Cellular pathology induced by snake venom phospholipase A2 myotoxins and neurotoxins: Common aspects of their mechanisms of action

Cellular and Molecular Life Sciences

Volumn 65, Issue 18, 2008, Pages 2897-2912

  Montecucco, C ^a,b   Gutierrez J M ^a   Lomonte, B ^a  

^a UNIVERSIDAD DE COSTA RICA   (Costa Rica)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

Ca2+; Myotoxins; Neurotoxins; PLA2; Snake venoms

Indexed keywords

ACL MYOTOXIN; AMMODYTIN L; AMMODYTOXIN A; APPK 49; BETA BUNGAROTOXIN; BOTHROPSTOXIN I; BOTHROPSTOXIN II; CALCIUM ION; CELL ENZYME; CELL PROTEIN; CREATINE KINASE; CROTOXIN; MEMBRANE RECEPTOR; MYOTOXIN; MYOTOXIN II; MYOTOXIN III; NEUROTOXIN; NOTEXIN; PHOSPHOLIPASE A2; SNAKE VENOM; TAIPOXIN; TEXTILOTOXIN; UNCLASSIFIED DRUG;

ACUTE KIDNEY FAILURE; AMINO ACID SEQUENCE; CALCIUM CELL LEVEL; CELL DEGENERATION; CELL MEMBRANE; CREATINE KINASE BLOOD LEVEL; CYTOTOXICITY; ENZYME METABOLISM; GENETIC CONSERVATION; HEMOLYSIS; HUMAN; HYPERKALEMIA; MEMBRANE DAMAGE; MOLECULAR EVOLUTION; MUSCLE CELL; MUSCLE TOXICITY; MYOGLOBINURIA; NEUROMUSCULAR SYNAPSE; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PROTEIN TARGETING; REVIEW; RHABDOMYOLYSIS; SNAKE; TARGET CELL; TISSUE REGENERATION; TISSUE REPAIR;

ANIMALS; CALCIUM; CELL MEMBRANE; ISOENZYMES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUROTOXINS; PHOSPHOLIPASES A2; PROTEIN CONFORMATION; SNAKE VENOMS;

EID: 52549092961     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-008-8113-3     Document Type: Review

References (168)

1. 2 Enzymes. John Wiley & Sons, Chichester.
2. Harris, J,B, (1997) Toxic phospholipases in snake venom: an introductory review. Symp. Zool. Soc. Lond. 70, 235-250.
3. 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. (1995) Neuromuscular effects of papuan taipan snake venom. Ann. Neurol. 38, 916-920.
4. Prasarnpun, S., Walsh, J., Awad, S. S. and Harris, J. B. (2005) Envenoming bites by kraits: the biological basis of treatment-resistant neuromuscular paralysis. Brain 128, 2987-2996.
5. 2 Enzymes. Structure, Function and Mechanism. John Wiley & Sons, Chichester, p. 129-154.
6. Warrell, D. A. (1995) 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. CRC Press, Florida, p. 433-492.
7. 2 on mouse endothelial (tEnd) and skeletal muscle (C2C12) cells in vitro. Toxicon 37, 145-158.
8. 2 isolated from Bothrops asper (terciopelo) venom. Biochim. Biophys. Acta 1179, 253-259.
9. 2 of Bothrops asper snake venom. Toxicon 32, 1359-1369.
10. 2. Toxicon 42, 947-962.
11. Saravia-Otten, P., Gutiérrez, J. M., Arvidson, S., Thelestam, M. and Flock, J-I. (2007) Increased infectivity of Staphylococcus aureus in an experimental model of snake venom-induced tissue damage. J. Infect. Dis. 196, 748-754.
12. Gutiérrez, J. M., Theakston, R. D. G. and Warrell, D. A. (2006) Confronting the neglected problem of snake bite envenoming: the need for a global partnership. PLoS Medicine 3, e 150.
13. Rappuoli, R. and Montecucco, C. (Editors) (1997) Protein Toxins and their Use in Cell Biology. Oxford University Press, Oxford.
14. Gutiérrez, J. M., Editor (2003) Special Issue: Myotoxic phospholipases. Toxicon 42, 825-986.
15. 2. Toxicon 50, 871-92.
16. Rossetto, O. and Montecucco, C. (2007) Presynaptic neurotoxins with enzymatic activities. Handb. Exp. Pharmacol. 184, 129-170.
17. 2 enzymes: structure, function and mechanism. John Wiley & Sons, Chichester, p 97-128.
18. 2 myotoxins from crotalid snake venoms and their structural determinants of myotoxic action. Toxicon 42, 885-901.
19. 2 by sequence analysis and site directed mutagenesis. Toxicon 42, 869-883.
20. Kwong, P. D., McDonald, N. Q., Sigler, P. B. and Hendrickson, W. A. (1995) Structure of beta 2-bungarotoxin: potassium channel binding by Kunitz modules and targeted phospholipase action. Structure 3, 1109-1119.
21. 2 enzymes: structure, function and mechanism. John Wiley & Sons, Chichester, p 269-285.
22. Montecucco, C. and Rossetto, O. (2008) On the quaternary structure of taipoxin and textilotoxin: the advantage of being multiple. Toxicon, in press
23. Milani, R., Jorge, M. T., Ferraz de Campos, F. P., Martins, F. P., Bousso, A., Cardoso, J. L. C., Ribeiro, L. A., Fan, H. W., Franca, F. O. S., Sano-Martins, I. S., Cardoso, D., Fernández, I. C. O. F., Fernandes, J. C., Aldred, V. L., Sandoval, M. P., Puorto, G., Theakston, R. D. G. and Warrell, D. A., 1997. Snake bites by the jararacucu (Bothrops jararacussu): clinicopathological studies of 29 proven cases in Sao Paulo state, Brazil. Q. J. Med. 90, 323-334.
24. Warrell, D. A. (2004) Snakebites in Central and South America: Epidemiology, clinical features and clinical management. In: Campbell, J. A., Lamar, W. W. (Eds.), The Venomous Reptiles of the Western Hemisphere, Vol II. Ithaca: Comstock, p. 709-761.
25. 2: insights into the mechanisms of local and systemic myotoxicity. Toxicon 42, 915-31.
26. Salvini, T. F., Amaral, A. C., Miyabara, E. H., Turri, J. A. O., Danella, P. M. and Selistre-de-Arafújo, H. S. (2001) Systemic skeletal muscle necrosis induced by crotoxin. Toxicon 39, 1141-1149.
27. Ponraj, D, and Gopalakrishnakone, P. (1996) Establishment of an animal model for myoglobinuria by use of amyotoxin from Pseudechis australis (king brown snake) venom in mice. Lab. Anim. Sci. 46, 393-398.
28. Rowan, E. G. (2001) What does beta-bungarotoxin do at the neuromuscular junction? Toxicon 39, 107-118.
29. 2. Trends Pharmacol. Sci. 20, 162-70.
30. Abe, T., Limbrick, A. R. and Miledi, R. (1976) Acute muscle denervation induced by beta-bungarotoxin. Proc. R. Soc. Lond. B Biol. Sci. 194, 545-553.
31. Rehm, H. and Betz, H. (1982) Binding of beta-bungarotoxin to synaptic membrane fractions of chick brain. J. Biol. Chem. 257, 10015-10022.
32. Lambeau, G., Barhanin, J., Schweitz, H., Qar, J. and Lazdunski, M. (1989) Identification and properties of very high affinity brain membrane-binding sites for a neurotoxic phospholipase from the taipan venom. J. Biol. Chem. 264, 11503-11510.
33. 3H-beta-bungarotoxin: demonstration of saturable binding to brain synapses and its inhibition by toxin I. Eur. J. Biochem. 128, 267-276.
34. 2 myotoxins from crotalid snake venoms. Cell Biochem. Funct. 23, 307-313.
35. 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, 1382-1389.
36. Harris, J. B., Johnson, M. A. and Karlsson, E. (1975) 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, 383-404.
37. Dixon, R. W. and Harris, J. B. (1996) Myotoxic activity of the toxic phospholipase, notexin, from the venom of the Australian tiger snake. J. Neuropathol. Exp. Neurol. 55, 1230-1237.
38. 2 myotoxins in vivo and in vitro. Comp. Biochem. Physiol. C 143, 284-294.
39. 2 OS2: The N-terminal region is more important than enzymatic activity. Biochemistry 45, 5800-5816.
40. 2. J. Biol. Chem. 280, 29989-29992.
41. 2 homologue binds to vascular endothelial growth factor receptor-2 via C-terminal loop region. Biochem. J. 411, 515-522.
42. 2: role of negatively-charged phospholipids as potential membrane binding sites. Arch. Biochem. Biophys. 391, 56-64.
43. Barchan, D., Kachalsky, S., Neumann, D., Vogel, Z., Ovadia, M., Kochva, E. and Fuchs, S. (1992) How the mongoose can fight the snake: the binding site of the mongoose acetylcholine receptor. Proc. Natl. Acad. Sci. USA 89, 7717-7721.
44. Takacs, Z., Wilhelmsen, K. C. and Sorota, S. (2001) Snake alpha-neurotoxin binding site on the Egyptian cobra (Naja haje) nicotinic acetylcholine receptor is conserved. Mol. Biol. Evol. 18, 1800-1809.
45. Tsai, I. H. and Wang, Y. M. (1998) Effect of site directed mutagenesis on the activity of recombinant trimucrotoxin, a neurotoxic phospholipase from Trimeresurus mucrosquamatus venom. Toxicon 36, 1591-1597.
46. 2 by scanning alanine mutagenesis. Biochim. Biophys. Acta 1768, 1247-1257.
47. 2+-independent membrane-damaging activity and increases its toxicity. Biochemistry 46, 12795-12809.
48. Ivanovski, G., Petan, T., Križaj, I., Gelb, M. H., Gubenšek, F. and Pungerčar J. (2004) Basic amino acid residues in the beta-structure region contribute, but not critically, to presynaptic neurotoxicity of ammodytoxin A. Biochim. Biophys. Acta 1702, 217-225.
49. 2 neurotoxins and lysophospholipid-fatty acid mixtures. Science 310, 1678-1680.
50. Caccin, P., Rigoni, M., Bisceglie, A., Rossetto, O. and Montecucco, C. (2006) Reversible skeletal neuromuscular paralysis induced by different lysophospholipids. FEBS Lett. 580, 6317-6321.
51. Megighian, A., Rigoni, M., Caccin, P., Zordan, M. A. and Montecucco, C. (2007) A lysolecithin/fatty acid mixture promotes and then blocks neurotransmitter release at the Drosophila melanogaster larval neuromuscular junction. Neurosci. Lett. 416, 6-11.
52. 2 enzymes. Toxicon 42, 827-840.
53. Rossetto, O., Morbiato, L., Caccin, P., Rigoni, M. and Montecucco, C. (2006) Presynaptic enzymatic neurotoxins. J. Neurochem. 97, 1534-1545.
54. Prasarnpun, S., Walsh, J. and Harris, J. B. (2004) Beta-bungarotoxin- induced depletion of synaptic vesicles at the mammalian neuromuscular junction. Neuropharmacology 47, 304-314.
55. Chernomordik, L. V., Leikina, E., Frolov, V., Bronk, P. and Zimmerberg, J. (1997) An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids. J. Cell Biol. 136, 81-93.
56. Chernomordik, L. V. and Kozlov, M. M. (2003) Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72, 175-207.
57. Chernomordik, L. V., Zimmerberg, J. and Kozlov, M. M. (2006) Membranes of the world unite! J. Cell Biol. 175, 201-207.
58. 2 stimulates exocytosis and neurotransmitter release in pheochromocytoma-12 cells and cultured rat hippocampal neurons. Neuroscience 121, 891-898.
59. 2 activity induce punctate swellings of neurites and exocytosis of synaptic vesicles. J. Cell Sci. 117, 3561-3570.
60. Bonanomi, D., Pennuto, M., Rigoni, M., Rossetto, O. and Montecucco, C. (2005) Taipoxin induces synaptic vesicle exocytosis and disrupts the interaction of synaptophysin Iwith VAMP2. Mol. Pharmacol. 67, 1901-1908.
61. Rizzoli, S. O. and Betz, W. J. (2005) Synaptic vesicle pools. Nat. Rev. Neurosci. 6, 57-69.
62. 2+ accumulation in rat cardiac myocytes. Am J Physiol. 244:H32-8.
63. Woodley, S. L., Ikenouchi, H. and Barry, W. H. (1991) Lysophosphatidylcholine increases cytosolic calcium in ventricular myocytes by direct action on the sarcolemma. J. Mol. Cell. Cardiol. 23, 671-680.
64. Leung, Y. M., Xion, Y., Ou, Y. J. and Kwan, C. Y. (1998) Perturbation by lysophosphatidylcholine of membrane permeability in cultured vascular smooth muscle and endothelial cells. Life Sci. 63, 965-973.
65. Wilson-Ashworth, H. A., Judd, A. M., Law, R. M., Freestone, B. D., Taylor, S., Mizukawa, M. K., Cromar, K. R., Sudweeks, S. and Bell, J. D. (2004) Formation of transient non-protein calcium pores by lysophospholipids in S49 lymphoma cells. J. Membr. Biol. 200, 25-33.
66. 2+ mobilization in N2a mouse and SH-SY5Y human neuroblastoma cells. Neurosci. Lett. 424, 22-26.
67. Rugolo, M., Dolly, J. O. and Nicholls, D. G. (1986) The mechanism of action of beta-bungarotoxin at the presynaptic plasma membrane. Biochem. J. 233, 519-523.
68. Rigoni, M., Pizzo, P., Schiavo, G., Weston, A. E., Zatti, G. Caccin, P., Rossetto, O., Pozzan, T. and Montecucco, C. (2007) Calcium influx and mitochondrial alterations at synapses exposed to snake neurotoxins or their phospholipid hydrolysis products. J. Biol. Chem. 282, 11238-11245.
69. 2+-dependent recycling of synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 87, 297-303.
70. Ushkaryov, Y. A., Volynski, K. E. and Ashton, A. C. (2004) The multiple actions of black widow spider toxins and their selective use in neurosecretion studies. Toxicon 43, 527-542.
71. Ong, W. L., Jiang, B., Tang, N., Ling, S. F., Yeo, J. F., Wei, S., Farooqui, A. A. and Ong W. Y. (2006) Differential effects of polyunsaturated fatty acids on membrane capacitance and exocytosis in rat pheochromocytoma-12 cells. Neurochem. Res. 31, 41-48.
72. Rickman C, Davletov B (2005) Arachidonic acid allows SNARE complex formation in the presence of Munc18. Chem. Biol. 12, 545-553.
73. Latham CF, Osborne SL, Cryle MJ, Meunier FA. (2007) Arachidonic acid potentiates exocytosis and allows neuronal SNARE complex to interact with Munc18a. J Neurochem. 100, 1543-1554.
74. Darios F, Davletov B (2006) Omega-3 and omega-6 fatty acids stimulate cell membrane expansion by acting on syntaxin 3. Nature 440, 813-817.
75. Bernardi, P., Penzo, D. and Wojtczak, L. (2002) Mitochondrial energy dissipation by fatty acids. Mechanisms and implications for cell death. Vitam. Horm. 65, 97-126.
76. Wernicke, J. F., Vanker, A. D. and Howard, B. D. (1975) The mechanism of action of beta-bungarotoxin. J. Neurochem. 25, 483-496.
77. Fletcher, J. E., Hubert, M., Wieland, S. J., Gong, Q. H. and Jiang, M. S. (1996) Similarities and differences in mechanisms of cardiotoxins, melittin and other myotoxins. Toxicon 34, 1301-1311.
78. 2 homologue from Bothrops jararacussu snake venom. Int. J. Biochem. Cell Biol. 34, 668-677.
79. Gutiérrez, J. M., Ownby, C. L. and Odell, G. V. (1984) Isolation of a myotoxin from Bothrops asper venom: partial characterization and action on skeletal muscle. Toxicon 22, 115-128.
80. Pestronk, A., Parhad, I. M., Drachman, D. B. and Price, D. L. (1982) Membrane myopathy: morphological similarities to Duchenne muscular dystrophy. Muscle Nerve 5, 209-214.
81. 2: biological and membrane-disrupting activities in the absence of catalysis. Biochem. J. 362, 89 -96.
82. Falconi, M., Desideri, A. and Rufini, S. (2000) Membrane-perturbing activity of Viperidae myotoxins: an electrostatic surface potential approach to a puzzling problem. J. Molec. Recogn. 13, 14-19.
83. 2s. Toxicon 42, 903-913.
84. 2 homologue. Toxicon 51, 80-92.
85. 2, anticoagulant and myotoxic activities. Biochim. Biophys. Acta 1070, 455-460.
86. Rufini, S., Cesaroni, P., Desideri, A., Farias, R., Gubensek, F., Gutiérrez, J. M., Luly, P., Massoud, R., Morero, R. and Pedersen, J. Z. (1992) Calcium ion independent membrane leakage induced by phospholipase-like myotoxins. Biochemistry 31, 12424-12430.
87. 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, 29867-29873.
88. 2 expresses enhanced membrane-damaging activities and reproduces its in vivo myotoxic effect. Biochim. Biophys. Acta 1461, 19-26.
89. 2 from Bothrops asper snake venom: synthetic Lys49 myotoxin II-(115-129)-peptide identifies its bactericidal region. Eur. J. Biochem. 253, 452-461.
90. 2 from Agkistrodon piscivorus piscivorus snake venom: synthetic C-terminal peptides from Lys49, but not from Asp49 myotoxins, exert membrane-damaging activities. Toxicon 39, 1587-1594.
91. 2 from snake venoms. Toxicon 42, 307-312.
92. 2. Biochem. J. 366, 971-976.
93. 2 homologue. Prot. Struct. Funct. Genet. 30, 442-454.
94. 2: quaternary structure and inhibition mechanism insights. Biochem. Biophys. Res. Comm. 311, 713-720.
95. 2 homologues are reduced, but not abolished, by a pH-induced dissociation. Toxicon 46, 291-296.
96. 2 activity based on ligand-induced conformational change. J. Biol. Chem. 280, 7326-7335.
97. 2, affects its pharmacological activities. Toxicon 31, 1202-1206.
98. 2 from Bothrops pirajai snake venom. Arch. Biochem. Biophys. 387, 188-196.
99. Lomonte, B., Lundgren, J., Johansson, B. and Bagge, U. (1994) The dynamics of local tissue damage induced by Bothrops asper snake venom and myotoxin II on the mouse cremaster muscle: an intravital and electron microscopic study. Toxicon 32, 41-55.
100. 2 isolated from Bothrops asper and Bothrops godmani snake venoms: effects on enzymatic and pharmacological properties. Toxicon 35, 241-252.
101. 2, on liposomes and mouse gastrocnemius muscle. Toxicon 31, 217-222.
102. 2 complex. Toxicon 22, 85-98.
103. Harris, J. B. and Maltin, C. A. (1982) Myotoxic activity of the crude venom and the principal neurotoxin, taipoxin, of the Australian taipan, Oxyuranus scutellatus. Br. J. Pharmacol. 76, 61-75.
104. Gutiérrez, J. M., Ownby, C. L. and Odell, G. V. (1984) Pathogenesis of myonecrosis induced by crude venom and a myotoxin of Bothrops asper. Exp. Mol. Pathol. 40, 367-379.
105. Heluany, N. F., Homsi-Brandeburgo, M. I., Giglio, J. R., Prado-Franceschi, J. and Rodrigues-Simioni, L. (1992) Effects induced by bothropstoxin, a component from Bothrops jararacussu snake venom, on mouse and chick muscle preparations. Toxicon 30, 1203-1210.
106. Melo, P. A., Burns, C. F., Blankemeyer, J. T. and Ownby, C. L. (2004) Membrane depolarization is the initial action of crotoxin on isolated murine skeletal muscle. Toxicon 43, 111-119.
107. Han, R. and Campbell, K. P. (2007) Dysferlin and muscle membrane repair. Curr. Opin. Cell Biol. 19, 409-416.
108. 2+: molecular determinants and functional consequences. Physiol Rev. 86, 369-408.
109. Clapham, D. E. (2007) Calcium signalling. Cell 131, 1047-1058
110. Harris, J. B. and Cullen, M. J. (1990) Muscle necrosis caused by snake venoms and toxins. Electron Microsc. Rev. 3, 183-211.
111. Chen, I. L. and Lee, C. Y. (1970) Ultrastructural changes in the motor nerve terminals caused by beta-bungarotoxin. Virchows Arch. B Cell Pathol. 6, 318-325.
112. Cull-Candy, S. G., Fohlman, J., Gustavsson, D., Lullmann-Rauch, R. and Thesleff, S. (1976) The effect of taipoxin and notexin on the function and fine structure of the murine neuromuscolar junction. Neuroscience 1, 175-180.
113. Dixon, R. W and Harris, J. B. (1999) Nerve terminal damage by β-Bungarotoxin: its clinical significance. Am. J. Pathol 154, 447-455.
114. Bernardi, P. and Rasola, A. (2007) Calcium and cell death: the mitochondrial connection. Subcell Biochem. 45, 481-506.
115. Bertipaglia, I. and Carafoli, E. (2007) Calpains and human disease. Subcell Biochem. 45, 29-53.
116. Gutiérrez, JM, Arce, V., Brenes, F. and Chaves, F. (1990) Changes in myofibrillar components after skeletal muscle necrosis induced by a myotoxin isolated from the venom of the snake Bothrops asper. Exp. Mol. Pathol. 52, 25 -36.
117. Vater, R., Cullen, M. J. and Harris, J. B. (1992) The fate of desmin and titin during the degeneration and regeneration of the soleus muscle of the rat. Acta Neuropathol. 84, 278-288.
118. Teixeira, C. F. P., Zamunér, S. R., Zuliani, J. P., Fernandes, C. M., Cruz-Hofling, M. A., Fernandes, I., Chaves, F. and Gutiérrez, J. M. (2003) Neutrophils do not contribute to local tissue damage, but play a key role in skeletal muscle regeneration, in mice injected with Bothrops asper snake venom. Muscle & Nerve 28, 449-459.
119. Herkert, M., Shakhman, O., Schweins, E. and Becker, C. M. (2001) Beta-bungarotoxin is a potent inducer of apoptosis in cultured rat neurons by receptor-mediated internalization. Eur. J. Neurosci. 14, 821-828.
120. Neco, P., Rossetto, O., Gil, A., Montecucco, C. and Gutiérrez, L. M. (2003) Taipoxin induces F-actin fragmentation and enhances release of catecholamines in bovine chromaffin cells. J Neurochem. 85, 329-337.
121. 2, can act in the cytosol of the nerve cell. Biochem. Biophys. Res. Commun. 324, 981-985.
122. Wagner, G. M., Mart, P. E. and Kelly, R. B. (1974) Beta-bungarotoxin inhibition of calcium accumulation by rat brain mitochondria. Biochem. Biophys. Res. Commun. 58, 475-481.
123. 2 on guinea-pig synaptosomes. Biochem. J. 229, 653-662
124. 2, notexin and taipoxin. Exp. Neurol. 161, 517-526.
125. Duchen, L. W., Gomez, S. and Queiroz, L. S. (1981) The neuromuscular junction of the mouse after black widow spider venom J. Physiol. 316, 279-291.
126. 2 in skeletal muscle. J. Biol. Chem. 265, 9526-9532.
127. 2. Biochemistry 34, 13146-13151.
128. 2 homologues: dissociation between enzymatic and biological activities. Eur. J. Pharmacol. 343, 257-263.
129. 2. Toxicon 38, 199-208.
130. Melo, P. A., Homsi-Brandeburgo, M. I., Giglio, J. R. and Suarez-Kurtz, G. (1993) Antagonism of the myotoxic effects of Bothrops jararacussu venom and bothropstoxin by polyanions. Toxicon 31, 285-291.
131. 2 from Bothrops asper snake venom by glycosaminoglycans of the heparin/heparan sulfate family. Biochem. Pharmacol. 47, 1509-1518.
132. Metz, M., Piliponsky, A. M., Chen, C. C., Lammel, V., Abrink, M., Pejler, G., Tsai, M. and Galli, S. J. (2006) Mast cells can enhance resistance to snake and honeybee venoms. Science 313, 526-530.
133. 2 myotoxin inhibitor proteins from snakes, mammals and plants. Toxicon 42, 963-977.
134. 2 and the regeneration of skeletal muscles. Toxicon 42, 933-945.
135. Son, Y. J., Trachtenberg, J. T., Thompson, W. J. (1996) Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. Trends Neurosci. 19, 280-285.
136. Gutiérrez, J. M., Ownby, C. L. and Odell, G. V. (1984) Skeletal muscle regeneration after myonecrosis induced by crude venom and a myotoxin from the snake Bothrops asper (Fer-de-Lance). Toxicon 22, 719-731.
137. Gutiérrez, J. M., Romero, M., Núñez, J., Chaves, F., Borkow, G. and Ovadia, M. (1995) Skeletal muscle necrosis and regeneration after injection of BaH1, a hemorrhagic metalloproteinase isolated from the venom of the snake Bothrops asper (terciopelo). Exp. Mol. Pathol. 62, 28-41.
138. 2 from Vipera ammodytes ammodytes venom. Biochim. Biophys. Acta 828, 306-312.
139. Wu, P. F. and Chang, L. S. (2000) Genetic organization of A chain and B chain of beta-bungarotoxin from Taiwan banded krait (Bungarus multicinctus). A chain genes and B chain genes do not share a common origin. Eur. J. Biochem. 267, 4668-4675.
140. Kondo, K., Toda, H., Narita, K. and Lee, C. Y. (1982) Amino acid sequence of beta 2-bungarotoxin from Bungarus multicinctus venom. The amino acid substitutions in the B chains. J. Biochem. 91, 1519-1530.
141. Sutcliffe, M. J., Dobson, C. M. and Oswald, R. E. (1992) Solution structure of neuronal bungarotoxin determined by two-dimensional NMR spectroscopy: calculation of tertiary structure using systematic homologous model building, dynamical simulated annealing, and restrained molecular dynamics. Biochemistry 31, 2962-2970.
142. Lind, P. and Eaker, D. (1982) Amino-acid sequence of the alpha-subunit of taipoxin, an extremely potent presynaptic neurotoxin from the Australian snake taipan (Oxyuranus s. scutellatus). Eur. J. Biochem. 124, 441-447.
143. Pearson, J. A., Tyler, M. I., Retson, K. V. and Howden, M. E. (1993) 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 1161, 223-229.
144. Halpert, J. and Eaker, D. (1975) Amino acid sequence of a presynaptic neurotoxin from the venom of Notechis scutatus scutatus (Australian tiger snake). J. Biol. Chem. 250, 6990-6997.
145. 2 at 2.0 A resolution. FEBS Lett. 301, 159-164.
146. Aird, S. D., Kaiser, I. I., Lewis, R. V. and Kruggel, W. G. (1985) Rattlesnake presynaptic neurotoxins: primary structure and evolutionary origin of the acidic subunit. Biochemistry 24, 7054-7058.
147. Aird, S. D., Yates, J. R., Martino, P. A., Shabanowitz, J., Hunt, D. F. and Kaiser, I. I. (1990) The amino acid sequence of the acidic subunit B-chain of crotoxin. Biochim. Biophys. Acta 1040, 217-224.
148. Kaiser, I. I., Gutiérrez, J. M., Plummer, D., Aird, S. D. and Odell, G. V. (1990) The amino acid sequence of a myotoxic phospholipase from the venom of Bothrops asper. Archs. Biochem. Biophys. 278, 319-325.
149. 2 activity. J. Protein Chem. 17, 381-386.
150. 2 with lysine in place of aspartate 49. J. Biol. Chem. 259, 13839-13843.
151. Dhillon, D. S., Condrea, E., Maraganore, J. M., Heinrikson, R. L., Benjamin, S. and Rosenberg, P. (1987) Comparison of enzymatic and
152. 2 from the venom of the cottonmouth snake at 2.0-A resolution. J. Biol. Chem. 265, 17649-17656.
153. Johnson, E. K. and Ownby, C. L. (1993) Isolation of a myotoxin from the venom of Agkistrodon contortrix laticinctus (broad-banded copperhead) and pathogenesis of myonecrosis induced by it in mice. Toxicon 31, 243-255.
154. 2 myotoxin from Agkistrodon contortrix laticinctus snake venom. Archs. Biochem. Biophys. 326, 21 -30.
155. 2 homologue. Int. J. Biochem. Cell Biol. 32, 63-71.
156. 2 homologue. Int. J. Biochem. Cell Biol. 34, 1268-1278.
157. 2 homologue from Atropoides nummifer venom. Acta Cryst. F 62, 423-426.
158. Lomonte, B. and Gutiérrez, J. M. (1989) A new muscle damaging toxin, myotoxin II, from the venom of the snake Bothrops asper (terciopelo). Toxicon 27, 725-733.
159. 2. Archs. Biochem. Biophys. 284, 352-359.
160. Arni, R. K., Ward, R. J., Gutiérrez, J. M. and Tulinsky, A. (1995) Structure of a calcium-independent phospholipase-like myotoxic protein from Bothrops asper venom. Acta Cryst. D 51, 311-317.
161. Homsi-Brandeburgo, M. I., Queiroz, L. S., Santo-Neto, H., Rodrigues-Simioni, L. and Giglio, J. R. (1988) Fractionation of Bothrops jararacussu snake venom: partial chemical characterization and biological activity of bothropstoxin. Toxicon 26, 615-627.
162. Cintra, A. C. O., Marangoni, S., Oliveira, B. and Giglio, J. R. (1993) Bothropstoxin-I: amino acid sequence and function. J. Prot. Chem. 12, 57-64.
163. 2 homologues. Toxicon 49, 378-387.
164. Soares, A. M., Rodrigues, V. M., Homsi-Brandeburgo, M. I., Toyama, M. H., Lombardi, F. R., Arni, R. K. and Giglio, J. R. (1998) A rapid procedure for the isolation of the Lys-49 myotoxin II from Bothrops moojeni (caissaca) venom: biochemical characterization, crystallization, myotoxic and edematogenic activity. Toxicon 36, 503-514.
165. 2: crystal structure of myotoxin II from Bothrops moojeni complexed with stearic acid. Biochimie 87, 161-167.
166. 2 homologue: an example of function versatility of snake venom proteins. Comp. Biochem. Physiol. C 142, 371-381.
167. 2 homologue from Vipera ammodytes venom. Eur. J. Biochem. 202, 1165-1168.
168. 2 from the venom of Agkistrodon piscivorus piscivorus. J. Biol. Chem. 272, 3573-3582.