Comparative study of the cytolytic activity of snake venoms from African spitting cobras (Naja spp., Elapidae) and its neutralization by a polyspecific antivenom

Toxicon

Volumn 58, Issue 6-7, 2011, Pages 558-564

  Méndez, Ileana ^a   Gutiérrez, José María ^a   Angulo, Yamileth ^a   Calvete, Juan J ^b   Lomonte, Bruno ^a  

^a UNIVERSIDAD DE COSTA RICA   (Costa Rica)

^b INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

Antivenom; C2C12; Cardiotoxin; Cytotoxicity; Naja; Neutralization; Snake venom

Indexed keywords

ECHITAB PLUS ICP; FUCOIDIN; NEUTRALIZING ANTIBODY; PHOSPHOLIPASE A2; SNAKE VENOM; SNAKE VENOM ANTISERUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY PRODUCTION; ANTIBODY TITER; ARTICLE; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG INHIBITION; ENZYME INHIBITION; IMMUNOGENICITY; IN VITRO STUDY; MOUSE; NAJA KATIENSIS; NAJA MOSSAMBICA; NAJA NIGRICOLLIS; NAJA NUBIAE; NAJA PALLIDA; NONHUMAN; PRIORITY JOURNAL; SERODIAGNOSIS; SNAKE; SPECIES DIFFERENCE;

ANIMALS; ANTIVENINS; CELLS, CULTURED; COBRA; COBRA VENOMS; CYTOTOXINS; MICE; NEUTRALIZATION TESTS; POLYSACCHARIDES;

ELAPIDAE; EQUIDAE; NAJA; NAJA MOSSAMBICA; NAJA NIGRICOLLIS; NAJA NUBIAE; NAJA PALLIDA;

EID: 82555164910     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2011.08.018     Document Type: Article

References (57)

1. Abubakar S.B., Abubakar I.S., Habib A.G., Nasidi A., Durfa N., Yusuf P.O., Larnyang S., Garnvwa J.M., Sokomba E., Salako L., Laing G.D., Theakston R.D., Juszczak E., Alder N., Warrell D.A. Pre-clinical and preliminary dose finding and safety studies to identify candidate antivenoms for treatment of envenoming by saw-scaled or carpet vipers (Echis ocellatus) in northern Nigeria. Toxicon 2010, 55:719-723. Nigeria-UK EchiTab Study Group.
2. Abubakar I.S., Abubakar S.B., Habib A.G., Nasidi A., Durfa N., Yusuf P.O., Larnyang S., Garnvwa J.M., Sokomba E., Salako L., Theakston R.D., Juszczak E., Alder N., Warrell D.A. Randomised controlled double-blind non-inferiority trial of two antivenoms for saw-scaled or carpet viper (Echis ocellatus) envenoming in Nigeria. PLoS Negl. Trop. Dis. 2010, 4(7):e767. Nigeria-UK EchiTab Study Group.
3. 2. Biochem. Pharmacol. 2003, 66:1993-2000.
4. 2 myotoxins from crotalid snake venoms. Cell Biochem. Funct. 2005, 23:307-313.
5. Antúnez J., Fernández J., Lomonte B., Angulo Y., Calvete J.J., Gutiérrez J.M. Antivenomics of Atropoides mexicanus and Atropoides picadoi snake venoms: relationship to the neutralization of toxic and enzymatic activities. J. Venom Res. 2010, 1:8-17.
6. Azofeifa K., Angulo Y., Lomonte B. Ability of fucoidan to prevent muscle necrosis induced by snake venom myotoxins: comparison of high- and low-molecular weight fractions. Toxicon 2008, 51:373-380.
7. Bieber A.L., Ziolkowski C., d'Avis P.A. Rattlesnake toxins alter development of muscle cells in culture. Ann. N.Y. Acad. Sci. 1994, 710:126-145.
8. Brusés J.L., Capaso J., Katz E., Pilar G. Specific in vitro biological activity of snake venom myotoxins. J. Neurochem. 1993, 60:1030-1042.
9. 2 isolated from Bothrops asper (terciopelo) venom. Biochim. Biophys. Acta 1993, 1179:253-259.
10. Calvete J.J., Sanz L., Angulo Y., Lomonte B., Gutiérrez J.M. Venom, venomics, antivenomics. FEBS Lett. 2009, 583:1736-1743.
11. Calvete J.J., Cid P., Sanz L., Segura A., Villalta M., Herrera M., León G., Harrison R.A., Durfa N., Nasidi A., Theakston R.D.G., Warrell D.A., Gutiérrez J.M. Antivenomic assessment of the immunological reactivity of EchiTAb-Plus-ICP, an antivenom for the treatment of snakebite envenoming in sub-Saharan Africa. Am. J. Trop. Med. Hyg. 2010, 82:1194-1201.
12. Casasola A., Ramos-Cerrillo B., de Roodt A.R., Carbajal A., Chippaux J.P., Alagón A., Stock R.P. Paraspecific neutralization of the venom of African species of cobra by an equine antiserum against Naja melanoleuca: a comparative study. Toxicon 2009, 53:602-608.
13. Chippaux J.P. Snake-bites: appraisal of the global situation. Bull. W.H.O. 1998, 76:515-524.
14. Chippaux J.P. Snakebite in Africa. Current situation and urgent needs. Handbook of Venoms and Toxins of Reptiles 2010, 453-473. CRC Press, Boca Raton. S.P. Mackessy (Ed.).
15. 2 polyvalent equine antivenom for African snake bites in Benin. Am. J. Trop. Med. Hyg. 2007, 77:538-546.
16. 2 from cobra venom with cytotoxic properties not related to esterase activity. J. Biol. Chem. 1989, 264:13289-13297.
17. Cintra-Francischinelli M., Pizzo P., Rodrigues-Simioni L., Ponce-Soto L.A., Rossetto O., Lomonte B., Gutiérrez J.M., Pozzan T., Montecucco C. Calcium imaging of muscle cells treated with snake myotoxins reveals toxin synergism and presence of acceptors. Cell. Mol. Life Sci. 2009, 66:1718-1728.
18. Fernández J., Alape-Girón A., Angulo Y., Sanz L., Gutiérrez J.M., Calvete J.J., Lomonte B. Venomic and antivenomic analyses of the Central American coral snake, Micrurus nigrocinctus (Elapidae). J. Proteome Res. 2011, 10:1816-1827.
19. Fry B.G., Wüster W., Kini R.M., Brusic V., Khan A., Venkataraman D., Rooney A.P. Molecular evolution and phylogeny of elapid snake venom three-finger toxins. J. Mol. Evol. 2003, 57:110-129.
20. 2 antibodies anti-african snake venom. Afr. J. Biotech. 2010, 9:2446-2455.
21. Gutiérrez J.M., Rojas G., Lomonte B., Gené J.A., Chaves F., Alvarado J., Rojas E. Standardization of assays for testing the neutralizing ability of antivenoms. Toxicon 1990, 28:1127-1129.
22. Gutiérrez J.M., Rojas E., Quesada L., León G., Núñez J., Laing G.D., Sasa M., Renjifo J.M., Nasidi A., Warrell D.A., Theakston R.D.G., Rojas G. Pan-African polyspecific antivenom produced by caprylic acid purification of horse IgG: an alternative to the antivenom crisis in Africa. Trans. Royal Soc. Trop. Med. Hyg. 2005, 99:468-475.
23. Gutiérrez J.M., Theakston R.D.G., Warrell D.A. Confronting the neglected problem of snake bite envenoming: the need for a global partnership. PLoS Med. 2006, 3(6):e150.
24. Gutiérrez J.M., Lomonte B., León G., Rucavado A., Chaves F., Angulo Y. Trends in snakebite envenomation therapy: scientific, technological and public health considerations. Curr. Pharm. Des 2007, 13:2935-2950.
25. Gutiérrez J.M., Lomonte B., León G., Alape-Girón A., Flores-Díaz M., Sanz L., Calvete J.J., Angulo Y. Proteomic tools in the design and control of antivenoms for the treatment of snakebite envenomings. J. Proteomics 2009, 72:165-182.
26. Harvey A.L. Cytolytic toxins. Handbook of Toxinology 1990, 48-53. Marcel Dekker, New York. W.R. Shier, D. Mebs (Eds.).
27. Hodges S.J., Agbaji A.S., Harvey A.L., Hider R.C. Cobra cardiotoxins. Purification, effects on skeletal muscle and structure/activity relationships. Eur. J. Biochem. 1987, 165:373-383.
28. Incerpi S., de Vito P., Luly P., Rufini S. Effect of ammodytin L from Vipera ammodytes on L-6 cells from rat skeletal muscle. Biochim. Biophys. Acta 1995, 1268:137-142.
29. Kalam Y., Isbister G.K., Mirtshin P., Hodgson W.C., Konstantakopoulos N. Validation of a cell-based assay to differentiate between the cytotoxic effects of elapid snake venoms. J. Pharmacol. Toxicol. Methods 2011, 63:137-142.
30. Kasturiratne A., Wickremasinghe R., de Silva N., Gunawardena N.K., Pathmeswaran A., Premaratna R., Savioli L., Lalloo D.G., de Silva H.J. The global burden of snakebite: a literature analysis and modelling based on regional estimates of envenoming and deaths. PLoS Med. 2008, 5(11):e218.
31. Laing G.D., Renjifo J.M., Ruiz F., Harrison R.A., Nasidi A., Gutiérrez J.M., Rowley P.D., Warrell D.A., Theakston R.D.G. A new Pan African polyspecific antivenom developed in response to the antivenom crisis in Africa. Toxicon 2003, 42:35-41.
32. Li S., Wang J., Zhang X., Ren Y., Wang N., Zhao K., Chen X., Zhao C., Li X., Shao J., Yin J., West M.B., Xu N., Liu S. Proteomic characterization of two snake venoms: Naja naja atra and Agkistrodon halys. Biochem. J. 2004, 384:119-127.
33. 2 depends on heparin chain length and amino acid specificity. FEBS Lett. 1999, 453:395-399.
34. 2 of Bothrops asper snake venom. Toxicon 1994, 32:1359-1369.
35. 2 from Bothrops asper snake venom by glycosaminoglycans of the heparin/heparan sulfate family. Biochem. Pharmacol. 1994, 47:1509-1518.
36. 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. 1994, 269:29867-29873.
37. 2 on mouse endothelial (tEnd) and skeletal muscle (C2C12) cells in vitro. Toxicon 1999, 37:145-158.
38. Lomonte B., Escolano J., Fernández J., Sanz L., Angulo Y., Gutiérrez J.M., Calvete J.J. Snake venomics and antivenomics of the arboreal neotropical pitvipers Bothriechis lateralis and Bothriechis schlegelii. J. Proteome Res. 2008, 7:2445-2457.
39. Lomonte B., León G., Angulo Y., Rucavado A., Núñez V. Neutralization of Bothrops asper venom by antibodies, natural products and synthetic drugs: contributions to understanding snakebite envenomings and their treatment. Toxicon 2009, 54:1012-1028.
40. Melo P.A., Homsi-Brandeburgo M.I., Giglio J.R., Suarez-Kurtz G. Antagonism of the myotoxic effect of Bothrops jararacussu venom and bothropstoxin by polyanions. Toxicon 1993, 31:285-291.
41. Nawarak J., Sichaikul S., Wu C.Y., Liau M.Y., Phutrakul S., Chen S.T. Proteomics of snake venoms from Elapidae and Viperidae families by multidimensional chromatographic methods. Electrophoresis 2003, 24:2838-2854.
42. Olamendi-Portugal T., Batista C.V.F., Restano-Cassulini R., Pando V., Villa-Hernandez O., Zavaleta-Martinez A., Salas-Arruz M., Rodríguez de la Vega R.C., Becerril B., Possani L.D. Proteomic analysis of the venom from the fish eating coral snake Micrurus surinamensis: novel toxins, their functions and phylogeny. Proteomics 2008, 8:1919-1932.
43. Ownby C.L., Fletcher J.E., Colberg T.R. Cardiotoxin 1 from cobra (Naja naja atra) venom causes necrosis of seletal muscle in vivo. Toxicon 1993, 31:697-709.
44. Patel H.V., Vyas A.A., Vyas K.A., Liu Y.S., Chiang C.M., Chi L.M., Wu W.G. Heparin and heparan sulfate bind to snake cardiotoxin. J. Biol. Chem. 1997, 272:1484-1492.
45. Petras D., Sanz L., Segura A., Herrera M., Villalta M., Solano D., Vargas M., León G., Warrell D.A., Theakston R.D.G., Harrison R.A., Durfa N., Nasidi A., Gutiérrez J.M., Calvete J.J. Snake venomics of African spitting cobras: toxin composition and assessment of congeneric cross-reactivity of the Pan-African EchiTAb-Plus-ICP antivenom by antivenomics and neutralization approaches. J. Proteome Res. 2011, 10:1266-1280.
46. Ramos-Cerrillo B., de Roodt A.R., Chippaux J.P., Olguín L., Casasola A., Guzmán G., Paniagua-Solís J., Alagón A., Stock R.P. Characterization of a new polyvalent antivenom (Antivipmyn-Africa) against African vipers and elapids. Toxicon 2008, 52:881-888.
47. Rees B., Samama J.P., Thierry J.C., Gilibert M., Fischer J., Schweitz H., Lazdunski M., Moras D. Crystal structure of a snake venom cardiotoxin. Proc. Natl. Acad. Sci. USA 1987, 84:3132-3136.
48. Segura A., Villalta M., Herrera M., León G., Harrison R., Durfa N., Nasidi A., Calvete J.J., Theakston R.D., Warrell D.A., Gutiérrez J.M. Preclinical assessment of the efficacy of a new antivenom (EchiTAb-Plus-ICP) for the treatment of viper envenoming in sub-Saharan Africa. Toxicon 2010, 55:369-374.
49. Stock R.P., Massougbodji A., Alagón A., Chippaux J.P. Bringing antivenoms to sub-Saharan Africa. Nat. Biotech. 2007, 25:173-177.
50. Theakston R.D.G., Reid H.A. Development of simple standard assay procedures for the characterization of snake venoms. Bull. W.H.O. 1983, 61:949-956.
51. Vyas A.A., Pan J.J., Patel H.V., Vyas K.A., Chiang C.M., Sheu Y.C., Hwang J.K., Wu W.G. Analysis of binding of cobra cardiotoxins to heparin reveals a new β-sheet heparin-binding structural motif. J. Biol. Chem. 1997, 272:9661-9670.
52. Warrell D.A. Clinical toxicology of snakebite in Africa and the Middle East/Arabian peninsula. Handbook of Clinical Toxicology of Animal Venoms and Toxins 1995, 433-492. CRC Press, Boca Raton. J. Meier, J. White (Eds.).
53. Warrell D.A. Clinical features of envenoming from snake bites. Envenomings and Their Treatments 1996, 63-76. Fondation Marcel Mérieux, Lyon. C. Bon, M. Goyffon (Eds.).
54. Warrell D.A. Snake bite. Lancet 2010, 375:77-88.
55. World Health Organization Progress in the Characterization of Venoms and Standardization of Antivenoms 1981, vol. 58. W.H.O. Offset Publications, Geneva, W.H.O.
56. World Health Organization Guidelines for the Prevention and Clinical Management of Snakebite in Africa 2010, W.H.O. Regional Office for Africa, WHO/AFR/EDM/EDP/10.01.
57. World Health Organization WHO Guidelines for the Production, Control and Regulation of Snake Antivenom Immunoglobulins 2010, http://www.who.int/bloodproducts/snakeantivenoms.