Effects of two serine proteases from Bothrops pirajai snake venom on the complement system and the inflammatory response

International Immunopharmacology

Volumn 15, Issue 4, 2013, Pages 764-771

  Menaldo, Danilo L ^a   Bernardes, Carolina P ^a   Pereira, Juliana C ^a   Silveira, Denise S C ^a   Mamede, Carla C N ^b,c   Stanziola, Leonilda ^b,c   Oliveira, Fábio De ^b,c   Pereira Crott, Luciana S ^a   Faccioli, Lúcia H ^a   Sampaio, Suely V ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF UBERLÂNDIA   (Brazil)

^c Instituto Nacional de Ciência e Tecnologia em NanoBiofarmacêutica N BIOFAR Avenida Antônio Carlos S n   (Brazil)

Author keywords

Bothrops pirajai; Complement system; Inflammation; Serine proteases; Snake venoms; Thrombin like enzymes

Indexed keywords

BPIRSP27 ENZYME; BPIRSP41 ENZYME; ENZYME INHIBITOR; LECTIN; SERINE PROTEINASE; SNAKE VENOM; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BOTHROPS; COMPLEMENT SYSTEM; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; ENZYME INHIBITION; FEMALE; HEMOLYSIS; INFLAMMATION; LEUKOCYTE; MALE; MOUSE; NONHUMAN; PAIN THRESHOLD; PAW EDEMA; PRIORITY JOURNAL; RAT;

ADULT; ANIMALS; BOTHROPS; CELLS, CULTURED; COMPLEMENT ACTIVATION; CROTALID VENOMS; EDEMA; ERYTHROCYTES; EXUDATES AND TRANSUDATES; FEMALE; HEMOLYSIS; HUMANS; HYPERALGESIA; LEUKOCYTE COUNT; LEUKOCYTES; MALE; MICE; MICE, INBRED BALB C; PERITONEAL CAVITY; RABBITS; RATS; RATS, WISTAR; SERINE PROTEASES; SERUM; SHEEP; YOUNG ADULT;

EID: 84875913286     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2013.02.023     Document Type: Article

References (48)

1. C. Teixeira, Y. Cury, V. Moreira, G. Picolo, and F. Chaves Inflammation induced by Bothrops asper venom Toxicon 154 2009 988 997
2. M. Rocha e Silva A brief survey of the history of inflammation Agents Actions 8 1978 45 49
3. J.M. Gutiérrez, and A. Rucavado Snake venom metalloproteinases: their role in the pathogenesis of local tissue damage Biochimie 82 2000 841 850
4. A.M. Moura-da-Silva, D. Butera, and I. Tanjoni Importance of snake venom metalloproteinases in cell biology: effects on platelets, inflammatory and endothelial cells Curr Pharm Des 13 2007 2893 2905 (Pubitemid 351545892)
5. D.S. Lopes, C. Baldo, C.F. Oliveira, T.M. de Alcântara, J.D. Oliveira, and L.R. Gourlart Characterization of inflammatory reaction induced by neuwiedase, a P-I metalloproteinase isolated from Bothrops neuwiedi venom Toxicon 54 2009 42 49
6. 2 Toxicon 42 2003 947 962 (Pubitemid 38201494)
7. C.F. Teixeira, C.M. Fernandes, J.P. Zuliani, and S.F. Zamuner Inflammatory effects of snake venom metalloproteinases Mem Inst Oswaldo Cruz 100 2005 181 184 (Pubitemid 40685461)
8. S. Braud, C. Bon, and A. Wisner Snake venom acting on hemostasis Biochimie 82 2000 851 859
9. S.M. Serrano, and R.C. Maroun Snake venom serine proteinases: sequence homology vs. substrate specificity, a paradox to be solved Toxicon 45 2005 1115 1132 (Pubitemid 40732585)
10. H. Pirkle Thrombin-like enzymes from snake venoms Thromb Haemost 79 1998 675 683
11. H.C. Castro, R.B. Zingali, M.G. Albuquerque, M. Pujol-Luz, and C.R. Rodrigues Snake venom thrombin-like enzymes: from reptilase to now Cell Mol Life Sci 61 2004 843 856 (Pubitemid 38651003)
12. M.M. Markiewski, B. Nilsson, K.N. Ekdahl, T.E. Mollnes, and J.D. Lambris Complement and coagulation: strangers or partners in crime? Trends Immunol 28 2007 184 192 (Pubitemid 46476881)
13. U. Amara, D. Rittirsch, M. Flierl, U. Bruckner, A. Klos, and F. Gebhard Interaction between the coagulation and complement system Adv Exp Med Biol 632 2008 71 79
14. E. Wagner, and M.M. Frank Therapeutic potential of complement modulation Nat Rev Drug Discov 9 2010 43 56
15. M. Huber-Lang, J.V. Sarma, F.S. Zetoune, D. Rittirsch, T.A. Neff, and S.R. McGuire Generation of C5a in the absence of C3: a new complement activation pathway Nat Med 12 2006 682 687 (Pubitemid 43865238)
16. G. Eggertsen, J. Fohlman, and J. Sjöquist In vitro studies on complement inactivation by snake venoms Toxicon 18 1980 87 96 (Pubitemid 10100700)
17. G. Pidde-Queiroz, M.F. Furtado, C.F. Filgueiras, L.A. Pessoa, M. Spadafora-Ferreira, and C.W. van den Berg Human complement activation and anaphylatoxins generation induced by snake venom toxins from Bothrops genus Mol Immunol 47 2010 2537 2544
18. G.D. Tanaka, G.P. Queiroz, M.D. Furtado, C.W. van den Berg, and D.V. Tambourgi Micrurus snake venoms activate human complement system and generate anaphylatoxins BMC Immunol 13 2012 4 11
19. S.H. Farsky, L.R. Gonçalves, J.M. Gutiérrez, A.P. Correa, A. Rucavado, and P. Gasque Bothrops asper snake venom and its metalloproteinase BaP-1 activate the complement system. Role in leucocyte recruitment Mediators Inflamm 9 2000 213 221 (Pubitemid 32055499)
20. B.B. Shoibonov, A.V. Osipov, E.V. Kryukova, A.A. Zinchenko, V.M. Lakhtin, and V.I. Tsetlin Oxiagin from the Naja oxiana cobra venom is the first reprolysin inhibiting the classical pathway of complement Mol Immunol 42 2005 1141 1153
21. Q.Y. Sun, and J. Bao Purification, cloning and characterization of a metalloproteinase from Naja atra venom Toxicon 56 2010 1459 1469
22. C. Yamamoto, D. Tsuru, N. Oda-Ueda, M. Ohno, S. Hattori, and S.T. Kim Flavoxobin, a serine protease from Trimeresurus flavoviridis (habu snake) venom, independently cleaves Arg726-Ser727 of human C3 and acts as a novel, heterologous C3 convertase Immunology 107 2002 111 117
23. D.L. Menaldo, C.P. Bernardes, N.A. Santos-Filho, L.A. Moura, A.L. Fuly, and E.C. Arantes Biochemical characterization and comparative analysis of two distinct serine proteases from Bothrops pirajai snake venom Biochimie 94 2012 2545 2558
24. J.O. Almeida, and E.H. Fife Jr. Quantitatively standardized complement-fixation methods for critical evaluation of antigens prepared from Trypanosoma cruzi Pan Am Health Org 319 1976 86
25. L.S. Crott, Y.M. Lucisano-Valim, C.L. Silva, and J.E. Barbosa Interactions of F1 fractions from different strains of Paracoccidioides brasiliensis with human complement and with human neutrophils Mycopathologia 140 1997 19 27 (Pubitemid 28202715)
26. C.G. Van Arman, A.J. Begany, J.M. Miller, and H.H. Pless Some details of the inflammation caused by yeast and carragenin J Pharmacol Exp Ther 150 1965 328 333
27. L.O. Randall, and J.J. Selitto A method for measurement of analgesic activity on inflamed tissue Arch Int Pharmacodyn Ther 111 1957 409 419
28. W. Dias da Silva, D.V. Tambourgi, A.C.M.R. Campos, F. Magnoli, V.L. Petricevich, and T.L. Kipnis Complement activation by animal venoms J Toxicol Toxin Rev 14 1995 375 400
29. H.J. Müller-Eberhard, and K.E. Fjellström Isolation of the anticomplementary protein from cobra venom and its mode of action on C3 J Immunol 107 1971 1666 1672
30. A. Gasmi, H. Louzir, H. Karoui, M. Ayeb, and K. Dellagi Purification from Vipera lebetina (desert adder) venom of a protein that depletes human complement Nat Toxins 2 1994 44 48 (Pubitemid 24123788)
31. 2 to the inflammatory reaction induced by Bothrops jararaca crude venom in mice Toxicon 55 2010 227 234
32. A. Vilca-Quispe, L.A. Ponce-Soto, F.V. Winck, and S. Marangoni Isolation and characterization of a new serine protease with thrombin-like activity (TLBm) from the venom of the snake Bothrops marajoensis Toxicon 55 2010 745 753
33. H.A. Trebien, and J.B. Calixto Pharmacological evaluation of rat paw ooedema induced by Bothrops jararaca venom Agents Actions 26 1989 292 300 (Pubitemid 19078123)
34. J. Perales, C.Z. Amorim, S.L.G. Rocha, G.B. Domont, and H. Moussatche Neutralization of the oedematogenic activity of Bothrops jararaca venom on the mouse paw by an antibothropic fraction isolated from opossum (Didelphis marsupialis) serum Agents Actions 37 1992 250 259 (Pubitemid 23062754)
35. B. Lomonte, A. Tarkowski, and L.A. Hanson Host response to Bothrops asper snake venom. Analysis of edema formation, inflammatory cells, and cytokine release in a mouse model Inflammation 17 1993 93 105 (Pubitemid 23105184)
36. F. Chaves, M. Barbosa, and J.M. Gutiérrez Pharmacological study of oedema induced by venom of the snake Bothrops asper (Terciopelo) in mice Toxicon 33 1995 31 39
37. A. Lôbo de Araújo, A.O. Souza, M.A. Cruz-Hofling, C.A. Flores, and C. Bon Bothrops lanceolatus (fer de lance) venom induces oedema formation and increases vascular permeability in the mouse hind paw Toxicon 38 2000 209 221 (Pubitemid 29512193)
38. A.M. Barbosa, R.O. do Amaral, C.F. Teixeira, S. Hyslop, and J.C. Cogo Pharmacological characterization of mouse hind paw oedema induced by Bothrops insularis (jararaca ilhoa) snake venom Toxicon 42 2003 515 523 (Pubitemid 38366202)
39. C.F.P. Teixeira, Y. Cury, S. Oga, and S. Jancar Hyperalgesia induced by Bothrops jararaca venom in rats: role of eicosanoids and platelet activating factor (PAF) Toxicon 32 1994 419 426 (Pubitemid 24160407)
40. M. Chacur, G. Picolo, J.M. Gutiérrez, C.F.P. Teixeira, and Y. Cury Pharmacological modulation of hyperalgesia induced by Bothrops asper (terciopelo) snake venom Toxicon 39 2001 1173 1181 (Pubitemid 32295884)
41. H. Ulbrich, E.E. Eriksson, and L. Lindbom Leukocyte and endothelial cell adhesion molecules as targets for therapeutic interventions in inflammatory disease Trends Pharmacol Sci 24 2003 640 647 (Pubitemid 37494786)
42. J.M. Gutiérrez, F. Chaves, and L. Cerdas Inflammatory infiltrate in skeletal muscle injected with Bothrops asper venom Rev Biol Trop 34 1986 209 214
43. C.A. Flores, A. Zappellini, and J. Prado-Franceschi Lipoxygenase-derived mediators may be involved in in vivo neutrophil migration induced by Bothrops erytromelas and Bothrops alternatus venoms Toxicon 31 1993 1551 1559 (Pubitemid 24033182)
44. V. Moreira, M.C. Dos-Santos, N.G. Nascimento, H.B. da Silva, C.M. Fernandes, and M.R. D'Império Lima Local inflammatory events induced by Bothrops atrox snake venom and the release of distinct classes of inflammatory mediators Toxicon 60 2012 12 20
45. C.M. Fernandes, S.R. Zamuner, J.P. Zuliani, A. Rucavado, J.M. Gutiérrez, and C.F. Teixeira Inflammatory effects of BaP1, a metalloproteinase isolated from Bothrops asper snake venom: leukocyte recruitment and release of cytokines Toxicon 47 2006 549 559
46. E. Ting, A.T. Guerrero, T.M. Cunha, W.A. Verri Jr., S.M. Taylor, and T.M. Woodruff Role of complement C5a in mechanical inflammatory hypernociception: potential use of C5a receptor antagonists to control inflammatory pain Br J Pharmacol 153 2008 1043 1053 (Pubitemid 351337543)
47. 2 homologue piratoxin-I in the rat and rabbit. Effect of polyanions and p-bromophenacyl bromide Biochem Pharmacol 59 2000 1289 1294 (Pubitemid 30157891)
48. P. Saravia-Otten, T. Frisan, M. Thelestam, and J.M. Gutiérrez Membrane independent activation of fibroblast proMMP-2 by snake venom: novel roles for venom proteinases Toxicon 44 2004 749 764 (Pubitemid 39410350)