Characterisation of the heterotrimeric presynaptic phospholipase A2 neurotoxin complex from the venom of the common death adder (Acanthophis antarcticus)

Biochemical Pharmacology

Volumn 80, Issue 2, 2010, Pages 277-287

  Blacklow, Benjamin ^a   Escoubas, Pierre ^b   Nicholson, Graham M ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

Acanthophis antarcticus; Death adder; Phospholipase A2; Presynaptic snake neurotoxin; SPAN; Taipoxin

Indexed keywords

4 BROMOPHENACYL BROMIDE; ACETYLCHOLINE; CHOLINERGIC RECEPTOR STIMULATING AGENT; NEUROTOXIN; PHOSPHOLIPASE A2; POTASSIUM CHLORIDE; SNAKE VENOM; SNAKE VENOM ANTISERUM; SURAMIN; TAIPOXIN;

ACANTHOPHIS ANTARCTICUS; ACETYLCHOLINE RELEASE; ALPHA CHAIN; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BETA CHAIN; BINDING AFFINITY; CHICK; COMMON DEATH ADDER; CONTROLLED STUDY; ENVENOMATION; ENZYME ACTIVITY; ENZYME INHIBITION; GEL PERMEATION CHROMATOGRAPHY; MOLECULAR WEIGHT; MUSCLE CONTRACTION; MUSCLE TETANIC CONTRACTION; NERVE; NERVE ENDING; NEUROMUSCULAR BLOCKING; NEUROTOXICITY; NONHUMAN; POISONOUS SNAKE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; STOICHIOMETRY;

ANIMALS; BIOLOGICAL ASSAY; CHICKENS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELAPID VENOMS; ELAPIDAE; MUSCLE CONTRACTION; NEUROMUSCULAR JUNCTION; NEUROTOXINS; PHOSPHOLIPASES A2; PRESYNAPTIC TERMINALS; RECEPTORS, PRESYNAPTIC; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 77952673300     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.03.030     Document Type: Article

References (60)

1. Wüster W., Dumbrell A.J., Hay C., Pook C.E., Williams D.J., Fry B.G. Snakes across the Strait: trans-Torresian phylogeographic relationships in three genera of Australasian snakes (Serpentes: Elapidae: Acanthophis, Oxyuranus, and Pseudechis). Mol Phylogenet Evol 2005, 34:1-14.
2. Lalloo D.G., Trevett A.J., Black J.A., Mapao J., Saweri A., Naraqi S., et al. Neurotoxicity, anticoagulant activity and evidence of rhabdomyolysis in patients bitten by death adders (Acanthophis sp.) in southern Papua New Guinea. QJM 1996, 89:25-35.
3. Campbell C.H. The death adder (Acanthophis antarcticus): the effect of the bite and its treatment. Med J Aust 1966, 2:922-925.
4. Kellaway C.H. The actions of venoms of the copper-head (Denisonia superba) and of the death adder (Acanthophis antarcticus) on the coagulation of the blood. Med J Aust 1929, 1:772-781.
5. Doery H.M., Pearson J.E. Haemolysins in venoms of Australian snakes. Observations on the haemolysins of the venoms of some Australian snakes and the separation of phospholipase A from the venom of Pseudechis porphyriacus. Biochem J 1961, 78:820-827.
6. Sutherland S.K., Tibballs J. Genus Acanthophis, death adders. Australian animal toxins: the creatures, their toxins and care of the poisoned patient 2001, Oxford University Press, Melbourne, p.160-6.
7. Mebs D., Samejima Y. Purification, from Australian elapid venoms, and properties of phospholipases A which cause myoglobinuria in mice. Toxicon 1980, 18:443-454.
8. Wickramaratna J.C., Fry B.G., Hodgson W.C. Species-dependent variations in the in vitro myotoxicity of death adder (Acanthophis) venoms. Toxicol Sci 2003, 74:352-360.
9. Currie B.J. Snakebite in Australia: moving from anecdotes to prospective studies. Emerg Med (Fremantle) 2003, 15:406-408.
10. Currie B.J. Urban envenomation. Med J Aust 1989, 151:724.
11. Currie B.J. Treatment of snakebite in Australia: the current evidence base and questions requiring collaborative multicentre prospective studies. Toxicon 2006, 48:941-956.
12. White J. Envenoming and antivenom use in Australia. Toxicon 1998, 36:1483-1492.
13. White J. CSL antivenom handbook 2001, CSL Ltd., Melbourne.
14. Isbister G.K., O'Leary M.A., Hagan J., Nichols K., Jacoby T., Davern K., et al. Cross-neutralisation of Australian brown snake, taipan and death adder venoms by monovalent antibodies. Vaccine 2010, 28:798-802.
15. Gunja N., Ling M., Dowsett R., Murray L., Isbister G.K. Antivenom and neostigmine failure in death adder envenoming. Clin Toxicol 2007, 45:389.
16. Wickramaratna J.C., Hodgson W.C. A pharmacological examination of venoms from three species of death adder (Acanthophis antarcticus, Acanthophis praelongus and Acanthophis pyrrhus). Toxicon 2001, 39:209-216.
17. Kuruppu S., Smith A.I., Isbister G.K., Hodgson W.C. Neurotoxins from Australo-Papuan elapids: a biochemical and pharmacological perspective. Crit Rev Toxicol 2008, 38:73-86.
18. Rossetto O., Montecucco C. Presynaptic neurotoxins with enzymatic activities. Handb Exp Pharmacol 2008, 129-170.
19. Wilson H.I., Nicholson G.M., Tyler M.I., Howden M.E. Induction of giant miniature end-plate potentials during blockade of neuromuscular transmission by textilotoxin. Naunyn-Schmiedeberg's Arch Pharmacol 1995, 352:79-87.
20. Kelly R., Brown F. Biochemical and physiological properties of a purified snake venom neurotoxin which acts presynaptically. J Neurobiol 1974, 5:135-150.
21. Blacklow B., Konstantakopoulos N., Hodgson W.C., Nicholson G.M. Presence of presynaptic neurotoxin complexes in the venoms of Australo-Papuan death adders (Acanthophis spp.). Toxicon 2010, 55:1171-1180.
22. Chippaux J.P., Williams V., White J. Snake venom variability: methods of study, results and interpretation. Toxicon 1991, 29:1279-1303.
23. Ginsborg B.L., Warriner J. The isolated chick biventer cervicis nerve-muscle preparation. Brit J Pharmacol Chemother 1960, 15:410-411.
24. Harvey A.L., Barfaraz A., Thomson E., Faiz A., Preston S., Harris J.B. Screening of snake venoms for neurotoxic and myotoxic effects using simple in vitro preparations from rodents and chicks. Toxicon 1994, 32:257-265.
25. Caccin P., Rigoni M., Bisceglie A., Rossetto O., Montecucco C. Reversible skeletal neuromuscular paralysis induced by different lysophospholipids. FEBS Lett 2006, 580:6317-6321.
26. Hodgson W.C., Dal Belo C.A., Rowan E.G. The neuromuscular activity of paradoxin: a presynaptic neurotoxin from the venom of the inland taipan (Oxyuranus microlepidotus). Neuropharmacology 2007, 52:1229-1236.
27. Wood S.J., Slater C.R. Safety factor at the neuromuscular junction. Prog Neurobiol 2001, 64:393-429.
28. 2 isolated from Bothrops asper and Bothrops godmani snake venoms: effects on enzymatic and pharmacological properties. Toxicon 1997, 35:241-252.
29. Chu C.C., Li S.H., Chen Y.H. Resolution of isotoxins in the β-bungarotoxin family. J Chromatogr A 1995, 694:492-497.
30. Aquilina J.A. The major toxin from the Australian Common Brown Snake is a hexamer with unusual gas-phase dissociation properties. Proteins 2009, 75:478-485.
31. King G.F., Gentz M.C., Escoubas P., Nicholson G.M. A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon 2008, 52:264-276.
32. 2 activity (β-bungarotoxin, taipoxin, crotoxin). Toxicon 1984, 22:631-640.
33. Lumsden N.G., Fry B.G., Ventura S., Kini R.M., Hodgson W.C. Pharmacological characterisation of a neurotoxin from the venom of Boiga dendrophila (mangrove catsnake). Toxicon 2005, 45:329-334.
34. Kuruppu S., Fry B.G., Hodgson W.C. Presynaptic neuromuscular activity of venom from the brown-headed snake (Furina tristis). Toxicon 2005, 45:383-388.
35. Kuruppu S., Reeve S., Banerjee Y., Kini R.M., Smith A.I., Hodgson W.C. Isolation and pharmacological characterization of cannitoxin, a presynaptic neurotoxin from the venom of the Papuan Taipan (Oxyuranus scutellatus canni). J Pharmacol Exp Ther 2005, 315:1196-1202.
36. Wilson H.I., Nicholson G.M. Presynaptic snake β-neurotoxins produce tetanic fade and endplate potential run-down during neuromuscular blockade in mouse diaphragm. Naunyn-Schmiedeberg's Arch Pharmacol 1997, 356:626-634.
37. de Oliveira M., Cavalcante W.L., Arruda E.Z., Melo P.A., Dal-Pai Silva M., Gallacci M. Antagonism of myotoxic and paralyzing activities of bothropstoxin-I by suramin. Toxicon 2003, 42:373-379.
38. Lin-Shiau S.Y., Lin M.J. Suramin inhibits the toxic effects of presynaptic neurotoxins at the mouse motor nerve terminals. Eur J Pharmacol 1999, 382:75-80.
39. Kelly R.B., Brown F.R. Biochemical and physiological properties of a purified snake venom neurotoxin which acts presynaptically. J Neurobiol 1974, 5:135-150.
40. Chu C.C., Li S.H., Chen Y.H. Resolution of isotoxins in the beta-bungarotoxin family. J Chromatogr A 1995, 694:492-497.
41. Fohlman J., Eaker D., Karlsson E., Thesleff S. Taipoxin, an extremely potent presynaptic neurotoxin from the venom of the Australian snake taipan (Oxyuranus s. scutellatus). Isolation, characterization, quaternary structure and pharmacological properties. Eur J Biochem 1976, 68:457-469.
42. Pearson J.A., Tyler M.I., Retson K.V., Howden M.E. Studies on the subunit structure of textilotoxin, a potent presynaptic neurotoxin from the venom of the Australian common brown snake (Pseudonaja textilis). 3. The complete amino-acid sequences of all the subunits. Biochim Biophys Acta 1993, 1161:223-229.
43. Volwerk J.J., Pieterson W.A., de Haas G.H. Histidine at the active site of phospholipase A2. Biochemistry 1974, 13:1446-1454.
44. Dixon R.W., Harris J.B. Myotoxic activity of the toxic phospholipase, notexin, from the venom of the Australian tiger snake. J Neuropathol Exp Neurol 1996, 55:1230-1237.
45. Chang C.C., Chen T.F., Lee C.Y. Studies of the presynaptic effect of β-bungarotoxin on neuromuscular transmission. J Pharmacol Exp Ther 1973, 184:339-345.
46. Kamenskaya M., Thesleff S. Effects of taipoxin on spontaneous and evoked transmitter release from motor nerve terminals. Toxicon 1979, 17(Suppl. 80).
47. Harris J.B., Karlsson E., Thesleff S. Effects of an isolated toxin from Australian Tiger snake (Notechis scutatus scutatus) venom at the mammalian neuromuscular junction. Brit J Pharmacol 1973, 47:141-146.
48. Chang C.C., Lee J.D. Crotoxin, the neurotoxin of South American rattlesnake venom, is a presynaptic toxin acting like β-bungarotoxin. Naunyn-Schmiedeberg's Arch Pharmacol 1977, 296:159-168.
49. Fohlman J. Comparison of two highly toxic Australian snake venoms: the taipan (Oxyuranus s. scutellatus) and the fierce snake (Parademansia microlepidotus). Toxicon 1979, 17:170-172.
50. Montecucco C., Rossetto O. On the quaternary structure of taipoxin and textilotoxin: The advantage of being multiple. Toxicon 2008, 51:1560-1562.
51. Mammen M., Choi S.K., Whitesides G.M. Polyvalent interaction in biological system: implications for design and use of multivalent ligands and inhibitors. Angew Chem Int Ed 1998, 37:2754-2794.
52. Chang C., Su M. Presynaptic toxicity of the histidine-modified, phospholipase A2-inactive, ß-bungarotoxin, crotoxin and notexin. Toxicon 1982, 20:895-905.
53. Fohlman J., Eaker D., Dowdall M.J., Lullmann-Rauch R., Sjodin T., Leander S. Chemical modification of taipoxin and the consequences for phospholipase activity, pathophysiology, and inhibition of high-affinity choline uptake. Eur J Biochem 1979, 94:531-540.
54. 2 suggest allosteric coupling between membrane binding and catalytic sites. Biophys J 2003, 84:1773-1783.
55. 2: the N-terminal region is more important than enzymatic activity. Biochemistry 2006, 45:5800-5816.
56. Cheah L.S., Gwee M.C.E. Train-of-four fade during neuromuscular blockade induced by tubocurarine, succinylcholine or α-bungarotoxin in the rat isolated hemidiaphragm. Clin Exp Pharmacol Physiol 1988, 15:937-943.
57. Faria M., Oliveira L., Timóteo M.A., Lobo M.G., Correia-De-Sá P. Blockade of neuronal facilitatory nicotinic receptors containing α3β2 subunits contribute to tetanic fade in the rat isolated diaphragm. Synapse 2003, 49:77-88.
58. Correia-de-Sá P., Sebastião A.M., Ribeiro J.A. Inhibitory and excitatory effects of adenosine receptor agonists on evoked transmitter release from phrenic nerve ending of the rat. Br J Pharmacol 1991, 103:1614-1620.
59. Montecucco C., Rossetto O., Caccin P., Rigoni M., Carli L., Morbiato L., et al. Different mechanisms of inhibition of nerve terminals by botulinum and snake presynaptic neurotoxins. Toxicon 2009, 54:561-564.
60. Oshima-Franco Y., Leite G.B., Silva G.H., Cardoso D.F., Hyslop S., Giglio J.R., et al. Neutralization of the pharmacological effects of bothropstoxin-I from Bothrops jararacussu (jararacucu) venom by crotoxin antiserum and heparin. Toxicon 2001, 39:1477-1485.