15. N.J. Saez, S. Senff, J.E. Jensen, S.Y. Er, V. Herzig, and L.D. Rash Spider-venom peptides as therapeutics Toxins 2 2010 2851 2871
16. W.S. Skinner, P.A. Dennis, J.P. Li, and G.B. Quistad Identification of insecticidal peptides from venom of the trap-door spider, Aptostichus schlingeri (Ctenizidae) Toxicon 30 1992 1043 1050
17. D.L. Wood, T. Miljenovic, S. Cai, R.J. Raven, Q. Kaas, and P. Escoubas ArachnoServer: a database of protein toxins from spiders BMC Genomics 10 2009 375
18. V. Herzig, D.L.A. Wood, F. Newell, P.-A. Chaumeil, Q. Kaas, and G.J. Binford ArachnoServer 2.0, an updated online resource for spider toxin sequences and structures Nucleic Acids Res 39 2011 D653 D657
19. J.K. Klint, S. Senff, D.B. Rupasinghe, S.Y. Er, V. Herzig, and G.M. Nicholson Spider-venom peptides that target voltage-gated sodium channels: pharmacological tools and potential therapeutic leads Toxicon 60 2012 478 491
20. L. Fang, K.Z. Jia, Y.L. Tang, D.Y. Ma, M. Yu, and Z.C. Hua An improved strategy for high-level production of TEV protease in Escherichia coli and its purification and characterization Protein Expr Purif 51 2007 102 109
21. L.D. Cabrita, W. Dai, and S.P. Bottomley A family of E. coli expression vectors for laboratory scale and high throughput soluble protein production BMC Biotechnol 6 2006 12
22. J.P. Bassford Export of the periplasmic maltose-binding protein of Escherichia coli J Bioenerg Biomembr 22 1990 401 439
23. R.B. Kapust, and D.S. Waugh Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused Protein Sci 8 1999 1668 1674
24. N.J. Saez, M. Mobli, M. Bieri, I.R. Chassagnon, A.K. Malde, and R. Gamsjaeger A dynamic pharmacophore drives the interaction between psalmotoxin-1 and the putative drug target acid-sensing ion channel 1a Mol Pharmacol 80 2011 796 808
25. M. Eitan, E. Fowler, R. Herrmann, A. Duval, M. Pelhate, and E. Zlotkin A scorpion venom neurotoxin paralytic to insects that affects sodium current inactivation: purification, primary structure, and mode of action Biochemistry 29 1990 5941 5947
26. V. Herzig, and W.C. Hodgson Neurotoxic and insecticidal properties of venom from the Australian theraphosid spider Selenotholus foelschei Neurotoxicology 29 2008 471 475
27. ca channels FEBS J 275 2008 4045 4059
28. + channels isolated from the venom of the theraphosid spider Eucratoscelus constrictus Mol Pharmacol 80 2011 1 13
29. P.H. Barry JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements J Neurosci Methods 51 1994 107 116
30. 2+ currents in central insect neurons: electrophysiological and pharmacological properties J Neurophysiol 77 1997 186 199
31. J. Tan, Z. Liu, Y. Nomura, A.L. Goldin, and K. Dong Alternative splicing of an insect sodium channel gene generates pharmacologically distinct sodium channels J Neurosci 22 2002 5300 5309
32. G. Feng, P. Deak, M. Chopra, and L.M. Hall Cloning and functional analysis of TipE, a novel membrane protein that enhances Drosophila para sodium channel function Cell 82 1995 1001 10011
33. V1.6 sodium channel Biophys J 87 2004 3862 3872
34. M. Mobli, A.S. Stern, W. Bermel, G.F. King, and J.C. Hoch A non-uniformly sampled 4D HCC(CO)NH-TOCSY experiment processed using maximum entropy for rapid protein sidechain assignment J Magn Reson 204 2010 160 164
35. M. Mobli, M.W. Maciejewski, M.R. Gryk, and J.C. Hoch An automated tool for maximum entropy reconstruction of biomolecular NMR spectra Nat Methods 4 2007 467 468
36. Y. Shen, F. Delaglio, G. Cornilescu, and A. Bax TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J Biomol NMR 44 2009 213 223
37. J.I. Fletcher, R. Smith, S.I. O'Donoghue, M. Nilges, M. Connor, and M.E.H. Howden The structure of a novel insecticidal neurotoxin, ω-atracotoxin-HV1, from the venom of an Australian funnel web spider Nat Struct Biol 4 1997 559 566
38. P. Güntert Automated NMR structure calculation with CYANA Methods Mol Biol 278 2004 353 378
39. I. Vetter, J.L. Davis, L.D. Rash, R. Anangi, M. Mobli, and P.F. Alewood Venomics: a new paradigm for natural products-based drug discovery Amino Acids 40 2011 15 28
40. E. Meng, T.F. Cai, W.Y. Li, H. Zhang, Y.B. Liu, and K. Peng Functional expression of spider neurotoxic peptide huwentoxin-I in E. coli PLoS ONE 6 2011 e21608
41. B. Heras, S.R. Shouldice, M. Totsika, M.J. Scanlon, M.A. Schembri, and J.L. Martin DSB proteins and bacterial pathogenicity Nat Rev Microbiol 7 2009 215 225
42. D. Sackett, P. Holmes, K. Abbott, S. Jephcott, and M. Barber Assessing the economic cost of endemic disease on the profitability of Australian beef cattle and sheep producers 2006 Meat & Livestock Australia Sydney
43. A. Vassilevski, S. Kozlov, and E. Grishin Molecular diversity of spider venom Biochemistry (Moscow) 74 2009 1505 1534
44. F. Bosmans, P. Escoubas, and G.M. Nicholson Spider venom peptides as leads for drug and insecticide design M.E. de Lima, A.M.C. Pimenta, M.-F. Martin-Eauclaire, R.B. Zingali, H. Rochat, Animal toxins: state of the art perspectives in health and biotechnology 2009 Federal University of Minas Gerais Press Belo Horizonte 269 290
45. N. Yamaji, M.J. Little, H. Nishio, B. Billen, E. Villegas, and Y. Nishiuchi Synthesis, solution structure, and phylum selectivity of a spider δ-toxin that slows inactivation of specific voltage-gated sodium channel subtypes J Biol Chem 284 2009 24568 24582
46. Y. Chong, J.L. Hayes, B. Sollod, S. Wen, D.T. Wilson, and P.G. Hains The ω-atracotoxins: selective blockers of insect M-LVA and HVA calcium channels Biochem Pharmacol 74 2007 623 638
47. M.M. Zhang, T.S. Han, B.M. Olivera, G. Bulaj, and D. Yoshikami μ-conotoxin KIIIA derivatives with divergent affinities versus efficacies in blocking voltage-gated sodium channels Biochemistry 49 2010 4804 4812
48. v channels by peptidic spider toxins Toxicon 49 2007 513 530
49. v channels Channels 2 2008 100 116
50. F. Grolleau, and B. Lapied Separation and identification of multiple potassium currents regulating the pacemaker activity of insect neurosecretory cells (DUM neurons) J Neurophysiol 73 1995 160 171
51. D. Wicher, C. Walther, and C. Wicher Non-synaptic ion channels in insects - basic properties of currents and their modulation in neurons and skeletal muscles Prog Neurobiol 64 2001 431 525
52. F. Bosmans, and K.J. Swartz Targeting voltage sensors in sodium channels with spider toxins Trends Pharmacol Sci 31 2010 175 182
53. M. Mobli, and G.F. King NMR methods for determining disulfide-bond connectivities Toxicon 56 2010 849 854
54. I.W. Davis, A. Leaver-Fay, V.B. Chen, J.N. Block, G.J. Kapral, and X. Wang MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res 35 2007 W375 W383
55. A.H. Kwan, M. Mobli, P.R. Gooley, G.F. King, and J.P. Mackay Macromolecular NMR spectroscopy for the non-spectroscopist FEBS J 278 2011 687 703
56. R.A. Laskowski PDBsum new things Nucleic Acids Res 37 2009 D355 D359
57. J. Gracy, D. Le-Nguyen, J.C. Gelly, Q. Kaas, A. Heitz, and L. Chiche KNOTTIN: the knottin or inhibitor cystine knot scaffold in 2007 Nucleic Acids Res 36 2008 D314 D319
58. K.J. Shon, B.M. Olivera, M. Watkins, R. Jacobsen, W.R. Gray, and C.Z. Floresca μ-Conotoxin PIIIA, a new peptide for discriminating among tetrodotoxin-sensitive Na channel subtypes J Neurosci 18 1998 4473 4481
59. D. Li, Y. Xiao, W. Hu, J. Xie, F. Bosmans, and J. Tytgat Function and solution structure of hainantoxin-I, a novel insect sodium channel inhibitor from the Chinese bird spider Selenocosmia hainana FEBS Lett 555 2003 616 622
60. R.L. Wang, S. Yi, and S.P. Liang Mechanism of action of two insect toxins huwentoxin-III and hainantoxin-VI on voltage-gated sodium channels J Zhejiang Univ Sci B 11 2010 451 457
61. B. Billen, A. Vassilevski, A. Nikolsky, J. Tytgat, and E. Grishin Two novel sodium channel inhibitors from Heriaeus melloteei spider venom differentially interacting with mammalian channel's isoforms Toxicon 2008 309 317
62. J.I. Fletcher, B.E. Chapman, J.P. Mackay, M.E.H. Howden, and G.F. King The structure of versutoxin (δ-atracotoxin-Hv1) provides insights into the binding of site 3 neurotoxins to the voltage-gated sodium channel Structure 5 1997 1525 1535
63. M.J. Little, H. Wilson, C. Zappia, S. Cestele, M.I. Tyler, and M.F. Martin-Eauclaire δ-atracotoxins from Australian funnel-web spiders compete with scorpion α-toxin binding on both rat brain and insect sodium channels FEBS Lett 1998 246 252
64. M.J. Little, C. Zappia, N. Gilles, M. Connor, M.I. Tyler, and M.F. Martin-Eauclaire δ-Atracotoxins from Australian funnel-web spiders compete with scorpion α-toxin binding but differentially modulate alkaloid toxin activation of voltage-gated sodium channels J Biol Chem 273 1998 27076 27083
65. + channels J Exp Biol 204 2001 711 721
66. A. Matavel, J.S. Cruz, C.L. Penaforte, D.A. Araujo, E. Kalapothakis, and V.F. Prado Electrophysiological characterization and molecular identification of the Phoneutria nigriventer peptide toxin PnTx2-6 FEBS Lett 2002 523
67. G.M. Nicholson Insect-selective spider toxins targeting voltage-gated sodium channels Toxicon 49 2007 490 512
68. X. Zeng, M. Deng, Y. Lin, C. Yuan, J. Pi, and S. Liang Isolation and characterization of Jingzhaotoxin-V, a novel neurotoxin from the venom of the spider Chilobrachys jingzhao Toxicon 49 2007 388 399
69. F. Bosmans, M.F. Martin-Eauclaire, and K.J. Swartz Deconstructing voltage sensor function and pharmacology in sodium channels Nature 456 2008 202 208
70. F. Bosmans, L. Rash, S. Zhu, S. Diochot, M. Lazdunski, and P. Escoubas Four novel tarantula toxins as selective modulators of voltage-gated sodium channel subtypes Mol Pharmacol 69 2006 419 429
71. G.F. King, M.C. Gentz, P. Escoubas, and G.M. Nicholson A rational nomenclature for naming peptide toxins from spiders and other venomous animals Toxicon 52 2008 264 276
72. + channels Proc Natl Acad Sci USA 95 1998 8585 8589
73. M. Wang, X. Guan, and S. Liang The cross channel activities of spider neurotoxin huwentoxin-I on rat dorsal root ganglion neurons Biochem Biophys Res Commun 357 2007 579 583
74. v2.1 channels Toxicon 50 2007 135 143
75. V3.1 by ProTxII Toxicon 56 2010 624 636
76. + channels of chromaffin cells Eur J Pharmacol 475 2003 11 18
77. + currents in neurosecretory insect neurons Receptors Channels 5 1998 355 366
78. W.A. Catterall Voltage-gated sodium channels at 60: structure, function and pathophysiology J Physiol 590 2012 2577 2589
79. H. Kubista, R.A. Mafra, G.M. Nicholson, P.S. Beirão, J.S. Cruz, and S. Boehm CSTX-1, a toxin from the venom of the hunting spider Cupiennius salei, is a selective blocker of L-type calcium channels in mammalian neurons Neuropharmacol 52 2007 1650 1662