Differential metalloprotease content and activity of three Loxosceles spider venoms revealed using two-dimensional electrophoresis approaches

Toxicon

Volumn 76, Issue , 2013, Pages 11-22

  Trevisan Silva, Dilza ^a   Bednaski, Aline Viana ^a   Gremski, Luiza Helena ^a   Chaim, Olga Meiri ^a   Veiga, Silvio Sanches ^a   Senff Ribeiro, Andrea ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

Author keywords

Astacin family; Loxosceles venom; Proteolytic activity; Two dimensional electrophoresis

Indexed keywords

FIBRINOGEN; METALLOPROTEINASE; SPIDER VENOM; PROTEOME;

ANALYTIC METHOD; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; LOXOSCELES; LOXOSCELES GAUCHO; LOXOSCELES INTERMEDIA; LOXOSCELES LAETA; MOLECULAR WEIGHT; NONHUMAN; POISONOUS SPIDER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; SPECIES COMPARISON; TWO DIMENSIONAL ELECTROPHORESIS; EXTRACELLULAR MATRIX; FEMALE; IMMUNOBLOTTING; MALE; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN EXPRESSION; ZYMOGRAPHY; ANIMAL; ASTACIN FAMILY; CHEMISTRY; COMPARATIVE STUDY; ENZYMOLOGY; LOXOSCELES VENOM; METABOLISM; SPECIES DIFFERENCE; SPIDER; TWO DIMENSIONAL GEL ELECTROPHORESIS; TWO-DIMENSIONAL ELECTROPHORESIS;

ASTACIN FAMILY; LOXOSCELES VENOM; PROTEOLYTIC ACTIVITY; TWO-DIMENSIONAL ELECTROPHORESIS;

ANIMALS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; MALE; METALLOPROTEASES; PROTEOME; SPECIES SPECIFICITY; SPIDER VENOMS; SPIDERS;

EID: 84884383469     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2013.08.065     Document Type: Article

References (52)

1. Appel M.H., Da Silveira R.B., Chaim O.M., Paludo K.S., Silva D.T., Chaves D.M., Da Silva P.H., Mangili O.C., Senff-Ribeiro A., Gremski W., Nader H.B., Veiga S.S. Identification, cloning and functional characterization of a novel dermonecrotic toxin (phospholipase D) from brown spider (Loxosceles intermedia) venom. Biochim. Biophys. Acta 2008, 1780:167-178.
2. Barbaro K.C., Sousa M.V., Morhy L., Eickstedt V.R., Mota I. Compared chemical properties of dermonecrotic and lethal toxins from spiders of the genus Loxosceles (Araneae). J. Protein Chem. 1996, 15:337-343.
3. Barbaro K.C., Knysak I., Martins R., Hogan C., Winkel K. Enzymatic characterization, antigenic cross-reactivity and neutralization of dermonecrotic activity of five Loxosceles spider venoms of medical importance in the Americas. Toxicon 2005, 45:489-499.
4. Bode W., Gomis-Rüth F.X., Huber R., Zwilling R., Stocker W. Structure of astacin and implications for activation of astacins and zinc-ligation of collagenases. Nature 1992, 358:164-167.
5. Bond J.S., Beynon R.J. The astacin family of metalloendopeptidases. Protein Sci. 1995, 4:1247-1261.
6. Bradford M.M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
7. Chaim O.M., Sade Y.B., Da Silveira R.B., Toma L., Kalapothakis E., Chavez-Olortegui C., Mangili O.C., Gremski W., Von Dietrich C.P., Nader H.B., Sanches Veiga S. Brown spider dermonecrotic toxin directly induces nephrotoxicity. Toxicol. Appl. Pharmacol. 2006, 211:64-77.
8. Chaim O.M., Trevisan-Silva D., Chaves-Moreira D., Wille A.C., Ferrer V.P., Matsubara F.H., Mangili O.C., Da Silveira R.B., Gremski L.H., Gremski W., Senff-Ribeiro A., Veiga S.S. Brown spider (Loxosceles genus) venom toxins: tools for biological Purposes. Toxins (Basel) 2011, 3:309-344.
9. Chaim O.M., Da Silveira R.B., Trevisan-Silva D., Ferrer V.P., Sade Y.B., Boia-Ferreira M., Gremski L.H., Gremski W., Senff-Ribeiro A., Takahashi H.K., Toledo M.S., Nader H.B., Veiga S.S. Phospholipase-D activity and inflammatory response induced by brown spider dermonecrotic toxin: endothelial cell membrane phospholipids as targets for toxicity. Biochim. Biophys. Acta 2011, 1811:84-96.
10. Chaves-Moreira D., Chaim O.M., Sade Y.B., Paludo K.S., Gremski L.H., Donatti L., De Moura J., Mangili O.C., Gremski W., Da Silveira R.B., Senff-Ribeiro A., Veiga S.S. Identification of a direct hemolytic effect dependent on the catalytic activity induced by phospholipase-D (dermonecrotic toxin) from brown spider venom. J. Cell Biochem. 2009, 107:655-666.
11. da Silva P.H., Da Silveira R.B., Appel M.H., Mangili O.C., Gremski W., Veiga S.S. Brown spiders and loxoscelism. Toxicon 2004, 44:693-709.
12. da Silveira R.B., Dos Santos Filho J.F., Mangili O.C., Veiga S.S., Gremski W., Nader H.B., Von Dietrich C.P. Identification of proteases in the extract of venom glands from brown spiders. Toxicon 2002, 40:815-822.
13. da Silveira R.B., Pigozzo R.B., Chaim O.M., Appel M.H., Dreyfuss J.L., Toma L., Mangili O.C., Gremski W., Dietrich C.P., Nader H.B., Veiga S.S. Molecular cloning and functional characterization of two isoforms of dermonecrotic toxin from Loxosceles intermedia (brown spider) venom gland. Biochimie 2006, 88:1241-1253.
14. da Silveira R.B., Wille A.C., Chaim O.M., Appel M.H., Silva D.T., Franco C.R., Toma L., Mangili O.C., Gremski W., Dietrich C.P., Nader H.B., Veiga S.S. Identification, cloning, expression and functional characterization of an astacin-like metalloprotease toxin from Loxosceles intermedia (brown spider) venom. Biochem. J. 2007, 406:355-363.
15. da Silveira R.B., Pigozzo R.B., Chaim O.M., Appel M.H., Silva D.T., Dreyfuss J.L., Toma L., Dietrich C.P., Nader H.B., Veiga S.S., Gremski W. Two novel dermonecrotic toxins LiRecDT4 and LiRecDT5 from brown spider (Loxosceles intermedia) venom: from cloning to functional characterization. Biochimie 2007, 89:289-300.
16. de Castro C.S., Silvestre F.G., Araujo S.C., Gabriel De M.Y., Mangili O.C., Cruz I., Chavez-Olortegui C., Kalapothakis E. Identification and molecular cloning of insecticidal toxins from the venom of the brown spider Loxosceles intermedia. Toxicon 2004, 44:273-280.
17. de Oliveira-Christoff A., De Oliveira A., Chaim O.M., Lugarini D., Bastos Pereira A.L., Paludo K.S., Queiroz Telles J.E., Bracht A., Veiga S.S., Acco A. Effects of the venom and the dermonecrotic toxin LiRecDT1 of Loxosceles intermedia in the rat liver. Toxicon 2008, 52:695-704.
18. dos Santos V.L., Franco C.R., Viggiano R.L., da Silveira R.B., Cantao M.P., Mangili O.C., Veiga S.S., Gremski W. Structural and ultrastructural description of the venom gland of Loxosceles intermedia (brown spider). Toxicon 2000, 38:265-285.
19. dos Santos L.D., Dias N.B., Pinto J.R.A.S., Palma M.S. Brown recluse spider venom: proteomic analysis and proposal of a putative mechanism of action. Protein Pept. Lett. 2009, 16:933-943.
20. Dumermuth E., Sterchi E.E., Jiang W.P., Wolz R.L., Bond J.S., Flannery A.V., Beynon R.J. The astacin family of metalloendopeptidases. J. Biol. Chem. 1991, 266:21381-21385.
21. Eskafi F.M., Norment B.R. Physiological action of Loxosceles reclusa (G&M) venom on insect larvae. Toxicon 1976, 14:7-13.
22. Feitosa L., Gremski W., Veiga S.S., Elias M.C., Graner E., Mangili O.C., Brentani R.R. Detection and characterization of metalloproteinases with gelatinolytic, fibronectinolytic and fibrinogenolytic activities in brown spider (Loxosceles intermedia) venom. Toxicon 1998, 36:1039-1051.
23. Fernandes-Pedrosa M.F., Junqueira-De-Azevedo Ide L., Goncalves-De-Andrade R.M., Kobashi L.S., Almeida D.D., Ho P.L., Tambourgi D.V. Transcriptome analysis of Loxosceles laeta (Araneae, Sicariidae) spider venomous gland using expressed sequence tags. BMC Genomic. 2008, 9:279.
24. Fischer M.L., Vasconcellos-Neto J. Microhabitats occupied by Loxosceles intermedia and Loxosceles laeta (Araneae: Sicariidae) in Curitiba, Parana, Brazil. J. Med. Entomol. 2005, 42:756-765.
25. Futrell J.M. Loxoscelism. Am. J. Med. Sci. 1992, 304:261-267.
26. Giron M.E., Rodriguez-Acosta A., Salazar A.M., Sanchez E.E., Galan J., Ibarra C., Guerrero B. Isolation and characterization of two new non-hemorrhagic metalloproteinases with fibrinogenolytic activity from the mapanare (Bothrops colombiensis) venom. Arch. Toxicol. 2013, 87:197-208.
27. Gomis-Rüth F.X. Structural aspects of the metzincin clan of metalloendopeptidases. Mol. Biotechnol. 2003, 24:157-202.
28. Gomis-Rüth F.X., Trillo-Muyo S., Stöcker W. Functional and structural insights into astacin metallopeptidases. Biol. Chem. 2012, 393:1027-1041.
29. Gremski L.H., Da Silveira R.B., Chaim O.M., Probst C.M., Ferrer V.P., Nowatzki J., Weinschutz H.C., Madeira H.M., Gremski W., Nader H.B., Senff-Ribeiro A., Veiga S.S. A novel expression profile of the Loxosceles intermedia spider venomous gland revealed by transcriptome analysis. Mol. Biosyst. 2010, 6:2403-2416.
30. Herrera C., Rucavado A., Warrell D.A., Gutierrez J.M. Systemic effects induced by the venom of the snake Bothrops caribbaeus in a murine model. Toxicon 2013, 63:19-31.
31. Kusma J., Chaim O.M., Wille A.C., Ferrer V.P., Sade Y.B., Donatti L., Gremski W., Mangili O.C., Veiga S.S. Nephrotoxicity caused by brown spider venom phospholipase-D (dermonecrotic toxin) depends on catalytic activity. Biochimie 2008, 90:1722-1736.
32. Luciano M.N., Da Silva P.H., Chaim O.M., Dos Santos V.L., Franco C.R., Soares M.F., Zanata S.M., Mangili O.C., Gremski W., Veiga S.S. Experimental evidence for a direct cytotoxicity of Loxosceles intermedia (brown spider) venom in renal tissue. J. Histochem. Cytochem. 2004, 52:455-467.
33. Machado L.F., Laugesen S., Botelho E.D., Ricart C.A., Fontes W., Barbaro K.C., Roepstorff P., Sousa M.V. Proteome analysis of brown spider venom: identification of loxnecrogin isoforms in Loxosceles gaucho venom. Proteomics 2005, 5:2167-2176.
34. Malaque C.M., Castro-Valencia J.E., Cardoso J.L., Francca F.O., Barbaro K.C., Fan H.W. Clinical and epidemiological features of definitive and presumed loxoscelism in Sao Paulo, Brazil. Rev. Inst. Med. Trop. Sao Paulo 2002, 44:139-143.
35. Malaque C.M., Santoro M.L., Cardoso J.L., Conde M.R., Novaes C.T., Risk J.Y., Franca F.O., De Medeiros C.R., Fan H.W. Clinical picture and laboratorial evaluation in human loxoscelism. Toxicon 2011, 58:664-671.
36. Matsubara F.H., Gremski L.H., Meissner G.O., Soares E.C.L., Gremski W., Chaim O.M., Veiga S.S. A novel ICK peptide from the Loxosceles intermedia (brown spider) venom gland: cloning, heterologous expression and immunological cross-reactivity approaches. Toxicon 2013, 71:147-178.
37. Mohrlen F., Hutter H., Zwilling R. The astacin protein family in Caenorhabditis elegans. Eur. J. Biochem. 2003, 270:4909-4920.
38. Mohrlen F., Bond J.S., Stöcker W. Other astacin homologues. Handbook of Proteolytic Enzymes 2004, Elsevier, London. second ed. A.J. Barrett, N.D. Rawlings, J.F. Woessner (Eds.).
39. Paes-Leme A.F., Kitano E.S., Furtado M.F., Valente R.H., Camargo A.C.M., Ho P.L., Fox J.W., Serrano S.M.T. Analysis of the subproteomes of proteinases and heparin-binding toxins of eight Bothrops venoms. Proteomics 2009, 9:733-745.
40. Paes-Leme A.F., Sherman N.E., Smalley D.M., Sizukusa L.O., Oliveira A.K., Menezes M.C., Fox J.W., Serrano S.M. Hemorrhagic activity of HF3, a snake venom metalloproteinase: insights from the proteomic analysis of mouse skin and blood plasma. J. Proteome Res. 2012, 11:279-291.
41. Platnick N.I. The World Spider Catalog, Version 13.5 2013, America Museum of Natural History, online at:. http://research.amnh.org/iz/spiders/catalog, 10.5531/db.iz.0001.
42. Ribeiro R.O., Chaim O.M., Da Silveira R.B., Gremski L.H., Sade Y.B., Paludo K.S., Senff-Ribeiro A., De Moura J., Chavez-Olortegui C., Gremski W., Nader H.B., Veiga S.S. Biological and structural comparison of recombinant phospholipase D toxins from Loxosceles intermedia (brown spider) venom. Toxicon 2007, 50:1162-1174.
43. Senff-Ribeiro A., Henrique Da Silva P., Chaim O.M., Gremski L.H., Paludo K.S., Bertoni Da Silveira R., Gremski W., Mangili O.C., Veiga S.S. Biotechnological applications of brown spider (Loxosceles genus) venom toxins. Biotechnol. Adv. 2008, 26:210-218.
44. Stocker W., Grams F., Baumann U., Reinemer P., Gomis-Rüth F.X., Mckay D.B., Bode W. The metzincins-topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases. Protein Sci. 1995, 4:823-840.
45. Swanson D.L., Vetter R.S. Bites of brown recluse spiders and suspected necrotic arachnidism. N. Engl. J. Med. 2005, 352:700-707.
46. Trevisan-Silva D., Gremski L.H., Chaim O.M., Da Silveira R.B., Meissner G.O., Mangili O.C., Barbaro K.C., Gremski W., Veiga S.S., Senff-Ribeiro A. Astacin-like metalloproteases are a gene family of toxins present in the venom of different species of the brown spider (genus Loxosceles). Biochimie 2010, 92:21-32.
47. Trevisan-Silva D., Gremski L.H., Chaim O.M., Senff-Ribeiro A., Veiga S.S. Chapter 247-Loxosceles astacin-like proteases (LALPs), an astacin metalloprotease family from the brown spider venom. Handbook of Proteolytic Enzymes 2013, 1081-1086. Academic Press, Oxford. third ed. N.D. Rawlings, G.S. Salvesen (Eds.).
48. Veiga S.S., Da Silveira R.B., Dreyfus J.L., Haoach J., Pereira A.M., Mangili O.C., Gremski W. Identification of high molecular weight serine-proteases in Loxosceles intermedia (brown spider) venom. Toxicon 2000, 38:825-839.
49. Veiga S.S., Zanetti V.C., Braz A., Mangili O.C., Gremski W. Extracellular matrix molecules as targets for brown spider venom toxins. Braz. J. Med. Biol. Res. 2001, 34:843-850.
50. Wille A.C.M., Chaves-Moreira D., Silva D.T., Magnoni M.G., Ferreira M.B., Gremski L.H., Gremski W., Chaim O.M., Senff-Ribeiro A., Veiga S.S. Modulation of membrane phospholipids, the cytosolic calcium influx and cell proliferation following treatment of B16-F10 cells with recombinant phospholipase-D from Loxosceles intermedia (brown spider) venom. Toxicon 2013, 67:17-30.
51. Young A.R., Pincus S.J. Comparison of enzymatic activity from three species of necrotising arachnids in Australia: Loxosceles rufescens, Badumna insignis and Lampona cylindrata. Toxicon 2001, 39:391-400.
52. Zanetti V.C., Da Silveira R.B., Dreyfuss J.L., Haoach J., Mangili O.C., Veiga S.S., Gremski W. Morphological and biochemical evidence of blood vessel damage and fibrinogenolysis triggered by brown spider venom. Blood Coagul. Fibrinolysis 2002, 13:135-148.