Understanding the in vitro neuromuscular activity of snake venom Lys49 phospholipase A2 homologues

Toxicon

Volumn 55, Issue 1, 2010, Pages 1-11

  Gallacci, M ^a   Cavalcante, W L G ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Neuromuscular junction; Phospholipase A2; Snake venom

Indexed keywords

ACETYLCHOLINE; CALCIUM ION; HEPARIN; LYSINE; PHOSPHOLIPASE A2; POTASSIUM CHLORIDE; SNAKE VENOM;

ACETYLCHOLINE RELEASE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME ISOLATION; ENZYME MECHANISM; ENZYME SYNTHESIS; IN VITRO STUDY; MEMBRANE STABILIZATION; NEUROMUSCULAR BLOCKING; NEUROMUSCULAR TRANSMISSION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEQUENCE HOMOLOGY; SNAKE;

ANIMALS; HUMANS; MEMBRANES; MUSCLES; NEUROMUSCULAR JUNCTION; NEURONS; PHOSPHOLIPASES A2; REPTILIAN PROTEINS; SPECIES SPECIFICITY; VIPER VENOMS; VIPERIDAE;

BOTHROPS; SERPENTES; VIPERIDAE;

EID: 70649086089     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2009.10.025     Document Type: Review

References (113)

1. 2 in Bothrops snake venoms: effect of chemical modifications on the enzymatic and pharmacological properties of bothropstoxins from Bothrops jararacussu. Biochimie 82 (2000) 755-763
2. 2 from the venom of the arboreal snake Bothriechis (Bothrops) schlegelii from Costa Rica. Arch. Biochem. Biophys. 339 (1997) 260-267
3. 2 homologues are reduced, but not abolished, by a pH-induced dissociation. Toxicon 46 (2005) 291-296
4. 2: a structural review. Toxicon 34 (1996) 827-841
5. 2 homologue isolated from the venom of Bothrops nummifer (jumping viper). Toxicon 37 (1999) 371-384
6. Azevedo-Marques M.M., Hering S.E., and Cupo P. Evidence that Crotalus durissus terrificus (South American rattlesnake) envenomation in human causes myolysis rather than hemolysis. Toxicon 11 (1987) 1163-1168
7. 2 from Agkistrodon piscivorus piscivorus venom. Eur. J. Biochem. 176 (1988) 353-357
8. 2 Neuwieditoxin-I and Neuwieditoxin-II, from Bothrops neuwiedi pauloensis (jararaca-pintada) venom. J. Venom. Anim. Toxin. Incl. Trop. Dis. 13 (2007) 103-121
9. Bowman W.C., and Rand M.J. Striated muscle and neuromuscular transmission. Textbook of Pharmacology (1980), Blackwell Scientific Publications, Oxford 17.1-17.56
10. 2, on liposomes and mouse gastrocnemius muscle. Toxicon 31 (1993) 217-222
11. 2 from Bothrops asper snake venom. Arch. Biochem. Biophys. 358 (1998) 343-350
12. Cavalcante W.L., Silva M.D., and Gallacci M. Influence of temperature upon paralyzing and myotoxic effects of bothropstoxin-I on mouse neuromuscular preparations. Chem. Biol. Interact. 151 (2005) 95-100
13. 2 toxins by aqueous extract of Casearia sylvestris (Flacourtiaceae) in mouse neuromuscular preparation. J. Ethnopharmacol 112 (2007) 490-497
14. 2 by sequence analysis and site directed mutagenesis. Toxicon 42 (2003) 869-883
15. Cintra A.C., Marangoni S., Oliveira B., and Giglio J.R. Bothropstoxin-I: amino acid sequence and function. J. Protein Chem. 12 (1993) 57-64
16. Colomar A., and Robitaille R. Glial modulation of synaptic transmission at the neuromuscular junction. Glia 47 (2004) 284-289
17. Connolly S., Trevett A.J., Nwokolo N.C., Lalloo D.G., Naraqi S., Mantle D., Schofield I.S., Fawcett P.R., Harris J.B., and Warrell D.A. Neuromuscular effects of papuan taipan snake venom. Ann. Neurol. 38 (1995) 916-920
18. 2 homologue. Proteins 30 (1998) 442-454
19. 2 from snake venom to human secreted forms. J. Mol. Evol. 31 (1990) 228-238
20. De Robertis E.D.P., and Bennet H.S. Some features of the submicroscopy morphology of synapses in frog and earthworm. J. Biophys. Biochem. Cytol. 1 (1955) 47-58
21. 2 homologue from the venom of Cerrophidion (Bothrops) godmani. Biochim. Biophys. Acta 1384 (1998) 204-208
22. Dennis E.A. Phospholipases. In: Boyer P.D. (Ed). The Enzymes vol. 16 (1983), Academic Press, New York 307-356
23. 2. Biochem. Biophys. Acta 70 (1963) 538-553
24. Del Castillo J., and Katz B. Quantal components of the end-plate potential. J. Phisiol. Lond 124 (1954) 560-573
25. 2 reduces its membrane-destabilizing effect. Arch. Biochem. Biophys. 312 (1994) 336-339
26. 2, anticoagulant and myotoxic activities. Biochim. Biophys. Acta 1070 (1991) 455-460
27. Dixon R.W., and Harris J.B. Myotoxic activity of the toxic phospholipase, notexin, from the venom of the Australian tiger snake. J. Neuropathol. Exp. Neurol. 55 (1996) 1230-1237
28. Fatt P., and Katz B. Spontaneous subthreshold activity at motor nerve endings. J. Physiol. Lond. 117 (1952) 109-128
29. + channels and ankyrin in neuromuscular junctions is complementary to that of acetylcholine receptors and the 43 kd protein. Neuron 3 (1989) 163-175
30. 2. Arch. Biochem. Biophys. 284 (1991) 352-359
31. Gallacci M., Oliveira M., Dal Pai-Silva M., Cavalcante W.L., and Spencer P.J. Paralyzing and myotoxic effects of a recombinant bothropstoxin-I (BthTX-I) on mouse neuromuscular preparations. Exp. Toxicol. Pathol. 57 (2006) 239-245
32. Gauthier G.F., and Padykula H.A. Cytological studies of fiber types in skeletal muscle. A comparative study of the mammalian diaphragm. J. Cell Biol. 28 (1966) 333-354
33. 2: insights into the mechanisms of local and systemic myotoxicity. Toxicon 42 (2003) 915-931
34. 2 myotoxins from Bothrops snake venoms. Toxicon 33 (1995) 1405-1424
35. Gutiérrez J.M., Lomonte B., Chaves F., Moreno E., and Cerdas L. Pharmacological activities of a toxic phospholipase A isolated from the venom of the snake Bothrops asper. Comp. Biochem. Physiol. C 84 (1986) 159-164
36. 2 homologue. Toxicon 51 (2008) 80-92
37. Haimovich B., Schotland D.L., Fieles W.E., and Barchi R.L. Localization of sodium channel subtypes in adult rat skeletal muscle using channel-specific monoclonal antibodies. J. Neurosci. 7 (1987) 2957-2966
38. Harris J.B., Johnson M.A., and Karlsson E. Pathological responses of rat skeletal muscle to a single subcutaneous injection of a toxin isolated from the venom of the Australian tiger snake, Notechis scutatus scutatus. Clin. Exp. Pharmacol. Physiol. 2 (1975) 383-404
39. Harvey A.L., Barfaraz A., Thomson E., Faiz A., Preston S., and Harris J.B. Screening of snake venoms for neurotoxic and myotoxic effects using simple in vitro preparations from rodents and chicks. Toxicon 32 (1994) 257-265
40. Heluany N.F., Homsi-Brandeburgo M.I., Giglio J.R., Prado-Franceschi J., and Rodrigues-Simioni L. Effects induced by bothropstoxin, a component from Bothrops jararacussu snake venom, on mouse and chick muscle preparations. Toxicon 30 (1992) 1203-1210
41. Heuser J.E., and Reese T.S. Structure of the synapse. In: Kandel E.R. (Ed). Handbook of Physiology. The Nervous System. Cellular Biology of Neurons vol. 1 (1977), American Physiological Society, Bethesda 261-294
42. Hodgson W.C., and Wickramaratna J.C. In vitro neuromuscular activity of snake venoms. Clin. Exp. Pharmacol. Physiol. 29 (2002) 807-814
43. Homsi-Brandeburgo M.I., Queiroz L.S., Santo-Neto H., Rodrigues-Simioni L., and Giglio J.R. Fractionation of Bothrops jararacussu snake venom: partial chemical characterization and biological activity of bothropstoxin. Toxicon 26 (1988) 615-627
44. Hughes B.W., Kusner L.L., and Kaminski H.J. Molecular architecture of the neuromuscular junction. Muscle Nerve 33 (2006) 445-461
45. Johnson E.K., and Ownby C.L. The role of extracellular ions in the pathogenesis of myonecrosis induced by a myotoxin isolated from broad-banded copperhead (Agkistrodon contortrix laticinctus) venom. Comp. Biochem. Physiol. Pharmacol. Toxicol. Endocrinol. 107 (1994) 359-366
46. Kaiser I.I., Gutiérrez J.M., Plummer D., Aird S.D., and Odell G.V. The amino acid sequence of a myotoxic phospholipase from the venom of Bothrops asper. Arch. Biochem. Biophys 278 (1990) 319-325
47. 2 enzymes. Toxicon 42 (2003) 827-840
48. 2 Enzymes: Structure, Function and Mechanism (1997), Wiley, Chichester 1-511
49. Kochva E. The origin of snakes and evolution of the venom apparatus. Toxicon 25 (1987) 65-106
50. Krejci E., Thomine S., Boschetti N., Legay C., Sketelj J., and Massoulie J. The mammalian gene of acetylcholinesterase-associated collagen. Biol. Chem. 272 (1997) 22840-22847
51. 2 homologue from Vipera ammodytes venom. Eur. J. Biochem 202 (1991) 1165-1168
52. 2-a hypothesis: the crystal structure of piratoxin II complexed to fatty acid. Biochemistry 40 (2001) 28-36
53. 2 with low activity, from Trimeresurus flavoviridis venom. J. Biochem. 107 (1990) 400-408
54. 2 myotoxins from crotalid snake venoms and their structural determinants of myotoxic action. Toxicon 42 (2003) 885-901
55. Lomonte B., and Gutiérrez J.M. A new muscle damaging toxin, myotoxin II, from the venom of the snake Bothrops asper (terciopelo). Toxicon 27 (1989) 725-733
56. Lomonte B., Gutiérrez J.M., and Mata E. Isolation from a polyvalent antivenom of antibodies to a myotoxin in Bothrops asper snake venom. Toxicon 23 (1985) 807-813
57. Lomonte B., Gutiérrez J.M., Moreno E., and Cerdas L. Antibody neutralization of a myotoxin from the venom of Bothrops asper (terciopelo). Toxicon 25 (1987) 443-449
58. 2 from the venom of the snake Bothrops asper by monoclonal antibodies. Toxicon 30 (1992) 239-245
59. 2 from Bothrops asper snake venom. Identification of a heparin binding and cytolytic toxin region by the use of synthetic peptides and molecular modeling. J. Biol. Chem. 269 (1994) 29867-29873
60. 2 of Bothrops asper snake venom. Toxicon 32 (1994) 1359-1369
61. 2 on mouse endothelial (tEnd) and skeletal muscle (C2C12) cells in vitro. Toxicon 37 (1999) 145-158
62. Luff A.R. Dynamic properties of the inferior rectus, extensor digitorum longus, diaphragm and soleus muscles of the mouse. J. Physiol. 313 (1981) 161-171
63. MacLennan D.H., and Toyofuku T. Structure-function relationships in the Ca(2+) pump of the sarco-plasmic reticulum. Biochem. Soc. Trans. 20 (1992) 559-562
64. Magro A.J., Soares A.M., Giglio J.R., and Fontes M.R. Crystal structures of BnSP-7 and BnSP-6, two Lys49-phospholipases A(2): quaternary structure and inhibition mechanism insights. Biochem. Biophys. Res. Commun. 311 (2003) 713-720
65. 2. J. Biol. Chem. 261 (1986) 4797-4804
66. 2 with lysine in place of aspartate 49. J. Biol. Chem. 259 (1984) 13839-13843
67. 2 inhibitors: medicinal chemistry and therapeutic potential. Curr. Top. Med. Chem. 7 (2007) 743-756
68. 2 myotoxin. Toxicon 47 (2006) 797-811
69. 2 myotoxins. Toxicon 37 (1999) 199-215
70. 2+ ions in excitation-contraction coupling of skeletal muscle fibers. Biochim. Biophys. Acta 1241 (1995) 59-116
71. 2 myotoxins and neurotoxins: common aspects of their mechanisms of action. Cell. Mol. Life Sci. 65 (2008) 2897-2912
72. Moura-da-Silva A.M., Cardoso D.F., Tanizaki M.M., and Mota I. Neutralization of myotoxic activity of Bothrops venoms by antisera to purified myotoxins and to crude venoms. Toxicon 29 (1991) 1471-1480
73. Oshima-Franco Y., Leite G.B., Belo C.A., Hyslop S., Prado-Franceschi J., Cintra A.C., Giglio J.R., da Cruz-Höfling M.A., and Rodrigues-Simioni L. The presynaptic activity of bothropstoxin-I, a myotoxin from Bothrops jararacussu snake venom. Basic Clin. Pharmacol. Toxicol. 95 (2004) 175-182
74. de Oliveira M., Cavalcante W.L., Arruda E.Z., Melo P.A., Dal-Pai Silva M., and Gallacci M. Antagonism of myotoxic and paralyzing activities of bothropstoxin-I by suramin. Toxicon 42 (2003) 373-379
75. Oshima-Franco Y., Leite G.B., Silva G.H., Cardoso D.F., Hyslop S., Giglio J.R., da Cruz-Höfling M.A., and Rodrigues-Simioni L. Neutralization of the pharmacological effects of bothropstoxin-I from Bothrops jararacussu (jararacuçu) venom by crotoxin antiserum and heparin. Toxicon 39 (2001) 1477-1485
76. 2 proteins. Toxicon 37 (1999) 411-445
77. 2 from Agkistrodon halys pallas venom, and its expression in E. coli. Toxicon 36 (1998) 1155-1163
78. 2, ecarpholin S, from the venom of Echis carinatus sochureki (saw-scaled viper). Biochem. J. 319 (1996) 961-968
79. 2 homologue isolated from the venom of the snake Bothrops alternatus. Biochim. Biophys. Acta 1770 (2007) 585-593
80. Prasarnpun S., Walsh J., Awad S.S., and Harris J.B. Envenoming bites by kraits: the biological basis of treatment resistant neuromuscular paralysis. Brain 128 (2005) 2987-2996
81. Randazzo-Moura P., Ponce-Soto L.A., Rodrigues-Simioni L., and Marangoni S. Structural characterization and neuromuscular activity of a new Lys49 phospholipase A(2) homologous (Bp-12) isolated from Bothrops pauloensis snake venom. Protein J 27 (2008) 355-362
82. Robitaille R., Adler E.M., and Charlton M.P. Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses. Neuron 5 (1990) 773-779
83. 2) from Bothrops pauloensis snake venom. Toxicon 50 (2007) 153-165
84. 2 from Bothrops neuwiedi pauloensis snake venom. Toxicon 44 (2004) 305-314
85. Rodrigues-Simioni L., Borgese N., and Ceccarelli B. The effects of Bothrops jararacussu venom and its components on frog nerve-muscle preparation. Neuroscience 10 (1983) 475-489
86. 2 myotoxin. Toxicon 33 (1995) 1479-1489
87. Rufini S., Cesaroni P., Desideri A., Farias R., Gubensek F., Gutiérrez J.M., Luly P., Massoud R., Morero R., and Pedersen J.Z. Calcium ion independent membrane leakage induced by phospholipase-like myotoxins. Biochemistry 31 (1992) 12424-12430
88. 2+-independent membrane-damaging activity. Biochem. J. 382 (2004) 191-198
89. 2 from the venom of Agkistridon piscivorus piscivorus. J. Biol. Chem. 267 (1992) 22,645-22,657
90. 2. Science 250 (1990) 1541-1546
91. 2 from Trimeresurus flavoviridis venom are membrane-acting enzymes. J. Biochem. 118 (1995) 1037-1044
92. 2 enzymes: classification and characterization. Biochim. Biophys. Acta 1488 (2000) 1-19
93. 2 homologue from Bothrops moojeni (caissaca) snake venom. Arch. Biochem. Biophys. 373 (2000) 7-15
94. 2 from Bothrops pirajai snake venom. Arch. Biochem. Biophys. 387 (2001) 188-196
95. 2 homologue from Bothrops neuwiedi pauloensis venom. Arch. Biochem. Biophys. 378 (2000) 201-209
96. 2) homologue from Bothrops jararacussu snake venom. Int. J. Biochem. Cell Biol. 34 (2002) 668-677
97. 2 homologue: an example of function versatility of snake venom proteins. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 142 (2006) 371-381
98. Standaert F.G. Basic physiology and pharmacology of the neuromuscular junction. In: Miller R.D. (Ed). Anesthesia. second ed. (1986), Churchill Livingstone, London 835-870
99. Takeuchi A., and Takeuchi N. On the permeability of the end-plate membrane during the action of transmitter. J. Physiol. 154 (1960) 52-67
100. Toutant J.P., Rouaud T., and Le Douarin G.H. Histochemical properties of the biventer cervicis muscle of the chick: a relationship between multiple innervation and slow-tonic fibre types. Histochem. J. 13 (1981) 481-493
101. 2 of bamboo viper (Trimeresurus stejnegeri): molecular characterization, geographic variations and evidence of multiple ancestries. Biochem. J. 377 (2004) 215-223
102. Trento E.P., Garcia O.S., Rucavado A., Franca S.C., Batalini C., Arantes E.C., Giglio J.R., and Soares A.M. Inhibitory properties of the anti-bothropic complex from Didelphis albiventris serum on toxic and pharmacological actions of metalloproteases and myotoxins from Bothrops asper venom. Biochem. Pharmacol 62 (2001) 1521-1529
103. 2?. Biochimie 82 (2000) 815-831
104. 2 homologue from the venom of the snake Bothrops asper: evidence of rapid plasma membrane damage and a dual role for extracellular calcium. Toxicol In Vitro 21 (2007) 1382-1389
105. 2: biological and membrane-disrupting activities in the absence of catalysis. Biochem. J. 362 (2002) 89-96
106. 2: clues towards identification of residues involved in a novel mechanism of membrane damage and in myotoxicity. Protein Eng. 11 (1998) 285-294
107. Warrell D.A. Clinical toxicology of snakebite in Africa and the Middle East/Arabian Peninsula. In: Meier J., and White J. (Eds). Handbook of Clinical Toxicology of Animal Venoms and Poisons (1995), CRC Press, Florida 433-492
108. Westenbroek R.E., Hoskins L., and Catterall W.A. Localization of calcium channel subtypes on rat spinal motor neurons, interneurons and nerve terminals. J. Neurosci. 18 (1998) 6319-6330
109. Wood S., and Slater C. The contribution of postsynaptic folds to the safety factor for neuromuscular transmission in rat fast and slow-twitch muscles. J. Physiol. 500 (1997) 165-176
110. Wood S.J., and Slater C.R. beta-Spectrin is colocalized with both voltage-gated sodium channels and ankyrinG at the adult rat neuromuscular junction. J. Cell Biol. 140 (1998) 675-684
111. Wood S.J., and Slater C.R. Safety factor at the neuromuscular junction. Prog. Neurobiol. 64 (2001) 393-429
112. 2 as active enzymes for beta-arachidonoyl phospholipid bilayer membranes. Biochem. Mol. Biol. Int. 43 (1997) 19-26
113. 2 with low activity, from the venom of Trimeresurus flavoviridis (Habu snake). Toxicon 28 (1990) 43-54