Spider and wasp neurotoxins: Pharmacological and biochemical aspects

European Journal of Pharmacology

Volumn 493, Issue 1-3, 2004, Pages 1-17

  Beleboni, Renê De O ^a   Pizzo, Andrea B ^a   Fontana, Andréia C K ^b   Carolino, Ruither De O G ^a   Coutinho Netto, Joaquim ^a   Dos Santos, Wagner F ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Ion channel; Neurotoxin; Receptor; Spider; Transporter and Neurotransmitter release; Wasp

Indexed keywords

ALPHA POMPILIDOTOXIN; ARGIOTOXIN 636; BETA POMPILIDOTOXIN; DELTA ATRACOTOXIN; DELTA PALUTOXIN IT1; DELTA PALUTOXIN IT2; DELTA PALUTOXIN IT3; DELTA PALUTOXIN IT4; HANATOXIN 1; HANATOXIN 2; HETEROPODATOXIN 1; HETEROPODATOXIN 2; HETEROPODATOXIN 3; HUWENTOXIN 4; ION CHANNEL; MU AGATOXIN I; MU AGATOXIN II; MU AGATOXIN III; MU AGATOXIN IV; NEUROTOXIN; OMEGA AGATOXIN IA; OMEGA AGATOXIN IIA; PHRIXOTOXIN 1; PHRIXOTOXIN 2; ROBUSTOXIN; SODIUM CHANNEL; SPIDER VENOM; STROMATOXIN 1; TETRODOTOXIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VERSUTOXIN; WASP VENOM;

INHIBITION KINETICS; MEMBRANE TRANSPORT; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SPIDER; TRANSPORT KINETICS; WASP;

ANIMALS; BRAZIL; HUMANS; ION CHANNEL GATING; NEUROTOXINS; SODIUM CHANNELS; SPIDER VENOMS; WASP VENOMS;

EID: 2942581318     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2004.03.049     Document Type: Review

References (188)

1. Abe T., Kawai N., Niwa A. Purification and properties of a presynaptically acting neurotoxin, mandaratoxin, from hornet (Vespa mandarinia). Biochemistry. 21:1982;1693-1697
2. Adams M.E., Carney R.L., Enderlin F.E., Fu E.T., Jarema M.A., Li J.P., Miller C.A., Schooley D.A., Shapiro M.J., Venema V.J. Structures and biological activities of three synaptic antagonists from orb weaver spider venom. Biochem. Biophys. Res. Commun. 148:1987;678-683
3. Adams M.E., Herold E.E., Venema V.J. Two classes of channel-specific toxins from funnel web spider venom. J. Comp. Physiol., A. 164:1989;333-342
4. Adams M.E., Bindokas V.P., Hasegawa L., Venema V.J. ω-Agatoxins: novel calcium channel antagonists of two subtypes from funnel web spider (Agelenopsis aperta) venom. J. Biol. Chem. 265:1990;861-867
5. Amara S.G., Fontana A.C. Excitatory amino acid transporters: keeping up with glutamate. Neurochem. Int. 41:2002;313-318
6. Attwell D., Barbour B., Szatkowski M. Nonvesicular release of neurotransmitter. Neuron. 11:1993;401-407
7. 2+ channels are coupled to adrenaline and noradrenaline release in bovine adrenal chromaffin cells. Pflugers. Arch. 434:1997;592-598
8. 2+. Pflugers. Arch. 432:1996;1039-1046
9. Bean B.P. Classes of calcium channels in vertebrate cells. Annu. Rev. Physiol. 51:1989;367-384
10. Bear M.F., Connors B.W., Paradiso M.A. Neuroscience: Exploring the Brain. first ed. 1996;Williams and Wilkins, Canada
11. Bergles D.E., Roberts J.D., Somogyi P., Jahr C.E. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature. 405:2000;187-191
12. Bernard C., Legros C., Ferrat G., Bischoff U., Marquardt A., Pongs O., Darbon H. Solution structure of HpTX2, a toxin from Heteropoda venatoria spider that blocks Kv4.2 potassium channel. Protein Sci. 9:2000;2059-2067
13. Birnbaumer L., Qin N., Olcese R., Tareilus E., Platano D., Costantin J., Stefani E. Structures and functions of calcium channel beta subunits. J. Bioenerg. Biomembr. 30:1998;357-375
14. Blagbrough I.S., Brackley P.T., Bruce M., Bycroft B.W., Mather A.J., Millington S., Sudan H.L., Usherwood P.N. Arthropod toxins as leads for novel insecticides: an assessment of polyamine amides as glutamate antagonists. Toxicon. 30:1992;303-322
15. Blagbrough I.S., Moya E., Taylor S. Polyamines and polyamine amides from wasps and spiders. Biochem. Soc. Trans. 22:1994;888-893
16. Blagbrough I.S., Moya E., Walford S.P. Practical, convergent total synthesis of polyamine amide spider toxin NSTX-3. Tetrahedron Lett. 37:1996;551-554
17. Bloomquist J.R., Kinne L.P., Deutsch V., Simpson S.F. Mode of action of an insecticidal peptide toxin from the venom of a weaving spider (Diguetia canities). Toxicon. 34:1996;1072-1075
18. Blum M.S. Chemical Defenses in Arthropods. 1981;562 Academic Press, New York, NY
19. Bowers C.W., Phillips H.S., Lee P., Jan Y.N., Jan L.Y. Identification and purification of an irreversible presynaptic neurotoxin from the venom of the spider Hololena curta. Proc. Natl. Acad. Sci. U. S. A. 84:1987;3506-3510
20. Brackley P.T., Bell D.R., Choi S.K., Nakanishi K., Usherwood P.N.J. Selective antagonism of native and cloned kainate and NMDA-R by polyamine toxins. Pharmacol. Exp. Ther. 266:1993;1573-1580
21. Branton W.D., Kolton L., Jan Y., Jan L.Y. Neurotoxins from Plectreurys spider venom are potent presynaptic blockers in Drosophila. J. Neurosci. 7:1987;4195-4200
22. Brown M.R., Sheumack D.D., Tyler M.I., Howden M.E. Amino acid sequence of versutoxin, a lethal neurotoxin from the venom of the funnel-web spider Atrax versutus. Biochem. J. 250:1988;401-405
23. Burmistrov Y.M., Shuranova Z.P., Artiukhina N.I. Effects of black widow spider venom and latrocrustatoxin on crustacean nerve cells: electrophysiological and ultrastructural study. Gen. Pharmacol. 28:1997;159-166
24. Cairrão M.A.R., Ribeiro A.M., Pizzo A.B., Fontana A.C.K., Beleboni R.O., Coutinho-Netto J., Miranda A., Santos W.F. Anticonvulsant and GABA uptake inhibition properties of venom fractions from the spiders Parawixia bistriata and Scaptocosa raptoria. Pharm. Biol. 40:2002;472-477
25. + channels. Toxicon. 41:2003;305-313
26. Cassola A.C., Jaffe H., Fales H.M., Castro A.S., Magnoli F., Cipolla-Neto J. ω-Phonetoxin-IIA: a calcium channel blocker from the spider Phoneutria nigriventer. Pflugers Arch. 436:1998;545-552
27. Catterall W.A. Structure and function of voltage-gated ion channels. Annu. Rev. Biochem. 64:1995;493-531
28. Catterall W.A., Beneski D.A. Interaction of polypeptide neurotoxins with a receptor site associated with voltage-sensitive sodium channels. J. Supramol. Struct. 14:1980;295-303
29. Catterral W.A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron. 26:2000;13-25
30. Cavalieri M., D'Urso D., Lassa A., Pierdominici E., Robello M., Grasso A. Characterization and some properties of the venom gland extract of a theridiid spider (Steatoda paykulliana) frequently mistaken for black widow spider (Latrodectus tredecimguttatus). Toxicon. 25:1987;965-974
31. Cestele S., Catterall W.A. Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie. 82:2000;883-892
32. Clark R.B., Donaldson P.L., Gration K.A., Lambert J.J., Piek T., Ramsey R., Spanjer W., Usherwood P.N. Block of locust muscle glutamate receptors by δ-PTX occurs after receptor activations. Brain Res. 241:1982;105-114
33. + channels. Ann. N.Y. Acad. Sci. 868:1990;233-285
34. Collingridge G.L., Lester R.A. Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol. Rev. 41:1989;143-210
35. Conn P.J., Pin J.P. Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37:1997;205-237
36. Corzo G., Escoubas P., Stankiewicz M., Pelhate M., Kristensen C.P., Nakajima T. Isolation, synthesis and pharmacological characterization of δ-palutoxins IT, novel insecticidal toxins from the spider Paracoelotes luctuosus (Amaurobiidae). Eur. J. Biochem. 267:2000;5783-5795
37. Coutinho V., Knopfel T. Metabotropic glutamate receptors: electrical and chemical signaling properties. Neuroscientist. 8:2002;551-561
38. Coutinho-Netto J., Abdul-Ghani A.S., Collins J.F., Bradford H.F. Is glutamate a trigger factor in epileptic hyperactivity? Epilepsia. 22:1981;289-296
39. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 65:2001;1-105
40. 2+-independent α-latrotoxin-binding protein. J. Biol. Chem. 271:1996;23239-23245
41. 2+. EMBO J. 17:1998;3909-3920
42. De Figueiredo S.G., de Lima M.E., Cordeiro M.N., Diniz C.R., Patten D., Halliwell R.F., Gilroy J., Richardson M. Purification and amino acid sequence of a highly insecticidal toxin from the venom of the Brazilian spider Phoneutria nigriventer which inhibits NMDA-evoked currents in rat hippocampal neurons. Toxicon. 39:2001;309-317
43. Diochot S., Drici M.D., Moinier D., Fink M., Lazdunski M. Effects of phrixotoxins on the Kv4 family of potassium channels and implications for the role of Ito1 in cardiac electrogenesis. Br. J. Pharmacol. 126:1999;251-263
44. + channels. J. Bioenerg. Biomembr. 28:1996;231-253
45. Dos Santos R.G., Van Renterghem C., Martin-Moutot N., Mansuelle P., Cordeiro M.N., Diniz C.R., Mori Y., De Lima M.E., Seagar M. Phoneutria nigriventer ω-phonetoxin IIA blocks the Cav2 family of calcium channels and interacts with ω-conotoxin-binding sites. J. Biol. Chem. 277:2002;13856-13862
46. Draguhn A., Jahn W., Witzemann V. Argiotoxin636 inhibits NMDA-activated ion channels expressed in Xenopus oocytes. Neurosci. Lett. 132:1991;187-190
47. 2+ channels coupled to catecholamine release in bovine adrenal chromaffin cells. J. Neurochem. 60:1993;908-913
48. Eldefrawi A.T., Eldefrawi M.E., Konno K., Mansour N.A., Nakanishi K., Oltz E., Usherwood P.N. Structure and synthesis of a potent glutamate receptor antagonist in wasp venom. Proc. Natl. Acad. Sci. U. S. A. 85:1988;4910-4913
49. Elrick D.B., Charlton M.P. α-Latrocrustatoxin increases neurotransmitter release by activating a calcium influx pathway at crayfish neuromuscular junction. J. Neurophysiol. 82:1999;3550-3562
50. Ertel E.A., Campbell K.P., Harpold M.M., Hofmann F., Mori Y., Perez-Reyes E., Schwartz A., Snutch T.P., Tanabe T., Birnbaumer L., Tsien R.W., Catterall W.A. Nomenclature of voltage-gated calcium channels. Neuron. 25:2000;533-535
51. Escoubas P., Diochot S., Celerier M.L., Nakajima T., Lazdunski M. Novel tarantula toxins for subtypes of voltage-dependent potassium channels in the Kv2 and Kv4 subfamilies. Mol. Pharmacol. 62:2002;48-57
52. Fagni L., Bockaert J. Action of argiotoxin636 on N-methyl-D-aspartate channels in cerebellar cells. NeuroReport. 6:1995;1037-1040
53. Finkelstein A., Rubin L.L., Tzeng M.C. Black widow spider venom: effect of purified toxin on lipid bilayer membranes. Science. 193:1976;1009-1011
54. Fletcher J.I., Chapman B.E., Mackay J.P., Howden M.E., King G.F. 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
55. Fonnum F. Glutamate: a neurotransmitter in mammalian brain. J. Neurochem. 42:1984;1-11
56. Fontana A.C., Cairrão M.A., Colusso A.J., Santos W.F., Coutinho-Netto J. Paralyzing activity of the Parawixia bistriata crude venom in termites: a new bioassay. Toxicon. 38:2000;133-138
57. Fontana A.C., Guizzo R., Beleboni R.O., Meirelles E Silva A.R., Coimbra N.C., Amara S.G., dos Santos W.F., Coutinho-Netto J. Purification of a neuroprotective component of Parawixia bistriata spider venom that enhances glutamate uptake. Br. J. Pharmacol. 139:2003;1297-1309
58. 2+ sensor for transmitter release at a central synapse. Cell. 79:1994;717-727
59. Goldin A.L. Resurgence of sodium channel research. Annu. Rev. Physiol. 63:2001;871-894
60. Goldin A.L., Barchi R.L., Caldwell J.H., Hofmann F., Howe J.R., Hunter J.C., Kallen R.G., Mandel G., Meisler M.H., Netter Y.B., Noda M., Tamkun M.M., Waxman S.G., Wood N., Catterall W.A. Nomenclature of voltage-gated sodium channels. Neuron. 28:2000;365-368
61. Green A.C., Nakanishi K., Usherwood P.N. Polyamine amides are neuroprotective in cerebellar granule cell cultures challenged with excitatory amino acids. Brain Res. 717:1996;135-146
62. Guatimosim C., Romano-Silva M.A., Cruz J.S., Beirão P.S., Kalapothakis E., Moraes-Santos T., Cordeiro M.N., Diniz C.R., Gómez M.V., Prado M.A. A toxin from the spider Phoneutria nigriventer that blocks calcium channels coupled to exocytosis. Br. J. Pharmacol. 122:1997;591-597
63. Harvey J., Wedley S., Findlay J.D., Sidell M.R., Pullar I.A. ω-Agatoxin IVA identifies a single calcium channel subtype which contributes to the potassium-induced release of acetylcholine, 5-hydroxytryptamine, dopamine, γ-aminobutyric acid and glutamate from rat brain slices. Neuropharmacology. 35:1996;385-392
64. Harvey A.L., Bradley K.N., Cochran S.A., Rowan E.G., Pratt J.A., Quillfeldt J.A., Jerusalinsky D.A. What can toxins tell us for drug discovery? Toxicon. 36:1998;1635-1640
65. Haspel G., Libersat F. Wasp venom blocks central cholinergic synapses to induce transient paralysis in cockroach prey. J. Neurobiol. 54:2003;628-637
66. Heading C.E. Conus peptides and neuroprotection. Curr. Opin. Invest. Drugs. 3:2002;915-920
67. Henkel A.W., Sankaranarayanan S. Mechanisms of α-latrotoxin action. Cell Tissue Res. 296:1999;229-233
68. Herlitze S., Raditsch M., Ruppersberg J.P., Jahn W., Monyer H., Schoepfer R., Witzemann V. Argiotoxin detects molecular differences in AMPA receptor channels. Neuron. 10:1993;1131-1140
69. Himi T., Saito H., Kawai N., Nakajima T. Spider toxin (JSTX-3) inhibits the convulsions induced by glutamate agonists. J. Neural Transm., Gen. Sect. 80:1990;95-104
70. Hollmann M., Heinemann S. Cloned glutamate receptors. Annu. Rev. Neurosci. 17:1994;31-108
71. Hurlbut W.P., Chieregatti E., Valtorta F., Haimann C. α-Latrotoxin channels in neuroblastoma cells. J. Membr. Biol. 138:1994;91-102
72. Ichtchenko K., Khvotchev M., Kiyatkin N., Simpson L., Sugita S., Sudhof T.C. α-Latrotoxin action probed with recombinant toxin: receptors recruit α-latrotoxin but do not transduce an exocytotic signal. EMBO J. 17:1998;6188-6199
73. Jackson H., Parks T.N. Spider toxins: recent applications in neurobiology. Annu. Rev. Neurosci. 12:1989;405-414
74. Kalapothakis E., Penaforte C.L., Leão R.M., Cruz J.S., Prado V.F., Cordeiro M.N., Diniz C.R., Romano-Silva M.A., Prado M.A., Gomez M.V., Beirao P.S. Cloning, cDNA sequence analysis and patch clamp studies of a toxin from the venom of the armed spider (Phoneutria nigriventer). Toxicon. 36:1998;1971-1980
75. 2+ currents from rat cultured sensory neurones and excitatory post synaptic currents from rat hippocampal slices. Cell Calcium. 30:2001;212-221
76. Kawai N., Niwa A., Abe T. Spider venom contains specific receptor blocker of glutaminergic synapses. Brain Res. 247:1982;169-171
77. Kawai N., Yamagishi S., Saito M., Furuya K. Blockade of synaptic transmission in the squid giant synapse by a spider toxin (JSTX). Brain Res. 278:1983;346-349
78. Kawai N., Miwa A., Shimazaki K., Sahara Y., Robinson H.P., Nakajima T. Spider toxin and the glutamate. Comp. Biochem. Physiol., C. 98:1991;87-95
79. Keith R.A., Mangano T.J., Lampe R.A., DeFeo P.A., Hyde M.J., Donzanti B.A. Comparative actions of synthetic ω-grammotoxin SIA and synthetic ω-Aga-IVA on neuronal calcium entry and evoked release of neurotransmitters in vitro and in vivo. Neuropharmacology. 34:1995;1515-1528
80. Khvotchev M., Sudhof T.C. α-Latrotoxin triggers transmitter release via direct insertion into the presynaptic plasma membrane. EMBO J. 19:2000;3250-3262
81. Kinoshita E., Maejima H., Yamaoka K., Konno K., Kawai N., Shimizu E., Yokote S., Nakayama H., Seyama I. Novel wasp toxin discriminates between neuronal and cardiac sodium channels. Mol. Pharmacol. 59:2001;1457-1463
82. Kiskin N.I., Kryshtal O.A., Tsyndrenko A.Ya., Volkova T.M., Grishin E.V. Argiopine, argiopinines and pseudoargiopinines, blockers of the glutamate receptors in hippocampal neurons. Neirofiziologiia. 21:1989;748-756
83. Kiskin N.I., Chizhmakov I.V., Tsyndrenko A.Ya., Mueller A.L., Jackson H., Krishtal O.A. A highly potent and selective N-methyl-D-aspartate receptor antagonist from the venom of the Agelenopsis aperta spider. Neuroscience. 51:1992;11-18
84. Kobayashi K., Fischer J.B., Knapo A.G., Margolin L., Daly D., Reddy N.L., Roach B., McCormick K., Meinwald J., Goldin S.M. A novel polyamine calcium channel antagonist isolated from venom of the spider Dolomedes okefinokensis. Soc. Neurosci. Abstr. 18:1992;10
85. + channels proteins. Neurosci. Lett. 285:2000;29-32
86. Konno K., Palma M.S., Hitara I.Y., Juliano M.A., Juliano L., Yasuhara T. Identification of bradykinins in solitary wasp venoms. Toxicon. 40:2002;309-312
87. Krasilnikov O.V., Sabirov R.Z. Comparative analysis of latrotoxin channels of different conductance in planar lipid bilayers. Evidence for cluster organization. Biochim. Biophys. Acta. 1112:1992;124-128
88. Krasnoperov V.G., Beavis R., Chepurny O.G., Little A.R., Plotnikov A.N., Petrenko A.G. The calcium-independent receptor of α-latrotoxin is not a neurexin. Biochem. Biophys. Res. Commun. 227:1996;868-875
89. Krasnoperov V.G., Bittner M.A., Beavis R., Kuang Y., Salnikow K.V., Chepurny O.G., Little A.R., Plotnikov A.N., Wu D., Holz R.W., Petrenko A.G. α-Latrotoxin stimulates exocytosis by the interaction with a neuronal G-protein-coupled receptor. Neuron. 18:1997;925-937
90. Kruger P.G., Mahata S.K., Helle K.B. Catestatin (CgA344-364) stimulates rat mast cell release of histamine in a manner comparable to mastoparan and other cationic charged neuropeptides. Regul. Pept. 114:2003;29-35
91. + channels. Am. J. Physiol. 268:1995;C535-C556
92. 2+ oscillation frequency in GH3 cells. J. Neurochem. 72:1999;1472-1481
93. Lampe R.A., Defeo P.A., Davison M.D., Young J., Herman J.L., Spreen R.C., Horn M.B., Mangano T.J., Keith R.A. Isolation and pharmacological characterization of ω-grammotoxin SIA, a novel peptide inhibitor of neuronal voltage-sensitive calcium channel responses. Mol. Pharmacol. 44:1993;451-460
94. Leão R.M., Cruz J.S., Diniz C.R., Cordeiro M.N., Beirão P.S. Inhibition of neuronal high-voltage activated calcium channels by the ω-Phoneutria nigriventer Tx3-3 peptide toxin. Neuropharmacology. 39:2000;1756-1767
95. + channel Kir2.1. J. Gen. Physiol. 113:1999;555-564
96. Leipold E., Lu S., Gordon D., Hansel A., Heinemann S.H. Combinatorial interaction of scorpion toxins Lqh-2, Lqh-3, and Lqh{alpha}IT with sodium channel receptor sites-3. Mol. Pharmacol. 65:2004;685-691
97. 2+-channel gamma subunit. Nat. Genet. 19:1998;340-347
98. Liang S.P., Chen X.D., Shu Q., Zhang Y., Peng K. The presynaptic activity of huwentoxin-I, a neurotoxin from the venom of the Chinese bird spider Selenocosmia huwena. Toxicon. 38:2000;1237-1246
99. Libersat F. Wasp uses venom cocktail to manipulate the behavior of its cockroach prey. J. Comp. Physiol., A Neuroethol. Sens. Neural Behav. Physiol. 189:2003;497-508
100. Lipkin A., Kozlov S., Nosyreva E., Blake A., Windass J.D., Grishin E. Novel insecticidal toxins from the venom of the spider Segestria florentina. Toxicon. 40:2002;125-130
101. Llinás R., Sugimori M., Lin J.W., Cherksey B. Blocking and isolation of a calcium channel from neurons in mammals and cephalopods utilizing a toxin fraction (FTX) from funnel-web spider poison. Proc. Natl. Acad. Sci. U. S. A. 86:1989;1689-1693
102. 2+ channels in the mammalian central nervous system. Trends Neurosci. 15:1992;351-355
103. Mafra R.A., Figueiredo S.G., Diniz C.R., Cordeiro M.N., Cruz J.D., De Lima M.E. PhTx4, a new class of toxins from Phoneutria nigriventer spider venom, inhibits the glutamate uptake in rat brain synaptosomes. Brain Res. 831:1999;297-300
104. Magazanik L.G., Fedorova I.M., Kovalevskaya G.I., Pashkov V.N., Bulgakov O.V., Grishin E.V. Selective presynaptic insectotoxin (α- latroinsectotoxin) isolated from black widow spider venom. Neuroscience. 46:1992;181-188
105. Matavel A., Cruz J.S., Penaforte C.L., Araújo D.A., Kalapothakis E., Prado V.F., Diniz C.R., Cordeiro M.N., Beirão P.S. Electrophysiological characterization and molecular identification of the Phoneutria nigriventer peptide toxin PnTx2-6. FEBS Lett. 523:2002;219-223
106. Matthies H. Jr., Brackley P.T., Usherwood P.N., Reymann K.G. Philanthotoxin-343 blocks long-term potentiation in rat hippocampus. NeuroReport. 3:1992;649-652
107. McCormick K.D., Meinwald J. Neurotoxic acylpolyamines from spider venoms. J. Chem. Ecol. 19:1993;2411-2451
108. Meinwald J., Eisner T. The chemistry of phyletic dominance. Proc. Natl. Acad. Sci. U. S. A. 92:1995;14-18
109. 2+ channels by the spider venom toxin ω-Aga-IIIA. Proc. Natl. Acad. Sci. U. S. A. 88:1991;6628-6631
110. Miyawaki T., Tsubokawa H., Yokota H., Oguro K., Konno K., Masuzawa T., Kawai N. Differential effects of novel wasp toxin on rat hippocampal interneurons. Neurosci. Lett. 328:2002;25-28
111. Moreno D.H. Molecular and functional diversity of voltage-gated calcium channels. Ann. N.Y. Acad. Sci. 868:1999;102-117
112. Nakajima T., Yasuhara T., Uzu S., Wakamatsu K., Miyazawa T., Fukuda K., Tsukamoto Y. Wasp venom peptides; wasp kinins, new cytotrophic peptide families and their physico-chemical properties. Peptides. 6(Suppl. 3):1985;425-430
113. Newcomb R., Palma A., Fox J., Gaur S., Lau K., Chung D., Cong R., Bell J.R., Horne B., Nadasdi L. SNX-325, a novel calcium antagonist from the spider Segestria florentina. Biochemistry. 34:1995;8341-8347
114. Nichols C.G., Lopatin A.N. Inward rectifier potassium channels. Annu. Rev. Physiol. 59:1997;171-191
115. Nicholson G.M., Willow M., Howden M.E., Narahashi T. Modification of sodium channel gating and kinetics by versutoxin from the Australian funnel-web spider Hadronyche versuta. Pflugers Arch. 428:1994;400-409
116. Nicholson G.M., Little M.J., Tyler M., Narahashi T. Selective alteration of sodium channel gating by Australian funnel-web spider toxins. Toxicon. 34:1996;1443-1453
117. Norris T.M., Moya E., Blagbrough I.S., Adams M.E. Block of high-threshold calcium channels by the synthetic polyamines sFTX-3.3 and FTX-3.3. Mol. Pharmacol. 50:1996;939-946
118. Norton R.S., Pallaghy P.K. The cystine knot structure of ion channel toxins and related polypeptides. Toxicon. 36:1998;1573-1583
119. + channels. Jpn. J. Pharmacol. 88:2002;365-377
120. Ohara-Imaizumi M., Nakamichi Y., Ozawa S., Katsuta H., Ishida H., Nagamatsu S. Mastoparan stimulates GABA release from MIN6 cells: relationship between SNARE proteins and mastoparan action. Biochem. Biophys. Res. Commun. 289:2001;1025-1030
121. Olivera B.M., Cruz L.J. Conotoxins, in retrospect. Toxicon. 39:2001;7-14
122. Olivera B.M., Miljanich G.P., Ramachandran J., Adams M.E. Calcium channel diversity and neurotransmitter release: the ω-conotoxins and ω-agatoxins. Annu. Rev. Biochem. 63:1994;823-867
123. Olney J.W. Excitotoxicity: an overview. Can. Dis. Wkly. Rep. 16(Suppl. 1E):1990;47-57
124. 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
125. Orlova E.V., Rahman M.A., Gowen B., Volynski K.E., Ashton A.C., Manser C., van Heel M., Ushkaryov Y.A. Structure of α-latrotoxin oligomers reveals that divalent cation-dependent tetramers form membrane pores. Nat. Struct. Biol. 7:2000;48-53
126. Ozawa S., Kamiya H., Tsuzuki K. Glutamate receptors in the mammalian central nervous system. Prog. Neurobiol. 54:1998;581-618
127. Pallaghy P.K., Alewood D., Alewood P.F., Norton R.S. Solution structure of robustoxin, the lethal neurotoxin from the funnel-web spider Atrax robustus. FEBS Lett. 419:1997;191-196
128. Pan-Hou H., Suda Y., Sumi M., Yoshioka M., Kawai N. A spider toxin (JSTX) inhibits L-glutamate uptake by rat brain synaptosomes. Brain Res. 476:1989;354-357
129. Peng K., Shu Q., Liu Z., Liang S. Function and solution structure of huwentoxin-IV, a potent neuronal tetrodotoxin-sensitive sodium channel antagonist from chinese bird spider Selenocosmia huwena. J. Biol. Chem. 277:2002;47564-47571
130. Petrenko A.G., Perin M.S., Davletov B.A., Ushkaryov Y.A., Geppert M., Sudhof T.C. Binding of synaptotagmin to the α-latrotoxin receptor implicates both in synaptic vesicle exocytosis. Nature. 353:1991;65-68
131. Phillis J.W., O'Regan M.H. Characterization of modes of release of amino acids in the ischemic/reperfused rat cerebral cortex. Neurochem. Int. 43:2003;461-467
132. Piek T. δ-Philanthotoxin, a semi-irreversible blocker of ion-channels. Comp. Biochem. Physiol., C. 72:1982;311-315
133. Piek T. Neurotoxic kinins from wasp and ant venoms. Toxicon. 29:1991;139-149
134. Pin J.P., Duvoisin R. The metabotropic glutamate receptors: structure and functions. Neuropharmacology. 34:1995;1-26
135. Pinto J.E., Rothlin R.P. Presynaptic adrenergic supersensitivity induced by crude Latrodectus mactans venom. Toxicon. 12:1974;535-540
136. 2+ channel subtypes in cultured rat hippocampal neurons. Mol. Pharmacol. 48:1995;131-139
137. Pizzo A.B., Fontana A.C., Coutinho-Netto J., Santos W.F. Effects of the crude venom of the social wasp Agelaia vicina on γ-aminobutyric acid and glutamate uptake in synaptosomes from rat cerebral cortex. J. Biochem. Mol. Toxicol. 14:2000;88-94
138. 2+ channel (CACNLG), cDNA sequence, gene structure, and chromosomal location. J. Biol. Chem. 268:1993;9275-9279
139. 2+ channel to chromosome 7q21-q22 by somatic cell hybrid analysis. Genomics. 19:1994;192-193
140. Protti D.A., Reisin R., MacKinley T.A., Uchitel O.D. Calcium channel blockers and transmitter release at the normal human neuromuscular junction. Neurology. 46:1996;1391-1396
141. Quistad G.B., Reuter C.C., Skinner W.S., Dennis P.A., Suwanrumpha S., Fu E.W. Paralytic and insecticidal toxins from the funnel web spider, Hololena curta. Toxicon. 29:1991;329-336
142. Rash L.D., Birinyi-Strachan L.C., Nicholson G.M., Hodgson W.C. Neurotoxic activity of venom from the Australian eastern mouse spider (Missulena bradleyi) involves modulation of sodium channel gating. Br. J. Pharmacol. 130:2000;1817-1824
143. Reis H.J., Prado M.A., Kalapothakis E., Cordeiro M.N., Diniz C.R., De Marco L.A., Gómez M.V., Romano-Silva M.A. Inhibition of glutamate uptake by a polypeptide toxin (phoneutriatoxin 3-4) from the spider Phoneutria nigriventer. Biochem. J. 343:1999;413-418
144. Reis H.J., Gómez M.V., Kalapothakis E., Diniz C.R., Cordeiro M.N., Prado M.A., Romano-Silva M.A. Inhibition of glutamate uptake by Tx3-4 is dependent on the redox state of cysteine residues. NeuroReport. 11:2000;2191-2194
145. Richard Benzinger G., Tonkovich G.S., Hanck D.A. Augmentation of recovery from inactivation by site-3 Na channel toxins. A single-channel and whole-cell study of persistent currents. J. Gen. Physiol. 113:1999;333-346
146. Richerson G.B., Wu Y. Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J. Neurophysiol. 90:2003;1363-1374
147. Rodrigues M.C., Guizzo R., Santos W.F., Cairasco N.G. A comparative neuroethological study of limbic seizures induced by Parawixia bistriata venom and kainic acid injections in rats. Brain Res. Bull. 55:2001;79-86
148. + channel alpha subunit. J. Biol. Chem. 271:1996;15950-15962
149. Sahara Y., Gotoh M., Konno K., Miwa A., Tsubokawa H., Robinson H.P., Kawai N. A new class of neurotoxin from wasp venom slows inactivation of sodium current. Eur. J. Neurosci. 12:2000;1961-1970
150. Sanguinetti M.C., Johnson J.H., Hammerland L.G., Kelbaugh P.R., Volkmann R.A., Saccomano N.A., Mueller A.L. Heteropodatoxins: peptides isolated from spider venom that block Kv4.2 potassium channels. Mol. Pharmacol. 51:1997;491-498
151. Schmidt J.O. Chemistry, pharmacology and chemical ecology of ant venoms. Piek T. Venoms of the Hymenoptera. 1986;425-508 Academic Press, London
152. 2+ channel currents by the funnel web spider toxin ω-Aga-IA. Mol. Pharmacol. 38:1990;711-718
153. Shatursky O.Ya., Pashkov V.N., Bulgacov O.V., Grishin E.V. Interaction of α-latroinsectotoxin from Latrodectus mactans venom with bilayer lipid membranes. Biochim. Biophys. Acta. 1233:1995;14-20
154. 3H]GABA from synaptosomes. Neurochem. Res. 20:1995;1065-1071
155. Skinner W.S., Adams M.E., Quistad G.B., Kataoka H., Cesarin B.J., Enderlin F.E., Schooley D.A. Purification and characterization of two classes of neurotoxins from the funnel web spider, Agelenopsis aperta. J. Biol. Chem. 264:1989;2150-2155
156. Stapleton A., Blankenship D.T., Ackermann B.L., Chen T.M., Gorder G.W., Manley G.D., Palfreyman M.G., Coutant J.E., Cardin A.D. Curtatoxins. Neurotoxic insecticidal polypeptides isolated from the funnel-web spider Hololena curta. J. Biol. Chem. 265:1990;2054-2059
157. Strichartz G., Rando T., Wang G.K. An integrated view of the molecular toxicology of sodium channel gating in excitable cells. Annu. Rev. Neurosci. 10:1987;237-267
158. Stromgaard K., Brierley M.J., Andersen K., Slok F.A., Mellor I.R., Usherwood P.N., Krogsgaard-Larsen P., Jaroszewski J.W. Analogues of neuroactive polyamine wasp toxins that lack inner basic sites exhibit enhanced antagonism toward a muscle-type mammalian nicotinic acetylcholine receptor. J. Med. Chem. 42:1999;5224-5234
159. Stromgaard K., Andersen K., Krogsgaard-Larsen P., Jaroszewski J.W. Recent advances in the medicinal chemistry of polyamine toxins. Mini Rev. Med. Chem. 1:2001;317-338
160. + channel through multiple binding sites. Neuron. 18:1997;665-673
161. Szeto T.H., Birinyi-Strachan L.C., 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. 470:2000;293-299
162. Takahashi M., Seagar M.J., Jones J.K., Reber B.F., Catterall W.A. Subunit structure of dihydropyridine-sensitive calcium channels from skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 84:1987;5478-5482
163. + channels: common surface features of gating modifier toxins. J. Mol. Biol. 297:2000;771-780
164. Terlau H., Stuhmer W. Structure and function of voltage-gated ion channels. Naturwissenschaften. 85:1998;437-444
165. Tuichibaev M.U., Tashmukhamedov B.A., Gotgil'f I.G., Mazannik L.G. Orientotoxin, a new presynaptic neurotoxin from the venom of the giant hornet Vespa orientalis. Bioorg. Khim. 10:1984;318-322
166. Uchitel O.D. Toxins affecting calcium channels in neurons. Toxicon. 35:1997;1161-1191
167. Uchitel O.D., Protti D.A., Sanchez V., Cherksey B.D., Sugimori M., Llinás R. P-type voltage-dependent calcium channel mediates presynaptic calcium influx and transmitter release in mammalian synapses. Proc. Natl. Acad. Sci. U. S. A. 89:1992;3330-3333
168. Usherwood P.N., Blagbrough I.S. Spider toxins affecting glutamate receptors: polyamines in therapeutic neurochemistry. Pharmacol. Ther. 52:1991;245-268
169. Usherwood P.N., Duce I.R., Boden P. Slowly-reversible block of glutamate receptor-channels by venoms of the spiders, Argiope trifasciata and Araneus gemma. J. Physiol. (Paris). 79:1984;241-245
170. Ushkaryov Y. α-Latrotoxin: from structure to some functions. Toxicon. 40:2002;1-5
171. Ushkaryov Y.A., Petrenko A.G., Geppert M., Sudhof T.C. Neurexins: synaptic cell surface proteins related to the α-latrotoxin receptor and laminin. Science. 257:1992;50-56
172. Vajda F.J. Neuroprotection and neurodegenerative disease. J. Clin. Neurosci. 9:2002;4-8
173. Van Marle J., Piek T., Lind A., Van Weeren-Kramer J. Reduction of high affinity glutamate uptake in rat hippocampus by two polyamine-like toxins isolated from the venom of the predatory wasp Philanthus triangulum FJ. Experientia. 42:1986;157-158
174. Van Marle J., Piek T., Karst H., Lind A., Van Weeren-Kramer J. Presynaptic effects of spider toxins: increase of high affinity uptake in the arthropod peripheral glutamatergic system. Experientia. 45:1989;155-156
175. Van Wilgenburg H., Piek T., Mantel P. Ion channel block in rat diaphragm by the venom of the digger wasp Philanthus triangulum. Comp. Biochem. Physiol., C. 79:1984;205-211
176. Venema V.J., Swiderek K.M., Lee T.D., Hathaway G.M., Adams M.E. Antagonism of synaptosomal calcium channels by subtypes of ω-agatoxins. J. Biol. Chem. 267:1992;2610-2615
177. Vergara C., Latorre R., Marrion N.V., Adelman J.P. Calcium-activated potassium channels. Curr. Opin. Neurobiol. 8:1998;321-329
178. 2+-dependent glutamate release in synaptosomes. Neurochem. Int. 42:2003;277-282
179. Wang X., Smith R., Fletcher J.I., Wilson H., Wood C.J., Howden M.E., King G.F. Structure-function studies of ω-atracotoxin, a potent antagonist of insect voltage-gated calcium channels. Eur. J. Biochem. 264:1999;488-494
180. v2/NaG channel is involved in control of salt-intake behavior in the CNS. J. Neurosci. 20:2000;7743-7751
181. Wilson M.L., Guild S.B. A direct inhibitory action of prostaglandins upon ACTH secretion at the late stages of the secretory pathway of AtT-20 cells. Br. J. Pharmacol. 135:2002;1851-1858
182. Williams K. Effects of Agelenopsis aperta toxins on the N-methyl-D-aspartate receptor: polyamine-like and high-affinity antagonist actions. J. Pharmacol. Exp. Ther. 266:1993;231-236
183. Williams M.E., Brust P.F., Feldman D.H., Patthi S., Simerson S., Maroufi A., McCue A.F., Velicelebi G., Ellis S.B., Harpold M.M. Structure and functional expression of an omega-conotoxin-sensitive human N-type calcium channel. Science. 257:1992;389-395
184. Xiao Y.C., Liang S.P. Inhibition of sodium channels in rat dorsal root ganglion neurons by Hainantoxin-IV, a novel spider toxin. Acta Biochim. Biophys. Sin. 35:2003;82-85
185. Yamada M., Inanobe A., Kurachi Y. G protein regulation of potassium ion channels. Pharmacol. Rev. 50:1998;723-760
186. Yi B.A., Minor D.L. Jr., Lin Y.F., Jan Y.N., Jan L.Y. Controlling potassium channel activities: interplay between the membrane and intracellular factors. Proc. Natl. Acad. Sci. U. S. A. 98:2001;11016-11023
187. Yokota H., Tsubokawa H., Miyawaki T., Konno K., Nakayama H., Masuzawa T., Kawai N. Modulation of synaptic transmission in hippocampal CA1 neurons by a novel neurotoxin (β-pompilidotoxin) derived from wasp venom. Neurosci. Res. 41:2001;365-371
188. Yu F.H., Catterall W.A. Overview of the voltage-gated sodium channel family. Genome Biol. 4:2003;207