Local inflammatory events induced by Bothrops atrox snake venom and the release of distinct classes of inflammatory mediators

Toxicon

Volumn 60, Issue 1, 2012, Pages 12-20

  Moreira, Vanessa ^a   Dos Santos, Maria Cristina ^b   Nascimento, Neide Galvão ^a   da Silva, Henrique Borges ^c   Fernandes, Cristina Maria ^a   D'Império Lima, Maria Regina ^c   Teixeira, Catarina ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b FEDERAL UNIVERSITY OF AMAZONAS   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Bothrops atrox; Cyclooxygenases; Cytokines; Eicosanoids; Inflammation; Leukocytes

Indexed keywords

CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PROSTAGLANDIN D2; PROSTAGLANDIN E2; SNAKE VENOM; THROMBOXANE A2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL PERMEABILITY; BOTHROPS; BOTHROPS ATROX; CELL INFILTRATION; CELL TRANSPORT; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENVENOMATION; INFLAMMATION; MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION;

ANIMALS; BLOTTING, WESTERN; BOTHROPS; CROTALID VENOMS; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOKINES; INFLAMMATION; INFLAMMATION MEDIATORS; LEUKOCYTES; MALE; MICE;

BOTHROPS ATROX; MUS; SERPENTES;

EID: 84859411203     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2012.03.004     Document Type: Article

References (73)

1. Acosta de Pérez O., Teibler P., Koscinczuk P., Sánchez Negrette M., Trulls H., Maruñak S. Edema and myonecrosis induced by Bothrops jararaca venom of Argentina in mice. Acta Physiol. Pharmacol. Ther. Latinoam. 1996, 46:233-238.
2. Aiello R.J., Bourassa P.A., Lindsey S., Weng W., Freeman A., Showell H.J. Leukotriene B4 receptor antagonism reduces monocytic foam cells in mice. Arterioscler. Thromb. Vasc. Biol. 2002, 22:443-449.
3. Arend W.P., Gabay C. Cytokines in the rheumatic diseases. Rheum. Dis. Clin. North Am. 2004, 30:41-67.
4. Avila-Agüero, M.L., París, M.M., Hu, S., Peterson, P.K., Gutiérrez, J.M., Lomonte, B., Faingezicht, I; Snakebite Study Group, 2001. Systemic cytokine response in children bitten by snakes in Costa Rica. Pediatr. Emerg. Care 17, 425-429.
5. Barros S.F., Friedlanskaia I., Petricevich V.L., Kipnis T.L. Local inflammation, lethality and cytokine release in mice injected with Bothrops atrox venom. Mediators Inflamm. 1998, 7:339-346.
6. Bevilacqua M.P., Nelson R.M. Selectins. J. Clin. Invest. 1993, 91:379-387.
7. Borges C.C., Sadahiro M., Dos-Santos M.C. Aspectos epidemiológicos e clínicos dos acidentes ocorridos nos municípios do Estado do Amazonas. Rev. Soc. Bras. Med. Trop. 1999, 32:637-646.
8. Calvete J.J., Sanz L., Pérez A., Borges A., Vargas A.M., Lomonte B., ângulo Y., Gutiérrez J.M., Chalkidis H.M., Mourão R.H., Furtado M.F., Moura-Da-Silva A.M. Snake population venomics and antivenomics of Bothrops atrox: paedomorphism along its transamazonian dispersal and implications of geographic venom variability on snakebite management. J. Proteomics 2011, 74:510-527.
9. Chaves F., Barbosa M., Gutierrez J.M. Pharmacological study of edema induced by venom of the snake Bothrops asper (terciopelo) in mice. Toxicon 1995, 33:31-39.
10. De Waal Malefyt R., Abrams J., Bennett B., Figdor C.G., de Vries J.E. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 1991, 174:1209-1220.
11. Di Rosa M., Ialenti A., Ianaro A., Sautebin L. Interaction between nitric oxide and cyclooxygenase pathways. Prostaglandins Leukot. Essent. Fatty Acids 1996, 54:229-238.
12. Durrant D.M., Metzger D.W. IL-12 can alleviate Th17-mediated allergic lung inflammation through induction of pulmonary IL-10 expression. Mucosal. Immunol. 2010, 3:301-311.
13. Escocard R.C., Kanashiro M.M., Petretski J.H., Azevedo-Silva J., Queiroz-de-Carvalho E.C., Dias-da-Silva W., Kipnis T.L. Neutrophils regulate the expression of cytokines, chemokines and nitric oxide synthase/nitric oxide in mice injected with Bothrops atrox venom. Immunobiology 2006, 211:37-43.
14. Farsky S.H., Walber J., Costa-Cruz M., Cury Y., Teixeira C.F.P. Leukocyte response induced by Bothrops jararaca venom: in vivo and in vitro studies. Toxicon 1997, 35:185-193.
15. Flores C.A., Zappellini A., Prado-Franceschi J. Lypoxygenase-derived mediators may be involved in in vivo neutrophil migration induced by Bothrops erytromelas and Bothrops alternatus venom. Toxicon 1993, 31:1551-1559.
16. Ford-Hutchinson A.W. Leukotriene B4 in inflammation. Crit. Rev. Immunol. 1990, 10:1-12.
17. Furtado M.F., Colletto G.M.D.D., Silva W.D. Controle de qualidade dos venenos animais e dos correspondentes antivenenos: I. Padronização dos métodos de ensaio das atividades bioquímicas e farmacológicas dos venenos de algumas espécies do gênero Bothrops e Crotalus. Mem. Inst. Butantan 1991, 53:149-159.
18. Galvão N.N., Sampaio M.C., Amaral R.O., Teixeira C. Contribution of mast cells to the oedema induced by Bothrops moojeni snake venom and a pharmacological assessment of the inflammatory mediators involved. Toxicon 2010, 55:343-352.
19. Garcia C.A., Wang H., Benakanakere M.R., Barrett E., Kinane D.F., Martin M. C-jun controls the ability of IL-12 to induce IL-10 production from human memory CD4+ T cells. J. Immunol. 2009, 183:4475-4482.
20. Gerosa F., Paganin C., Perilt D., Paiola F., Seupoli M.T., Asteanezaga M., Frank I., Trinchieri G. Inteleukin-12 prime human CD4 e CD8 T cell clones for high production of both Interferon-gamma and IL-10. J. Exp. Med. 1996, 183:2559-2569.
21. Hart P.H. Regulation of the inflammatory response in asthma by mast cell products. Immunol. Cell Biol. 2001, 79:149-153.
22. Henderson R.B., Hobbs J.A., Mathies M., Hogg N. Rapid recruitment of inflammatory monocytes is independent of neutrophil migration. Blood 2003, 102:328-335.
23. 2 via prostanoid DP receptor on TNF-alpha-induced production of MCP-1 and IL-8 in human monocytic THP-1 cells. Eur. J. Pharmacol. 2007, 560:81-88.
24. Hubbard A.K., Rothlein R. Intercellular adhesion molecule-1 (ICAM-1) expression and cell signaling cascades. Free Radic. Biol. Med. 2000, 28:1379-1386.
25. Ishizuka T., Suzuki K., Kawakami M., Hidaka T., Matsuki Y., Nakamura H. Thromboxane A2 receptor blockade suppresses intercellular adhesion molecule-1 expression by stimulated vascular endothelial cells. Eur. J. Pharmacol. 1996, 312:367-377.
26. James M.J., Penglis P.S., Caughey G.E., Demasi M., Clenland L.G. Eicosanoids production by human monocytes: does COX-2 contribute to a self-limiying inflammatory response?. Inflamm. Res. 2001, 50:249-253.
27. Jiang Y., Beller D.I., Frendl G., Graves D.T. Monocyte chemoattractant protein-1 regulates adhesion molecule expression and cytokine production in human monocytes. J. Immunol. 1992, 148:2423-2428.
28. Kanaoka Y., Urade Y. Hematopoietic prostaglandin D synthase. Prostaglandins Leukot. Essent. Fatty Acids 2003, 69:163-167.
29. Kanashiro M.M., Escocard R.C.M., Petretski J.H., Prates M.V., Alves E.W., Machado O.L., Dias-da-Silva W.D., Kipnis T.L. Biochemical and biological properties of phospholipases A(2) from Bothrops atrox snake venom. Biochem. Pharmacol. 2002, 64:1179-1186.
30. Kaplanski G., Marin V., Montero-Julian F., Mantovani A., Farnarier C. IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends Immunol. 2003, 24:25-29.
31. Kitaura J., Kinoshita T., Matsumoto M., Chung S., Kawakami Y., Leitges M., Wu D., Lowell C.A., Kawakami T. IgE- and IgE+Ag-mediated mast cell migration in an autocrine/paracrine fashion. Blood 2005, 105:3222-3229.
32. Lomonte B., Tarkowski A., Hanson L.A. Host response to Bothrops asper snake venom. Analysis of edema formation, inflammatory cells, and cytokine release in a mouse model. Inflammation 1993, 17:93-105.
33. Luster A.D. Chemokines - chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 1998, 338:436-445.
34. 2 in lipopolysaccharide-stimulated rat peritoneal macrophages. Biochem. Biophys. Res. Commun. 1997, 230:110-114.
35. Mehrotra P.T., Donnelly R.P., Wong S., Kanegane H., Geremew A., Mostowski H.S., Furuke K., Siegel J.P., Bloom E.T. Production of IL-10 by human natural killer cells stimulated with IL-2 and/or IL-12. J. Immunol. 1998, 160:2637-2644.
36. Miyata R., Iwabuchi K., Watanabe S., Sato N., Nagaoka I. Short exposure of intestinal epithelial cells to TNF-alpha and histamine induces Mac-1-mediated neutrophil adhesion independent of protein synthesis. J. Leukoc. Biol. 1999, 66:437-446.
37. 2, and expression of cyclooxygenases. Toxicon 2007, 49:615-624.
38. Moreira V., Gutiérrez J.M., Amaral R.B., Zamunér S.R., Teixeira C.F. Effects of Bothrops asper snake venom on the expression of cyclooxygenases and production of prostaglandins by peritoneal leukocytes in vivo, and by isolated neutrophils and macrophages in vitro. Prostaglandins Leukot. Essent. Fatty Acids 2009, 80:107-114.
39. 2, cyclooxygenases, and terminal prostanoid synthases in different phases of prostanoid biosynthesis in rat peritoneal macrophages. J. Immunol. 1998, 160:2974-2982.
40. Niiro H., Otsuka T., Izuhara K., Yamaoka K., Ohshima K., Tanabe T., et al. Regulation by interleukin-10 and interleukin-4 of cyclooxygenase-2 expression in human neutrophils. Blood 1997, 89:1621-1628.
41. Núñez V., Arce V., Gutiérrez J.M., Lomonte B. Structural and functional characterization of myotoxin I, a Lys49 phospholipase A2 homologue from the venom of the snake Bothrops atrox. Toxicon 2004, 44:91-101.
42. Núñez V., Cid P., Sanz L., De La Torre P., Angulo Y., Lomonte B., Gutiérrez J.M., Calvete J.J. Snake venomics and antivenomics of Bothrops atrox venoms from Colombia and the Amazon regions of Brazil, Perú and Ecuador suggest the occurrence of geographic variation of venom phenotype by a trend towards paedomorphism. J. Proteomics 2009, 73:57-78.
43. Olivo R.A., Teixeira C.F.P., Wallace J.L., Gutierrez J.M., Zamuner S.R. Role of cyclooxygenases in oedema-forming activity of bothropic venoms. Toxicon 2007, 49:670-677.
44. Otero R., Núñes V., Barona J., Fonnegra R., Jiménez S.L., Osorio R.G., Saldarriaga M., Díaz A. Snakebites and ethnobotany in the northwest region of Colombia. Part III: neutralization of the haemorrhagic effect of Bothrops atrox venom. J. Ethnopharmacol. 2000, 73:233-241.
45. 2 modulates the functional responsiveness of human monocytes to chemokines. Eur. J. Immunol. 2004, 34:3682-3689.
46. Petretski J.H., Kanashiro M.M., Rodrigues F.R., Alves E.W., Machado O.L.T., Kipnis T.L. Edema induction by the disintegrin-like/cysteine-rich domains from a Bothrops atrox hemorrhagin. Biochem. Biophys. Res. Commun. 2000, 276:29-34.
47. 2 blocks inflammation, hyperalgesia, and interleukin 6 production in vivo. J. Exp. Med. 1996, 184:883-891.
48. Pradelles P., Grassi J., Maclouf J. Enzyme immunoassays of eicosanoids using acetylcholine esterase as label: an alternative to radioimmunoassay. Anal. Chem. 1985, 57:1170-1173.
49. Rodrigues F.G., Petretski J.H., Kanashiro M.M., Lemos L., da Silva W.D., Kipnis T.L. The complement system is involved in acute inflammation but not in the hemorrhage produced by a Bothrops atrox snake venom low molecular mass proteinase. Mol. Immunol. 2004, 40:1149-1156.
50. Sabat R. IL-10 family of cytokines. Cytokine Growth Factor Rev. 2010, 21:315-324.
51. Sedgwick J.D., Riminton D.S., Cyster J.G., Körner H. Tumor necrosis factor: a master-regulator of leukocyte movement. Immunol. Today 2000, 21:110-113.
52. Sherwood E.R., Toliver-Kinsky T. Mechanisms of the inflammatory response. Best. Pract. Res. Clin. Anaesthesiol. 2004, 18:385-405.
53. Simon L.S. Nonsteroidal antiinflammatory drugs and their effects. J. Clin. Rheumatol. 1996, 2:135-140.
54. Sirois M.G., Jancar S., Braquet P., Plante G.E., Sirois P. PAF increases vascular permeability in selected tissues: effect of BN-52021 and L-655,240. Prostaglandins 1988, 36:631-644.
55. Smith W.L., DeWitt D.L., Garavito R.M. Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 2000, 69:145-182.
56. Smith J.A. Neutrophils, host defense, and inflammation: a double-edged sword. J. Leukoc. Biol. 1994, 56:672-686.
57. Speiran K., Bailey D.P., Fernando J., Macey M., Barnstein B., Kolawole M., Curley D., Watowich S.S., Murray P.J., Oskeritzian C., Ryan J.J. Endogenous suppression of mast cell development and survival by IL-4 and IL-10. J. Leukoc. Biol. 2009, 85:826-836.
58. Suwa T., Hogg J.C., English D., Van Eeden S.F. Interleukin-6 induces demargination of intravascular neutrophils and shortens their transit in marrow. Am. J. Physiol. Heart Circ. Physiol. 2000, 279:H2954-H2960.
59. Tajima T., Murata T., Aritake K., Urade Y., Hirai H., Nakamura M., Ozaki H., Hori M. Lipopolysaccharide induces macrophage migration via prostaglandin D(2) and prostaglandin E(2). J. Pharmacol. Exp. Ther. 2008, 326:493-501.
60. Takayama K., Mitchell D.H., Din Z.Z., Mukerjee P., Li C., Coleman D.L. Monomeric Re lipopolysaccharide from Escherichia coli is more active than the aggregated form in the Limulus amebocyte lysate assay and in inducing Egr-1 mRNA in murine peritoneal macrophages. J. Biol. Chem. 1994, 269:2241-2244.
61. Teixeira C., Cury Y., Moreira V., Picolo G., Chaves F. Inflammation induced by Bothrops asper venom. Toxicon 2009, 54:988-997.
62. Trebien H.A., Calixto J.B. Pharmacological evaluation of rat paw oedema induced by Bothrops jararaca venom. Agents Actions 1989, 26:292-300.
63. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptative immunity. Nat. Rev. Immunol. 2003, 3:133-146.
64. Tull S.P., Yates C.M., Maskrey B.H., O'Donnell V.B., Madden J., Grimble R.F., Calder P.C., Nash G.B., Rainger G.E.D. Omega-3 fatty acids and inflammation: novel interactions reveal a new step in neutrophil recruitment. PLoS Biol. 2009, 7:1-11.
65. Ulich T.R., Del Castillo J., Busser K., Guo K.Z., Yin S.M. Acute in vivo effects of IL-3 alone and in combination with IL-6 on the blood cells of the circulation and bone marrow. Am. J. Pathol. 1989, 135:663-670.
66. Vieira P., O'Garra A. Regula'ten' the gut. Nat. Immunol. 2007, 8:905-907.
67. Waldez F., Vogt R.C. Aspectos ecológicos e epidemiológicos de acidentes ofídicos em comunidades ribeirinhas do Baixo Rio Purus, Amazonas, Brasil. Acta Amaz. 2009, 39:681-692.
68. Warner T.D., Mitchell J.A. Cyclooxygenases: new forms, new inhibitors, and lessons from the clinic. FASEB J. 2004, 18:790-804.
69. Wendy T., Moriguchi W.M., Morinobu A., O'Shea J.J. The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev. 2003, 14:361-368.
70. Weringer E.J., Perry B.D., Sawyer P.S., Gilman S.C., Showell H.J. Antagonizing leukotriene B4 receptors delays cardiac allograft rejection in mice. Transplantation 1999, 67:808-815.
71. Wiles M.E., Welbourn R., Goldman G., Hechtman H.B., Shepro D. Thromboxane-induced neutrophil adhesion to pulmonary microvascular and aortic endothelium is regulated by CD18. Inflammation 1991, 15:181-199.
72. Zamuner S.R., Teixeira C.F. Cell adhesion molecules involved in the leukocyte recruitment induced by venom of the snake Bothrops jararaca. Mediators Inflamm. 2002, 11:351-357.
73. Zamuner S.R., Zuliani J.P., Fernandes C.M., Gutiérrez J.M., Teixeira C.F.P. Inflammation induced by Bothrops asper venom: release of proinflammatory cytokines and eicosanoids, and role of adhesion molecules in leukocyte infiltration. Toxicon 2005, 46:806-813.