Calcium imaging of muscle cells treated with snake myotoxins reveals toxin synergism and presence of acceptors

Cellular and Molecular Life Sciences

Volumn 66, Issue 10, 2009, Pages 1718-1728

  Cintra Francischinelli, M ^a   Pizzo, P ^a   Rodrigues Simioni, L ^b   Ponce Soto, L A ^b   Rossetto, O ^a   Lomonte, B ^c   Gutierrez J M ^c   Pozzan, T ^a   Montecucco, C ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c UNIVERSIDAD DE COSTA RICA   (Costa Rica)

Author keywords

Calcium imaging; Myoblasts; Myotubes; PLA2; Snake myotoxins

Indexed keywords

ASPARTIC ACID; CALCIUM; LYSINE; MYOTOXIN; PHOSPHOLIPASE A2; SNAKE VENOM; TOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CELL DEATH; CELL MEMBRANE PERMEABILITY; CELL VIABILITY; CYTOTOXICITY; ENZYME ACTIVITY; MOUSE; MYOBLAST; MYOTUBE; NONHUMAN; SNAKE;

ANIMALS; BOTHROPS; CALCIUM; CELL LINE; CELL SURVIVAL; CROTALID VENOMS; MURINAE; MUSCLE FIBERS, SKELETAL; MYOBLASTS;

BOTHROPS;

EID: 67650665793     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-009-9053-2     Document Type: Article

References (46)

1. Azevedo-Marques, M. M., Cupo, P., Coimbra, T. M., Hering, S. E., Rossi, M. A. and Laure, C. J. (1985) Myonecrosis, myoglobinuria and acute renal failure induced by South American rattlesnake (Crotalus durissus terrificus) envenomation in Brazil. Toxicon 23, 631-636.
2. Azevedo-Marques, M. M., Hering, S. E. and Cupo, P. (1987) Evidence that Crotalus durissus terrificus (South American rattlesnake) envenomation in humans causes myolysis rather than hemolysis. Toxicon 25, 1163-1168.
3. Lomonte, B., Angulo, Y. and Calderón, L. (2003) An. overview of lysine-49 phospholipase A.2 myotoxins from crotalid snake venoms and their structural, determinants of myotoxic action. Toxicon 42, 885-901.
4. 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 Med. 3, e150.
5. Aragón E and Gubensek, F. (1981) Bothrops asper venom from the Atlantic and Pacific zones of Costa Rica. Toxicon 19, 797805.
6. Prado-Franceschi, J., Hyslop, S., Cogo, J. C., Andrade, A. L., Assakura, M. T., Reichl, A, P., Cruz-Höfling, M. A. and Rodrigues-Simioni, L. (1998) Characterization of a myotoxin from the Duvemoy's gland secretion of the xenodontine colubrid Philodryas olfersii (green snake): effects on striated muscle and the neuromuscular junction. Toxicon 36, 14071421,
7. Alape-Girón, A., Sanz, L., Escolano, J., Flores-Diaz, M., Madrigal, M., Sasa, M. and Calvete, J. J. (2008) Snake venomics of the lancehead pitviper Bothrops asper: geographic, individual, and ontogenetic variations. J. Proteome Res. 7, 3556-3571.
8. Warrell, D. A, (2004) Snakebites in Central and South. America: Epidemiology, clinical, features and clinical management. In : The Venomous Reptiles of the Western Hemisphere, pp. 709-761, Campbell J. A. and Lamar W W (ed.), Ithaca, Comstock.
9. Gutiérrez, J. M. and Ownby, G. L. (2003) Skeletal muscle degeneration induced by venom phospholipases A2: insights into the mechanisms of local and systemic myotoxicity. Toxicon 42, 915-931.
10. Chioato, L. and Ward, R. J. (2003) Mapping structural determinants of biological, activities in snake venom, phospholipases A.2 by sequence analysis and site directed mutagenesis. Toxicon 42, 869-883.
11. Montecucco, C., Gutierrez J. M. and Lomonte B. (2008) Cellular pathology induced by snake venom phospholipase A2 myotoxins and neurotoxins: common aspects of their mechanisms of action. Cell. Mol. Life Sci. 65, 2897-2912.
12. Ami, R. K. and Ward, R. J. (1996) Phospholipase A2- a structural review. Toxicon 34, 827-841.
13. Lomonte, B., Angulo, Y., Sasa, M. and Gutiérrez, J. M. (2008) The phospholipase A2 homologues of snake venoms: biological activities and their possible adaptive roles. Prot. Pept. Lett., in press.
14. Kini, R. M. (2003) Excitement ahead: structure, function and mechanism of snake venom phospholipase A2 enzymes. Toxicon 42, 827-840.
15. Lambeau, G., Schmid-Alliana, A., Lazdunski, M. and Barhanin, J. (1990) Identification and purification of a very high, affinity binding protein for toxic phospholipases A2 in skeletal muscle. J. Biol. Chem. 265, 9526-9532.
16. Lambeau, G. and Lazdunski, M. (1999) Receptors for a growing family of secreted phospholipases A2. Trends Pharmacol. Sci. 20, 162-170.
17. Yamazaki, Y., Matsunaga, Y., Nakano Y. and Morita, T. (2005) Identification of vascular endothelial growth factor receptorbinding protein in the venom of eastern cottonmouth. A new role of snake venom myotoxic Lys49-phospholipase A.2. J. Biol. Chem. 280, 29989-29992.
18. Fujisawa, D., Yamazaki, Y., Lomonte, B. and Morita, T. (2008) Catalytically inactive phospholipase A2 homologue binds to vascular endothelial growth factor receptor-2 via a C-terminal. loop region. Biochem. J. 411, 515-522.
19. 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.
20. Miyabara, E. H., Baptista, I. L., Lomonte, B., Selistre-deAraújo, H. S., Gutiérrez, J. M. and Moriscot, A. S. (2006) Effect of calcineurin inhibitors on myotoxic activity of crotoxin and Bothrops asper phospholipase A2 myotoxins in vivo and in vitro. Comp. Biochem. Physiol. G. Toxicol. Pharmacol. 143, 284-294.
21. Angulo, Y. and Lomonte, B. (2005) Differential, susceptibility of C2C12 myoblasts and myotubes to group II phospholipase A2 myotoxins from crotalid snake venoms. Cell. Biochem. Funct. 23, 307-313.
22. Villalobos, J. C., Mora, R., Lomonte, B., Gutiérrez, J. M. and Angulo, Y. (2007) Cytotoxicity induced in myotubes by a Lys49 phospholipase A2 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.
23. 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.
24. Falconi, M., Desideri, A. and Rufini, S. (2000) Membraneperturbing activity of Viperidae myotoxins: an electrostatic surface potential approach to a puzzling problem. J. Mol. Recognit. 13, 14-19.
25. Diaz, C., León, G., Ruca vado, A., Rojas, H, Schroit, A. J. and Gutiérrez, J. M. (2001) Modulation of the susceptibility of human erythrocytes to snake venom myotoxic phospholipases A(2): role of negatively charged phospholipids as potential membrane binding sites. Arch. Biochem. Biophys. 391, 56-64.
26. Lomonte, B., Angulo, Y. and Santamaría, C. (2003) Comparative study of synthetic peptides corresponding to region 115 129 in Lys49 myotoxic phospholipases A2 from snake venoms. Toxicon 42, 307-312.
27. Mora, R., Maldonado, A., Valverde, B. and Gutiérrez, J. M. (2006) Calcium plays a key role in the effects induced by a snake venom Lys49 phospholipase A2 homologue on a lymphoblastoid cell line. Toxicon 47, 75-86.
28. 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.
29. 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 (Ferde-Lance). Toxicon 22, 115-128.
30. 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.
31. Ruller, R., Aragão, E. A., Chioato, L., Ferreira, T L., de Oliveira, A. H., Sa, J. M. and Ward, R. J. (2005) A predominant role for hydrogen bonding in the stability of the homodimer of bothropstoxin-I, A lysine 49-phospholipase A2. Biochimie. 87, 993-1003.
32. Rigoni, M., Caccin, P., Gschmeissner, S., Koster, G., Postle, A. D., Rossetto, O., Schiavo, G. and Montecucco, G. (2005) Equivalent effects of snake PLA2 neurotoxins and lysophospholipid-fatty acid mixtures. Science 310, 1678-1680.
33. Angulo, Y., Gutiérrez, J. M., Soares, A. M., Cho, W. and Lomonte, B. (2005) Myotoxic and cytolytic activities of dimeric Lys49 phospholipase A2 homologues are reduced, but not abolished, by a pH-induced dissociation. Toxicon 46, 291-296.
34. Lomonte, B., Angulo, Y., Rufini, S., Cho, W., Giglio, J. R., Ohno, M., Daniele, J. J., Geoghegan, P. and Gutiérrez, J. M. (1999) Comparative study of the cytolytic activity of myotoxic phospholipases A2 on mouse endothelial (tEnd) and skeletal muscle (C2C12) cells in vitro. Toxicon 37, 145-158.
35. Yaffe, D. and Saxel, O. (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270, 725-727.
36. Bernardi, P. and Rasóla, A. (2007) Calcium and cell death: the mitochondrial connection. Subcell. Biochem, 45, 481-506.
37. Bertipaglia, I. and Carafoli, E. (2007) Calpains and human disease. Subcell. Biochem. 45, 29-53.
38. Diaz, C., Gutiérrez, J. M., Lomonte, B. and Gené, J. A. (1991) The effect of myotoxins isolated from Bothrops snake venoms on multilamellar liposomes: relationship to phospholipase A2, anticoagulant and myotoxic activities. Biochim. Biophys. Acta 1070, 455-460.
39. Lomonte, B., Moreno, E., Tarkowski, A., Hanson, L. A. and Maccarana, M. (1994) Neutralizing interaction between heparins and myotoxin II, a lysine 49 phospholipase A2 from Bothrops asper snake venom. Identification of a heparinbinding and cytolytic toxin region by the use of synthetic peptides and molecular modeling. J. Biol. Chem. 269, 2986729873.
40. Chioato, L., De Oliveira, A. H. C., Ruller, R., Sa, J. M. and Ward, R. J. (2002) Distinct sites for myotoxic and membranedamaging activities in the C-terminal region of a Lys49phospholipase A2. Biochem. J. 366, 971-976.
41. Diaz-Oreiro, C. and Gutiérrez, J. M. (1997) Chemical modification of histidine and lysine residues of myotoxic phospholipases A2 isolated from Bothrops asper and Bothrops godmani snake venoms: effects on enzymatic and pharmacological properties. Toxicon 35, 241-252.
42. Soares, A. M., Andriao-Escarso, S. H., Bortoleto, R. K., Rodrigues-Simioni, L., Ami, R. K., Ward, R. J., Gutiérrez, J. M. and Giglio, J. R. (2001) Dissociation of enzymatic and pharmacological properties of piratoxins-I and -III, two myotoxic phospholipases A2 from Bothrops pirajai snake venom. Arch. Biochem. Biophys. 387, 188-19644
43. Diaz, C., Gutiérrez, J. M. and Lomonte, B. (1992) Isolation and characterization of basic myotoxic phospholipases A2 from. Bothrops godmani (Godman's pit viper) snake venom. Arch. Biochem. Biophys. 298, 135-142.
44. Gutiérrez, J. M. and Lomonte, B. (1995) Phospholipase A2 myotoxins from Bothrops snake venoms. Toxicon 33, 14051424.
45. Ohno, M., Chijiwa, T., Oda-Ueda, N., Ogawa, T. and Hattori, S. (2003) Molecular evolution of myotoxic phospholipases A2 from, snake venom. Toxicon 42, 841-854,
46. da Silva Giotto, M. T., Garratt, R. C., Oliva, G., Mascarenhas, Y. P., Giglio, J. R., Cintra, A. G. O., Azevedo, W F., Ami, R. K. and Ward, R. J. (1998) Crystallographic and spectroscopic characterization of a molecular hinge : conformational changes in bothropstoxin I, a dimeric Lys49-phospholipase A2 homologue. Proteins 30, 442-454.