Immunomodulatory effects of crotoxin isolated from Crotalus durissus terrificus venom in mice immunised with human serum albumin

Toxicon

Volumn 57, Issue 4, 2011, Pages 600-607

  Favoretto, B C ^a   Ricardi, R ^a   Silva, S R ^a   Jacysyn, J F ^b   Fernandes, I ^a   Takehara, H A ^a   Faquim Mauro, E L ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Antibody production; Crotoxin; Immunomodulation; Snake venom; T cell proliferative response

Indexed keywords

CROTOXIN; HUMAN SERUM ALBUMIN; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; CROTALUS TERRIFICUS; HUMORAL IMMUNITY; IMMUNOMODULATION; IMMUNOREGULATION; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; POISONOUS SNAKE; PRIORITY JOURNAL; T LYMPHOCYTE; TOXIN ANALYSIS;

ADAPTIVE IMMUNITY; ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELL SURVIVAL; CROTALID VENOMS; CROTOXIN; HUMANS; LYMPH NODES; MALE; MICE; MICE, INBRED BALB C; NECROSIS; SERUM ALBUMIN; T-LYMPHOCYTES;

CROTALUS DURISSUS TERRIFICUS; MUS;

EID: 79952361541     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2010.12.023     Document Type: Article

References (78)

1. Abbas A.K., Lichtman A.H. Imunologia Celular e Molecular 2005, Elsevier, Rio de Janeiro. fifth ed.
2. Adorini L., Trembleau S. Immune deviation towards Th2 inhibits Th1-mediated autoimmune diabetes. Biochem. Soc. Trans. 1997, 25:625-629.
3. Amarante-Mendes G.P., Green D.R. The regulation of apoptotic cell death. Braz. J. Med. Biol. Res. 1999, 32:1053-1061.
4. Azevedo-Marques M.M., Cupo P., Coimbra T.M., Hering S.E., Rossi M.A., Laure C.J. Myonecrosis, myoglobinuria and acute renal failure induced by South American rattlesnake (Crotalus durissus terrificus) envenomation in Brazil. Toxicon 1985, 23:631-636.
5. Bon C., Changeux J.P., Jeng T.W., Fraenkel-Conrat H. Postsynaptic effects of crotoxin and its isolated subunits. Eur. J. Biochem. 1979, 99:471-481.
6. Bolano R., Cerdas L. The production and control of anti-venoms sera. Deal. Biol. Stand. 1978, 41:109-116.
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
8. Campling B.G., Pym J., Galbraith P.R., Cole S.P. Use of the MTT assay for rapid determination of chemosensitivity of human leukemic blast cells. Leuk. Res. 1988, 12:823-831.
9. Cardoso D.F., Mota I. Effect of Crotalus venom on the humoural and cellular immune response. Toxicon 1997, 35:607-612.
10. Catron D.M., Itano A.A., Pape K.A., Mueller D.L., Jenkins M.K. Visualizing the first 50h of the primary immune response to a soluble antigen. Immunity 2004, 21:341-347.
11. Chaplin D.D. 1. Overview of the immune response. J. Allergy Clin. Immunol. 2003, 111:S442-S459.
12. Chiu C.C., Lin K.L., Chien C.M., Chang L.S., Lin S.R. Effects of cardiotoxin III on NF-kappa B function, proliferation and apoptosis in human breast MCF-7 cancer cells. Oncol. Res. 2009, 17:311-321.
13. Cruz A.H., Mendonça R.Z., Petricevich V.L. Crotalus durissus terrificus venom interferes with morphological, functional, and biochemical changes in murine macrophage. Mediators Inflamm. 2005, 6:349-359.
14. Doetze A., Satoguina J., Burchard G., Rau T., Löliger C., Fleischer B., Hoerauf A. Antigen-specific cellular hyporesponsiveness in a chronic human helminth infections is mediated by T (h)3/T (r) 1-type cytokines IL-10 and transforming growth factor-beta but not by a T (h) 1 to T(h)2 shift. Int. Immunol. 2000, 12:623-630.
15. Dos Santos M.C., Diniz C.R., Pacheco M.A., Dias da Silva W. Phospholipase A2 injection in mice induces immunity against the lethal effects of Crotalus durissus terrificus venom. Toxicon 1988, 26:207-213.
16. Dos-Santos M.C., D'Império Lima M.R., Dias da Silva W. Influence of Crotalus venom on the response to sheep red blood cells. Braz. J. Med. Biol. Res. 1986, 19:636a.
17. Faure G., Bon C. Several isoforms of crotoxin are present in individual venoms from the South American rattlesnake Crotalus durissus terrificus. Toxicon 1987, 25:229-234.
18. Faure G., Bon C. Crotoxin, a phospholipase A2 neurotoxin from the South American rattlesnake Crotalus durissus terrificus: purification of several isoforms and comparison of their molecular structure and of their biological activities. Biochemistry 1988, 27:730-738.
19. Faure G., Choumet V., Bouchier C., Camoin L., Guillaume J.L., Monegier B., Vuilhorgne M., Bon C. The origin of the diversity of crotoxin isoforms in the venom of Crotalus durissus terrificus. Eur. J. Biochem. 1994, 223:161-164.
20. Faure G., Choumet V., Bouchier C., Camoin L., Guillaume J.L., Monegier B., Vuilhorgne M., Bon C. Immunization with Ascaris suum extract impairs T cell functions in mice. Cell. Immunol. 1994, 162:202-210.
21. Ferreira A.P., Faquim E.S., Abrahamsohn I.A., Macedo M.S. Immunization with Ascaris suum extract impairs T cells function in mice. Cell Immunol 1995, 162(2):202-210.
22. 2 synthesis. Toxicon 2003, 42:433-437.
23. Gazzinelli R.T., Oswald I.P., James S.L., Sher A. IL-10 inhibits parasite killing and nitrogen oxide production by IFN-gamma-activated macrophages. J. Immunol. 1992, 148:1792-1796.
24. Geijtenbeek T.B., Gringhuis S.I. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 2009, 9:465-479.
25. Geissmann F., Manz M.G., Jung S., Sieweke M.H., Merad M., Ley K. Development of monocytes, macrophages, and dendritic cells. Science 2010, 327:656-661.
26. Goodyear C.S., Silverman G.J. Death by a B cell superantigen: in vivo VH-targeted apoptotic supraclonal B cell deletion by a Staphylococcal Toxin. J. Exp. Med. 2003, 197:1125-1139.
27. Gunzer M., Schäfer A., Borgmann S., Grabbe S., Zänker K.S., Bröcker E.B., Kämpgen E., Friedl P. Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity 2000, 13:323-332.
28. Grütz G. New insights into the molecular mechanism of interleukin-10-mediated immunosuppression. J. Leukoc. Biol. 2005, 77:3-15.
29. Han S., Lee K., Yeo J., Kweon H., Woo S., Lee M., Baek H., Kim S., Park K. Effect of honey bee venom on microglial cells nitric oxide and tumor necrosis factor-α production stimulated by LPS. J. Ethno-Pharmacol 2007, 111:176-181.
30. 2 enhances the production of endogenous IL-10, which down-regulates dendritic cell functions. J. Immunol. 2002, 168:2255-2263.
31. Hawgood B.J., Smith J.W. The mode of action at the mouse neuromuscular junction of the phospholipase A-crotapotin complex isolated from venom of the South American rattlesnake. Br. J. Pharmacol. 1977, 61:597-606.
32. Hunter C.A., Ellis-Neyes L.A., Slifer T., Kanaly S., Grünig G., Fort M., Rennick D., Araujo F.G. IL-10 is required to prevent immune hyperactivity during infection with Trypanosoma cruzi. J. Immunol. 1997, 158:3311-3316.
33. Itano A.A., Jenkins M.K. Antigen presentation to naive CD4 T cells in the lymph node. Nat. Immunol. 2003, 4:733-739.
34. Iwasaki A., Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science 2010, 327:291-295.
35. Janeway C.A., Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20:197-216.
36. Jendro M.C., Deutsch T., Körber B., Köhler L., Kuipers J.G., Krausse-Opatz B., Westermann J., Raum E., Zeidler H. Infection of human monocyte-derived macrophages with Chlamydia trachomatis induces apoptosis of T cells: a potential mechanism for persistent infection. Infect. Immun. 2000, 68:6704-6711.
37. + dendritic cells: the levels of IL-12 are determined during the final dendritic cell maturation and are resistant to further modulation. J. Immunol. 1998, 161:2804-2809.
38. Kang S.S., Pak S.C., Choi S.H. The effect of whole bee venom on Arthritis. Amer. J. Chin. Med. 2002, 30:73-80.
39. Kim S.J., Park J.H., Kim K.H., Lee W.R., Chang Y.C., Park K.K., Lee K.G., Han S.M., Yeo J.H., Pak S.C. Bee venom inhibits hepatic fibrosis through suppression of pro-fibrogenic cytokine expression. Am. J. Clin. Med. 2010, 38:921-935.
40. Lee J.D., Kim S.Y., Kim T.W., Lee S.H., Yang H.I., Lee D.I., Lee Y.H. Anti-inflammatory effect of bee venom on type II Collagen-induced Arthritis. Amer. J. Chin. Med. 2004, 32:361-367.
41. Liebig T.M., Fiedler A., Zoghi S., Shimabukuro-Vornhagen A., von Bergwelt-Baildon M.S. Generation of human CD40-activated B cells. J. Vis. Exp. 2009, 16:3791-3799.
42. Lim S.K. Freund adjuvant induces TLR2 but not TLR4 expression in the liver of mice. Int. Immunopharmacol. 2003, 3:115-118.
43. Liu Y.J., Zhang J., Lane P.J., Chan E.Y., MacLennan I.C. Sites of specific B-cell activation in primary and secondary responses to T cell dependent and T cell-independent antigens. Eur. J. Immunol. 1991, 21:2951-2962.
44. Liu Y.L., Lin H.M., Zou R., Wu J.C., Han R., Raymond L.N., Reid P.F., Qin Z.H. Suppression of complete Freund's adjuvant-induced arthritis by cobratoxin. Acta Pharmacol. Sin 2009, 30:219-227.
45. Medzhitov R., Janeway C. Innate immune recognition: mechanisms and pathways. Immunol. Rev. 2000, 173:89-97.
46. Moll H. Dendritic cells and host resistance to infection. Cell Microbiol. 2003, 5:493-500.
47. Mosmann T.R., Coffman R.L. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 1989, 7:145-173.
48. Mosmann T.R., Moore K.W. The role of IL-10 in crossregulation of TH1 and TH2 responses. Immunol. Today 1991, 12:49-53.
49. Nunes F.P., Zychar B.C., Della-Casa M.S., Sampaio S.C., Gonçalves L.R., Cirillo M.C. Crotoxin is responsible for the long-lasting anti-inflammatory effect of Crotalus durissus terrificus snake venom: involvement of formyl peptide receptors. Toxicon 2010, 55:1100-1106.
50. Pearlman E., Kazura J.W., Hazlett F.E., Boom W.H. Modulation of murine cytokine responses to mycobacterial antigens by helminth-induced T helper 2 cell responses. J. Immunol. 1993, 151:4857-4864.
51. Petrovsky N. Novel human polysaccharide adjuvants with dual Th1 and Th2 potentiating activity. Vaccine 2006, 24:26-29.
52. Ponce-Soto L.A., Toyama M.H., Hyslop S., Novello J.C., Marangoni S. Isolation and preliminary enzymatic characterization of a novel PLA2 from Crotalus durissus collilineatus venom. J. Protein Chem. 2002, 21:131-136.
53. Rangel-Santos A., Lima C., Lopes-Ferreira M., Cardoso D.F. Immunosuppresive role of principal toxin (crotoxin) of Crotalus durissus terrificus venom. Toxicon 2004, 44:609-616.
54. Riccardi C., Nicoletti I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat. Protoc. 2006, 1:1458-1461.
55. Rimaniol A.C., Gras G., Verdier F., Capel F., Grigoriev V.B., Porcheray F., Sauzeat E., Fournier J.G., Clayette P., Siegrist C.A., Dormont D. Aluminum hydroxide adjuvant induces macrophage differentiation towards a specialized antigen-presenting cell type. Vaccine 2004, 13:3127-3135.
56. Rolim-Rosa R., Vieira E.G.J., Silles-Villarroel M., Siracusa Y.Q., Tizuka H. Análise comparativa entre os diferentes esquemas de hiperimunização empregados na produção de soros antiofídicos do Instituto Butantan (1957-1979). Mem. Inst. Butantan 1980-1981, 44-45:259-265.
57. Rosen F.S., Steiner L.A., Unanue E.R. Dictionary of Immunology 1989, The Macmillan Press Ltd, London.
58. Sampaio S.C., Brigatte P., Sousa-e-Silvados-Santos M.C., dos-Santos E.C., Rangel-Santos A.C., Curi R., Cury Y. Contribution of crotoxin for the inhibitory effect of Crotalus durissus terrificus snake venom on macrophage function. Toxicon 2003, 41:899-907.
59. Sampaio S.C., Rangel-Santos A.C., Peres C.M., Curi R., Cury Y. Inhibitory effect of phospholipase A2 isolated from Crotalus durissus terrificus venom on macrophage function. Toxicon 2005, 45:671-676.
60. Sampaio S.C., Santos M.F., Costa E.P., Rangel-Santos A.C., Carneiro S.M., Curi R., Cury Y. Crotoxin induces actin reorganization and inhibits tyrosine phosphorylation and activity of small GTPases in rat macrophages. Toxicon 2006, 47:909-919.
61. Schaeffer R.C., Randall H., Resk J., Carlson R.W. Enzyme-linked immunosorbant assay (ELISA) of size-selected crotalid venom antigens by Wyeth's polyvalent antivenom. Toxicon 1988, 26:67-76.
62. Schijns V.E. Immunological concepts of vaccine adjuvant activity. Curr. Opin. Immunol. 2000, 12:456-463.
63. Schnare M., Barton G.M., Holt A.C., Takeda K., Akira S., Medzhitov R. Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2001, 2:947-950.
64. Silva M.C., Gonçalves L.R., Mariano M. The venom of South American rattlesnakes inhibits macrophage functions and is endowed with anti-inflammatory properties. Mediators Inflamm. 1996, 5:18-23.
65. Silva D.G., Cooper P.D., Petrovsky N. Inulin-derived adjuvants efficiently promote both Th1 and Th2 immune responses. Immunol. Cell Biol. 2004, 82:611-616.
66. Slotta K.H., Frankel-Conrat H. Estudos químicos sobre venenos ofídicos: 4-purificação e cristalização do veneno da cobra cascavel. Mem. Instituto Butantan 1938, 12:505-512.
67. Sokolovska A., Hem S.L., HogenEsch H. Activation of dendritic cells and induction of CD4(+) T cell differentiation by aluminum-containing adjuvants. Vaccine 2007, 25:4575-4585.
68. Son D.J., Ha S.J., Song H.S., Lim Y., Yun Y.P., Lee J.W., Moon D.C., Park Y.H., Park B.S., Song M.J., Hong J.T. Melittin inhibits vascular smooth muscle cell proliferation through induction of apoptosis via suppression of nuclear factor-KappaB and Akt activation and enhancement of apoptotic protein expression. J. Pharmacol. Exp. Ther. 2006, 317:627-634.
69. Stephano M.A., Guidolin R., Higashi H.G., Tambourgi D.V., Sant'Anna O.A. The improvement of the therapeutic anti-Lachesis muta serum production in horses. Toxicon 2005, 45:467-473.
70. Szomolanyi-Tsuda E., Welsh R.M. T cell-independent antibody-mediated clearance of polyoma virus in T cell deficient mice. J. Exp. Med. 1996, 183:403-411.
71. Ulanova M., Tarkowski A., Hahn-Zoric M., Hanson L.A. The Common vaccine adjuvant aluminum hydroxide up-regulates accessory properties of human monocytes via an interleukin-4-dependent mechanism. Infect. Immun. 2001, 69:1151-1159.
72. van Vliet S.J., den Dunnen J., Gringhuis S.I., Geijtenbeek T.B., van Kooyk Y. Innate signaling and regulation of Dendritic cell immunity. Curr. Opin. Immunol. 2007, 19:435-440.
73. Vital Brazil O., Excell B.J. Action of crotoxin and crotactin from the venom of Crotalus durissus terrificus (South American rattlesnake) on the frog neuromuscular junction. J. Physiol. 1971, 212:34-35.
74. Vogel T.U., Fournier J., Sherring A., Ko D., Parenteau M., Bogdanovic D., Mihowich J., Rud E.W. Presence of circulating CTL induced by infection with wild-type or attenuated SIV and their correlation with protection from pathogenic SHIV challenge. J. Med. Primatol. 1998, 27:65-72.
75. Walls R.S. Eosinophil response to alum adjuvants: involvement of T cells in non-antigen-dependent mechanisms. Proc. Soc. Exp. Biol. Med. 1977, 156:431-435.
76. + regulatory T cells from peripheral Foxp3 precursors. Blood 2007, 110:4293-4302.
77. Zambelli V.O., Sampaio S.C., Sudo-Hayashi L.S., Greco K., Britto L.R., Alves A.S., Zychar B.C., Gonçalves L.R., Spadacci-Morena D.D., Otton R., Della-Casa M.S., Curi R., Cury Y. Crotoxin alters lymphocyte distribution in rats: involvement of adhesion molecules and lipoxygenase-derived mediators. Toxicon 2008, 51:1357-1367.
78. Zychlinsky A., Prevost M.C., Sansonetti P.J. Shigella flexneriinduces apoptosis in infected macrophages. Nature 1992, 358:167-169.