Structure and function of δ-atracotoxins: Lethal neurotoxins targeting the voltage-gated sodium channel

Toxicon

Volumn 43, Issue 5, 2004, Pages 587-599

  Nicholson, Graham M ^a   Little, Michelle J ^a   Birinyi Strachan, Liesl C ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

atracotoxin; Funnel web spider; Inhibitor cystine knot; Scorpion toxin; Sea anemone toxin; Voltage gated sodium channel

Indexed keywords

ATRACOTOXIN DERIVATIVE; DISULFIDE; NEUROTOXIN; POLYPEPTIDE; SCORPION VENOM; SEA ANEMONE TOXIN; SNAIL VENOM; SPIDER VENOM; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

AUTONOMIC NERVE; BINDING AFFINITY; BINDING SITE; COCKROACH; ELECTROPHYSIOLOGY; ENVENOMATION; HYPERPOLARIZATION; LETHALITY; LOCUST; MAMMAL; NERVE ENDING; NERVE POTENTIAL; NEUROCHEMISTRY; NEUROTRANSMITTER RELEASE; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN MOTIF; RECEPTOR BINDING; REVIEW; SEQUENCE HOMOLOGY; SPIDER; TAXONOMY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; AUSTRALIA; ELECTROPHYSIOLOGY; MOLECULAR SEQUENCE DATA; NEUROTOXINS; PEPTIDES; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SODIUM CHANNELS; SPIDER VENOMS; SPIDERS; STRUCTURE-ACTIVITY RELATIONSHIP; SYNAPSES;

ACTINIARIA; ANEMONE; ARANEAE; BLATTARIA; DIPLURIDAE; GASTROPODA; MAMMALIA; SCORPIONES;

EID: 1942438958     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2004.02.006     Document Type: Review

References (90)

1. Alewood D., Birinyi-Strachan L.C., Pallaghy P., Norton R., Nicholson G.M., Alewood P.F. Synthesis and characterisation of δ-atracotoxin-Ar1 the lethal neurotoxin from venom of the Sydney funnel-web spider (Atrax robustus). Biochemistry. 2004;. 42, 12933-12940.
2. Benzinger G.R., Kyle J.W., Blumenthal K.M., Hanck D.A. A specific interaction between the cardiac sodium channel and site-3 toxin anthopleurin B. J. Biol. Chem. 273:1998;80-84.
3. Bernard C., Corzo G., Mosbah A., Nakajima T., Darbon H. Solution structure of Ptu1, a toxin from the assassin bug Peirates turpis that blocks the voltage-sensitive calcium channel N-type. Biochemistry. 40:2001;12795-12800.
4. v4.2 potassium channel. Protein Sci. 9:2000;2059-2067.
5. Brown M.R., Sheumack D.D., Tyler M.I., Howden M.E.H. Amino acid sequence of versutoxin, a lethal neurotoxin from the venom of the funnel-web spider Atrax versutus. Biochem. J. 250:1988;401-405.
6. Calvete J.J., Wang Y., Mann K., Schafer W., Niewiarowski S., Stewart G.J. The disulfide bridge pattern of snake venom disintegrins, flavoridin and echistatin. FEBS Lett. 309:1992;316-320.
7. + ionophore by neurotoxins. J. Biol. Chem. 252:1977;8669-8676.
8. Catterall W.A. Cellular and molecular biology of voltage-gated sodium channels. Physiol. Rev. 72:1992;S15-S48.
9. Cestèle S., Ben Khalifa R.B., Pelhate M., Rochat H., Gordon D. Alpha-scorpion toxins binding on rat brain and insect sodium channels reveal divergent allosteric modulations by brevetoxin and veratridine. J. Biol. Chem. 270:1995;15153-15161.
10. Cestèle S., Catterall W.A. Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie. 82:2000;883-892.
11. 1H NMR of ω-conotoxin MVIID, a calcium channel blocker peptide. Biochem. Biophys. Res. Commun. 254:1999;32-35.
12. Darbon H., Zlotkin E., Kopeyan C., van Rietschoten J., Rochat H. Covalent structure of the insect toxin of the North African scorpion Androctonus australis Hector. Int. J. Pept. Protein Res. 20:1982;320-330.
13. DeBin J.A., Maggio J.E., Strichartz G.R. Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion. Am. J. Physiol. 264:1993;C361-C369.
14. Dias-Kadambi B.L., Drum C.L., Hanck D.A., Blumenthal K.M. Leucine 18, a hydrophobic residue essential for high affinity binding of anthopleurin B to the voltage-sensitive sodium channel. J. Biol. Chem. 271:1996;9422-9428.
15. Dieckmann J., Prebble J., McDonogh A., Sara A., Fisher M. Efficacy of funnel-web spider antivenom in human envenomation by Hadronyche species. Med. J. Aust. 151:1989;706-707.
16. Eitan M., Fowler E., Herrmann R., Duval A., Pelhate M., Zlotkin E. A scorpion venom neurotoxin paralytic to insects that affects sodium current inactivation-purification, primary structure, and mode of action. Biochemistry. 29:1990;5941-5947.
17. Escoubas P., Diochot S., Corzo G. Structure and pharmacology of spider venom neurotoxins. Biochimie. 82:2000;893-907.
18. 2+ release channel/ryanodine receptors. FEBS Lett. 469:2000;179-185.
19. 1H NMR spectroscopy and complete relaxation matrix analysis. J. Mol. Biol. 248:1995;106-124.
20. Fletcher J.I., Chapman B.E., Mackay J.P., Howden M.E.H., King G.F. The structure of versutoxin (δ-atracotoxin-Hv1): implications for binding of site-3 toxins to the voltage-gated sodium channel. Structure. 5:1997;1525-1535.
21. Fletcher J.I., Dingley A.J., Smith R., Connor M., Christie M.J., King G.F. High-resolution solution structure of gurmarin, a sweet-taste-suppressing plant polypeptide. Eur. J. Biochem. 264:1999;525-533.
22. Fletcher J.I., Smith R., O'Donoghue S.I., Nilges M., Connor M., Howden M.E.H., Christie M.J., King G.F. 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.
23. Fontecilla-Camps J.C., Habersetzer-Rochat C., Rochat H. Orthorhombic crystals and three-dimensional structure of the potent toxin II from the scorpion Androctonus australis Hector. Proc. Natl. Acad. Sci. USA. 85:1988;7443-7447.
24. Fontecilla-Camps J.C., Almassy R.J., Suddath F.L., Bugg C.E. The three-dimensional structure of scorpion neurotoxins. Toxicon. 20:1982;1-7.
25. Gilles N., Harrison G., Karbat I., Gurevitz M., Nicholson G.M., Gordon D. Variations in receptor site-3 on rat brain and insect sodium channels highlighted by binding of a funnel-web spider δ-atracotoxin. Eur. J. Biochem. 269:2002;1500-1510.
26. Gilles N., Krimm I., Bouet F., Froy O., Gurevitz M., Lancelin J.M., Gordon D. Structural implications on the interaction of scorpion alpha-like toxins with the sodium channel receptor site inferred from toxin iodination and pH-dependent binding. J. Neurochem. 75:2000;1735-1745.
27. Gilles N., Leipold E., Chen H., Heinemann S.H., Gordon D. Effect of depolarization on binding kinetics of scorpion alpha-toxin highlights conformational changes of rat brain sodium channels. Biochemistry. 40:2001;14576-14584.
28. Gordon D. A new approach to insect-pest control-combination of neurotoxins interacting with voltage sensitive sodium channels to increase selectivity and specificity. Invert. Neurosci. 3:1997;103-116.
29. Gordon D. Sodium channels as targets for neurotoxins: mode of action and interaction of neurotoxins with receptor sites on sodium channels. Lazarowici P., Gutman Y. Toxins and Signal Transduction. 1997;119-149 Harwood Press, Amsterdam.
30. Gordon D., Martin-Eauclaire M.-F., Cestèle S., Kopeyan C., Carlier E., Khalifa R.B., Pelhate M., Rochat H. Scorpion toxins affecting sodium channel current inactivation bind to distinct homologous receptor sites on rat brain and insect sodium channels. J. Biol. Chem. 271:1996;8034-8045.
31. Gordon D., Savarin P., Gurevitz M., Zinn-Justin S. Functional anatomy of scorpion toxins affecting sodium channels. J. Toxicol. Toxin Rev. 17:1998;131-159.
32. Gordon D., Zlotkin E. Binding of an α-scorpion toxin to insect sodium channels is not dependent on membrane potential. FEBS Lett. 315:1993;125-128.
33. Graudins A., Wilson D., Alewood P.F., Broady K.W., Nicholson G.M. Cross-reactivity of Sydney funnel-web spider antivenom: neutralization of the in vitro toxicity of other Australian funnel-web (Atrax and Hadronyche) spider venoms. Toxicon. 40:2002;259-266.
34. Gray M.R. Aspects of the systematics of the Australian funnel web spiders (Araneae: Hexathelidae: Atracinae) based upon morphological and electrophoretic data. Austin A.D., Heather N.W. Australian Arachnology. 1988;113-125 The Australian Entomological Society, Brisbane.
35. Gregson R.P., Spence I. Isolation and characterization of a protein neurotoxin from the venom glands of the funnel-web spider (Atrax robustus). Comp. Biochem. Physiol. C. 74:1983;125-132.
36. + channels. J. Exp. Biol. 204:2001;711-721.
37. Gunning S.J., Chong Y., Khalife A.A., Hains P.G., Broady K.W., Nicholson G.M. Isolation of δ-missulenatoxin-Mb1a, the major vertebrate-active spider δ-toxin from the venom of Missulena bradleyi (Actinopodidae). FEBS Lett. 554:2003;211-218.
38. Gurevitz M., Gordon D., Ben-Natan S., Turkov M., Froy O. Diversification of neurotoxins by C-tail 'wiggling': a scorpion recipe for survival. FASEB J. 15:2001;1201-1205.
39. Hanck D.A., Sheets M.F. Modification of inactivation in cardiac sodium channels: ionic current studies with anthopleurin-A toxin. J. Gen. Physiol. 106:1995;601-616.
40. Harrington A.P., Raven R.J., Bowe P.C., Hawdon G.M., Winkel K.D. Funnel-web spider (Hadronyche infensa) envenomations in coastal south-east Queensland. Med. J. Aust. 171:1999;651-653.
41. Hill J.M., Alewood P.F., Craik D.J. Solution structure of the sodium channel antagonist conotoxin GS: a new molecular caliper for probing sodium channel geometry. Structure. 5:1997;571-583.
42. v1.3-specific immunosuppressive polypeptide. J. Biol. Chem. 273:1998;32697-32707.
43. Khera P.K., Blumenthal K.M. Importance of highly conserved anionic residues and electrostatic interactions in the activity and structure of the cardiotonic polypeptide anthopleurin B. Biochemistry. 35:1996;3503-3507.
44. Kim J.I., Konishi S., Iwai H., Kohno T., Gouda H., Shimada I., Sato K., Arata Y. Three-dimensional solution structure of the calcium channel antagonist ω-agatoxin IVA; consensus molecular folding of calcium channel blockers. J. Mol. Biol. 250:1995;659-671.
45. King G.F., Tedford H.W., Maggio F. Structure and function of insecticidal neurotoxins from Australian funnel-web spiders. J. Toxicol. Toxin Rev. 21:2002;359-389.
46. Kobayashi K., Sasaki T., Sato K., Kohno T. Three-dimensional solution structure of ω-conotoxin TxVII, an L-type calcium channel blocker. Biochemistry. 39:2000;14761-14767.
47. Kohno T., Sasaki T., Kobayashi K., Fainzilber M., Sato K. Three-dimensional solution structure of the sodium channel agonist/antagonist δ-conotoxin TxVIA. J. Biol. Chem. 277:2002;36387-36391.
48. Little M.J., Wilson H., Zappia C., Cestèle S., Tyler M.I., Martin-Eauclaire M.-F., Gordon D., Nicholson G.M. δ-Atracotoxins from Australian funnel-web spiders compete with scorpion α-toxin binding on both rat brain and insect sodium channels. FEBS Lett. 439:1998;246-252.
49. Little M.J., Zappia C., Gilles N., Connor M., Tyler M.I., Martin-Eauclaire M.-F., Gordon D., Nicholson G.M. 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.
50. Martin-Eauclaire M.-F., Courand F. Scorpion neurotoxins: effects and mechanisms. Chang L.W., Dyer R.S. Handbook of Neurotoxicology. 1995;683-716 Marcel Dekker, New York.
51. Miller M.K., Whyte I.M., White J., Keir P.M. Clinical features and management of Hadronyche envenomation in man. Toxicon. 38:2000;409-427.
52. Monks S.A., Pallaghy P.K., Scanlon M.J., Norton R.S. Solution structure of the cardiostimulant polypeptide anthopleurin-B and comparison with anthopleurin-A. Structure. 3:1995;791-803.
53. Mylecharane E.J., Spence I., Sheumack D.D., Claassens R., Howden M.E.H. Actions of robustoxin, a neurotoxic polypeptide from the venom of the male funnel-web spider (Atrax robustus), in anaesthetized monkeys. Toxicon. 27:1989;481-492.
54. Naranjo D. Inhibition of single Shaker K channels by κ-conotoxin- PVIIA. Biophys. J. 82:2002;3003-3011.
55. Nicholson G.M., Walsh R., Little M.J., Tyler M.I. Characterisation of the effects of robustoxin, the lethal neurotoxin from the Sydney funnel-web spider Atrax robustus, on sodium channel activation and inactivation, Pflügers Archiv. Eur. J. Physiol. 436:1998;117-126.
56. Nicholson G.M., Willow M., Howden M.E.H., Narahashi T. Modification of sodium channel gating and kinetics by versutoxin from the Australian funnel-web spider Hadronyche versuta, Pflügers Archiv. Eur. J. Physiol. 428:1994;400-409.
57. Nielsen K.J., Thomas L., Lewis R.J., Alewood P.F., Craik D.J. A consensus structure for ω-conotoxins with different selectivities for voltage-sensitive calcium channel subtypes: comparison of MVIIA, SVIB and SNX-202. J. Mol. Biol. 263:1996;297-310.
58. Norton R.S., Pallaghy P.K. The cystine knot structure of ion channel toxins and related polypeptides. Toxicon. 36:1998;1573-1583.
59. Omecinsky D.O., Holub K.E., Adams M.E., Reily M.D. Three-dimensional structure analysis of μ-agatoxins: further evidence for common motifs among neurotoxins with diverse ion channel specificities. Biochemistry. 35:1996;2836-2844.
60. Oswald R.E., Suchyna T.M., McFeeters R., Gottlieb P., Sachs F. Solution structure of peptide toxins that block mechanosensitive ion channels. J. Biol. Chem. 277:2002;34443-34450.
61. Pallaghy P.K., Alewood D., Alewood P.F., Norton R.S. Solution structure of robustoxin, the lethal neurotoxin from the funnelweb spider Atrax robustus. FEBS Lett. 419:1997;191-196.
62. Pallaghy P.K., Neilsen K.J., Craik D.J., Norton R.S. 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.
63. Pallaghy P.K., Norton R.S. Refined solution structure of ω-conotoxin GVIA: implications for calcium channel binding. J. Peptide Res. 53:1999;343-351.
64. Peng K., Shu Q., Liu Z., Liang S. Function and solution structure of huwentoxin-IV, a potent neuronal tetrodotoxin (TTX)-sensitive sodium channel antagonist from Chinese bird spider Selenocosmia huwena. J. Biol. Chem. 277:2002;47564-47571.
65. Phillips C.A., Spence I., Mylecharane E.J., Brown M.R., Sheumack D.D., Claassens R., Howden M.E.H. The effects of the venom from the Blue Mountains funnel-web spider (Atrax versutus) in anaesthetized monkeys. Clin. Exp. Pharmacol. Physiol. Suppl. 10:1987;14-15.
66. Qu Y., Liang S., Ding J., Liu X., Zhang R., Gu X. Proton nuclear magnetic resonance studies on huwentoxin-I from the venom of the spider Selenocosmia huwena: 2. Three-dimensional structure in solution. J. Protein Chem. 16:1997;565-574.
67. Rash L.D., Hodgson W.C. Pharmacology and biochemistry of spider venoms. Toxicon. 40:2002;225-254.
68. Ray R., Morrow C.S., Catterall W.A. Binding of scorpion toxin to receptor sites associated with voltage-sensitive sodium channels in synaptic nerve ending particles. J. Biol. Chem. 253:1978;7307-7313.
69. Reily M.D., Thanabal V., Adams M.E. The solution structure of ω-Aga-IVB, a P-type calcium channel antagonist from venom of the funnel web spider, Agelenopsis aperta. J. Biomol. NMR. 5:1995;122-132.
70. + channel α subunit. J. Biol. Chem. 271:1996;15950-15962.
71. Rosengren K.J., Wilson D., Daly N.L., Alewood P.F., Craik D.J. Solution structures of the cis- and trans-Pro30 isomers of a novel 38-residue toxin from the venom of Hadronyche infensa sp. that contains a cystine-knot motif within its four disulfide bonds. Biochemistry. 41:2002;3294-3301.
72. Sautière P., Cestèle S., Kopeyan C., Martinage A., Drobecq H., Doljansky Y., Gordon D. New toxins acting on sodium channels from the scorpion Leiurus quinquestriatus hebraeus suggest a clue to mammalian vs insect selectivity. Toxicon. 36:1998;1141-1154.
73. Sheumack D.D., Baldo B.A., Carroll P.R., Hampson F., Howden M.E., Skorulis A. A comparative study of properties and toxic constituents of funnel web spider (Atrax) venoms. Comp. Biochem. Physiol. C. 78:1984;55-68.
74. Sheumack D.D., Claassens R., Whiteley N.M., Howden M.E.H. Complete amino acid sequence of a new type of lethal neurotoxin from the venom of the funnel-web spider Atrax robustus. FEBS Lett. 181:1985;154-156.
75. Sheumack D.D., Comis A., Claassens R., Mylecharane E.J., Spence I., Howden M.E.H. An endogenous antitoxin to the lethal venom of the funnel web spider, Atrax robustus, in rabbit sera. Comp. Biochem. Physiol. 99C:1991;157-161.
76. Strichartz G.R., Wang G.K. Rapid voltage-dependent dissociation of scorpion α-toxins coupled to Na channel inactivation in amphibian myelinated nerves. J. Gen. Physiol. 88:1986;413-435.
77. Sutherland S.K. Antivenom to the venom of the male Sydney funnel-web spider Atrax robustus. Preliminary report. Med. J. Aust. 2:1980;437-441.
78. Sutherland S.K., Tibballs J. The genera Atrax and Hadronyche, funnel-web spiders, Australian animal toxins: the creatures, their toxins and care of the poisoned patient. 2001;Oxford University Press, Melbourne. pp. 402-464.
79. Szeto T.H., Birinyi-Strachan L.C., Wang X.-H., Smith R., Connor M., Christie M.J., King G.F., Nicholson G.M. Isolation and pharmacological characterisation of δ-atracotoxin-Hv1b, a vertebrate-selective sodium channel toxin. FEBS Lett. 470:2000a;293-299.
80. Szeto, T.H., Wang, X.-H., Smith, R., Connor, M., Christie, M.J., Nicholson, G.M., King, G.F., 2000b. Isolation of a funnel web spider polypeptide with homology to mamba intestinal toxin 1 and the embryonic head inducer Dickkopf1. Toxicon 38, 429-442.
81. + channels: common surface features of gating modifier toxins. J. Mol. Biol. 297:2000;771-780.
82. 2+ channel. J. Mol. Biol. 321:2002;517.
83. Torda T.A., Loong E., Greaves I. Severe lung oedema and fatal consumption coagulopathy after funnel-web bite. Med. J. Aust. 2:1980;442-444.
84. Tugarinov V., Kustanovich I., Zilberberg N., Gurevitz M., Anglister J. Solution structures of a highly insecticidal recombinant scorpion alpha-toxin and a mutant with increased activity. Biochemistry. 36:1997;2414-2424.
85. Wang X.-H., Connor M., Smith R., Maciejewski M.W., Howden M.E.H., Nicholson G.M., Christie M.J., King G.F. Discovery and characterization of a family of insecticidal neurotoxins with a rare vicinal disulfide bridge. Nat. Struct. Biol. 7:2000;505-513.
86. Wang X.-H., Connor M., Wilson D., Wilson H., Nicholson G.M., Smith R., Shaw D., Mackay J.P., Alewood P.F., Christie M.J., King G.F. Biopesticide panning: discovery of a potent and highly specific peptide antagonist of insect calcium channels. J. Biol. Chem. 276:2001;40306-40312.
87. Wang X.-H., Smith R., Fletcher J.I., Wilson H., Wood C.J., Howden M.E.H., King G.F. Structure-function studies of omega-atracotoxin, a potent antagonist of insect voltage-gated calcium channels. Eur. J. Biochem. 264:1999;488-494.
88. White J., Carduso J.L., Fan H.W. Clinical toxicology of spider bites. Meier J., White J. Handbook of Clinical Toxicology of Animal Venoms and Poisons. 1995;259-329 CRC Press, New York.
89. Zilberberg N., Froy O., Loret E., Cestèle S., Arad D., Gordon D., Gurevitz M. Identification of structural elements of a scorpion α-neurotoxin important for receptor site recognition. J. Biol. Chem. 272:1997;14810-14816.
90. Zlotkin E., Fishman Y., Elazar M. AaIT: from neurotoxin to insecticide. Biochimie. 82:2000;869-881.