Seminars in Nephrology
Volume 28, Issue 4 , Pages 373-382 , July 2008

Nephrotoxicity of Insect and Spider Venoms in Latin America

  • Regina C.R.M. Abdulkader, MD, PhD

      Affiliations

    • Laboratory of Renal Physiopathology, School of Medicine, University of São Paulo, São Paulo, Brazil.
    • Corresponding Author InformationAddress reprint requests to Regina C. R. M. Abdulkader, Laboratório de Fisiopatologia Renal, LIM 16, Faculdade de Medicina da Universidade de São Paulo, Av. Dr. Arnaldo, 455, Sala 3342, Cerqueira César, 01246-903 São Paulo, SP, Brazil.
    • ,
  • Katia C. Barbaro, PhD

      Affiliations

    • Laboratory of Immunopathology, Butantan Institute, São Paulo, Brazil.
    • ,
  • Elvino José Guradão Barros, MD, PhD

      Affiliations

    • Department of Internal Medicine, Federal University of Rio Grande do Sul School of Medicine, Porto Alegre, Brazil.
    • ,
  • Emmanuel A. Burdmann, MD, PhD

      Affiliations

    • Division of Nephrology, São José do Rio Preto Medical School, São Paulo, Brazil.

References 

  1. Watson WA, Litovitz TL, Rodgers GC, Klein-Schwartz W, Reid N, Youniss J, et al. 2004 Annual report of the American association of poison control centers toxic exposure surveillance system. Am J Emerg Med. 2005;23:589–666
  2. Cupo P, Azevedo-Marques MM, Hering SE. Escorpionismo. In:  Cardoso JLC,  França FOS,  Wen FH,  Málaque CMS,  Haddad V editor. Animais peçonhentos no Brasil. São Paulo: Sarvier; 2003;
  3. Habermann E. Bee and wasp venoms. Science. 1972;177:314–322
  4. Piek T. Pharmacology of Hymenoptera venoms. In:  Tu AT editors. Handbook of natural toxins. Vol 2:New York: Marcel Dekker; 1984;p. 135–185
  5. Shipolini RA. Biochemistry of bee venom. In:  Tu AT editors. Handbook of natural toxins. Vol 2:New York: Marcel Dekker; 1984;p. 49–85
  6. Dotimas EM, Hider RC. Honeybee venom. Bee World. 1987;67:51–70
  7. Schumacher MJ, Schmidt JO, Egen NB, Lowry JE. Quantity, analysis, and lethality of European and Africanized honey bee venoms. Am J Trop Med Hyg. 1990;43:79–86
  8. Matsuzaki K, Yoneyama S, Miyajima K. Pore formation and translocation of mellitin. Biophys J. 1997;73:831–838
  9. Lee SY, Park HS, Lee SJ, Choi M. Melittin exerts multiple effects on the release of free fatty acids from L1210 cells: lack of selective activation of phospholipase A2 by melittin. Arch Biochem Biophys. 2001;389:57–67
  10. Constantinescu I, Lafleur M. Influence of the lipid composition on the kinetics concerted insertion and folding of melittin in bilayers. Biochim Biophys Acta. 2004;1667:26–27
  11. Fletcher JE, Jiang MS. Possible mechanisms of action of cobra snake venom cardiotoxins and bee venom melittin. Toxicon. 1993;31:669–695
  12. Azevedo-Marques MM, Ferreira DD, Costa RS. Rhabdomyonecrosis experimentally induced in Wistar rats by Africanized bee venom. Toxicon. 1992;30:344–348
  13. Ownby CL, Powell JR, Jiang MS, Fletcher JE. Melittin and phospholipase A2 from bee (Apis mellifera) venom cause necrosis of murine skeletal muscle in vivo. Toxicon. 1997;35:67–80
  14. Han HJ, Lee JH, Park SH, Choi HJ, Yang IS, Mar WC, et al. Effect of bee venom and its melittin on apical transporters of renal proximal tubule cells. Kidney Blood Press Res. 2000;23:393–399
  15. Han HJ, Park SH, Lee JH, Yoon BC, Park KM, Mar WC, et al. Involvement of oxidative stress in bee venom-induced inhibition of Na+/glucose cotransporter in renal proximal cells. Clin Exp Pharmacol Physiol. 2002;29:564–568
  16. da Silva PH, da Silveira RB, Appel MH, Mangili OC, Gremski W, Veiga SS. Brown spider and loxoscelism. Toxicon. 2004;44:693–709
  17. Hogan CJ, Barbaro KC, Winkel K. Loxoscelism: old obstacles, new directions. Ann Emerg Med. 2004;44:608–624
  18. Castro CS, Silvestre FG, Araújo SC, Gabriel MY, Mangili OC, Cruz I, et al. Identification and molecular cloning of insecticidal toxins from the venom of the brown spider Loxosceles intermedia. Toxicon. 2004;44:273–280
  19. Smith CW, Micks DW. The role of polymorphonuclear leukocytes in the lesion caused by the venom of brown spider, Loxosceles reclusa. Lab Invest. 1970;22:90–93
  20. Swanson DL, Vetter RS. Loxoscelism. Clin Dermatol. 2006;24:213–221
  21. Tambourgi DV, Morgan BP, Andrade RMG, Magnoli FC, Berg CW. Loxosceles intermedia spider envenomation induces activation of an endogenous metalloproteinase, resulting in cleavage of glycophorins from the erythrocyte surface and facilitating complement-mediated lysis. Blood. 2000;9:683–691
  22. Patel KD, Modur V, Zimmerman GA. The necrotic venom of the brown recluse spider induces dysregulated endothelial cell-dependent neutrophil activation: differential induction of GM-CSF, IL-8, and E-selectin expression. J Clin Invest. 1994;94:631–642
  23. Desai A, Miller MJ, Gomez HF, Warren JS. Loxosceles deserta spider venom induces NF-kB-dependent chemokine production by endothelial cells. Clin Toxicol. 1999;37:447–456
  24. Gomez HF, Miller MJ, Desai A, Warren JS. Loxosceles spider venom induces the production of alpha and beta chemokines: implications for the pathogenesis of dermonecrotic arachnidism. Inflammation. 1999;23:207–215
  25. Málaque CM, Ori M, Santos SA, Andrade DR. Production of TNF-α by primary cultures of human keratinocytes challenged with Loxosceles gaucho venom. Rev Inst Med Trop Sao Paulo. 1999;41:179–182
  26. Desai A, Lankford HA, Warren JS. Loxosceles deserta spider venom induces the expression of vascular endothelial growth factor (VEGF) in keratinocytes. Inflammation. 2000;24:1–9
  27. Kurpiewski G, Forrester LJ, Barrett JT, Campbell BJ. Platelet aggregation and sphingomyelinase D activity of a purified toxin from the venom of Loxosceles reclusa. Biochim Biophys Acta. 1981;678:467–476
  28. da Silva PH, Hashimoto Y, Santos FA, Mangili O, Gremski W, Veiga SS. Hematological cell findings in bone marrow and peripheral blood of rabbits after experimental acute exposure to Loxosceles intermedia (brown spider) venom. Toxicon. 2003;42:155–161
  29. Tavares FL, Sousa-e-Silva MCC, Santoro ML, Barbaro KC, Rebecchi IMM, Sano-Martins IS. Changes in hematological, hemostatic and biochemical parameters induced experimentally in rabbits by Loxosceles gaucho spider venom. Human Exp Toxicol. 2004;23:477–486
  30. Ramos-Cerrillo B, Olvera A, Odell GV, Zamudio F, Paniagua-Sólis J, Alagón A, et al. Genetic and enzymatic characterization of sphingomyelinase D isoforms from the North American fiddleback spiders Loxosceles boneti and Loxosceles reclusa. Toxicon. 2004;44:507–514
  31. Machado LF, Laugesen S, Botelho ED, Ricart CA, Fontes W, Barbaro KC, et al. Proteome analysis of brown spider venom: identification of loxnecrogin isoforms in Loxosceles gaucho venom. Proteomics. 2005;5:2167–2176
  32. Andrade SA, Murakami MT, Cavalcante DP, Arni RK, Tambourgi DV. Kinetic and mechanistic characterization of the sphingomyelinases D from Loxosceles intermedia spider venom. Toxicon. 2006;47:380–386
  33. da Silveira RB, Pigozzo RB, Chaim OM, Appel MH, Dreyfuss JL, Toma L, et al. Molecular cloning and functional characterization of two isoforms of dermonecrotic toxin from Loxosceles intermedia (Brown spider) venom gland. Biochimie. 2006;88:1241–1253
  34. da Silveira RB, Pigozzo RB, Chaim OM, Appel MH, Silva DT, Dreyfuss JL, et al. Two novel dermonecrotic toxins LiRecDT4 and LiRecDT5 from Brown spider (Loxosceles intermedia) venom: from cloning to functional characterization. Biochimie. 2007;89:289–300
  35. Kalapothakis E, Chatzaki M, Gonçalves-Dornelas H, de Castro CS, Silvestre FG, Laborne FV, et al. The Loxtox protein family in Loxosceles intermedia (Mello-Leitão) venom. Toxicon. 2007;50:938–946
  36. Feitosa L, Gremski W, Veiga SS, Elias MCQB, Graner E, Mangili OC, et al. Detection and characterization of metalloproteinases with gelatinolytic, fibronectinolytic and fibrinogenolytic activities in brown spider (Loxosceles intermedia) venom. Toxicon. 1998;36:1039–1051
  37. da Silveira RB, Filho JFS, Mangili OC, Veiga SS, Gremski W, Nader HB, et al. Identification of proteases in the extract of venom glands from brown spider. Toxicon. 2002;40:815–822
  38. Barbaro KC, 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
  39. Veiga SS, Zanetti VC, Braz A, Mangili OC, Gremski W. Extracellular matrix molecules as targets for brown spider venom toxins. Braz J Med Biol Res. 2001;34:843–850
  40. da Silveira RB, Wille ACM, Chaim OM, Appel MH, Silva DT, Franco CRC, et al. Identification, cloning, expression and functional characterization of an astacin-like metalloprotease toxin from Loxosceles intermedia (brown spider) venom. Biochem J. 2007;406:355–363
  41. Luciano MN, Silva PH, Chaim OM, Santos VP, Franco CRC, Soares MFS, et al. Experimental evidence for a direct cytotoxicity of Loxosceles intermedia (brown spider) venom on renal tissue. J Histochem Cytochem. 2004;52:455–467
  42. Wright RP, Elgert KD, Campbell BJ, Barret JT. Hyaluronidase and esterase activities of the venom of the poisonous brown recluse spider. Arch Biochem Biophys. 1973;159:415–426
  43. Young AR, Pincus SJ. Comparison of enzymatic activity from three species of necrotising arachnids in Australia: Loxosceles rufescens, Badumna insignis and Lampona cylindrata. Toxicon. 2001;39:391–400
  44. da Silveira RB, Chaim OM, Mangili OC, Gremski W, Dietrich CP, Nader HB, et al. Hyaluronidases in Loxosceles intermedia (brown spider) venom are endo-b-N-acetylhexosaminidases hydrolases. Toxicon. 2007;49:758–768
  45. Carrijo-Carvalho L, Chudzinski-Tavassi . The venom of the Lonomia caterpillar: an overview. Toxicon. 2007;49:741–757
  46. Arocha-Piñango CL, Layrisse M. Fibrinolysis produced by contact with a caterpillar. Lancet. 1969;7597:810–812
  47. Arocha-Piñango CL, Torres A. Fibrinolytic and procoagulat agents from a saturnidae moth caterpillar. In:  Pirkle H,  Markland B editor. Hemostatic and animal venoms. New York: Marcel Dekker; 1988;p. 223–239
  48. Arocha-Piñango CL, Bosch NB, Torres A, Goldstein C, Nouel A, Argüello A, et al. Six new cases of a caterpillar-induced bleeding syndrome. Thromb Haemost. 1992;67:402–407
  49. Wen FH, Duarte AC. Acidentes por Lonomia. In:  Cardoso JLC,  França FOS,  Wen FH,  Málaque CMS,  Haddad V editor. Animais peçonhentos no Brasil. São Paulo: Sarvier; 2003;
  50. Pinto MA, Rubinack WL, Patton JC, Coulson RN, Johnston JS. Africanization of the United States: replacement of feral European honey bees (Apis mellifera L) by an African hybrid swarm. Genetics. 2005;170:1653–1661
  51. Meier J. Biology and distribution of hymenopterans of medical importance, their venom apparatus and venom composition. In:  Meier J,  White J editor. Handbook of clinical toxicology of animal venoms and poisons. Boca Raton: CRC Press; 1995;p. 331–348
  52. Richers KJ, Gillis D, James RA. An autopsy approach to bee sting-related deaths. Pathology. 2002;34:257–262
  53. Medeiros CR, França FOS. Acidentes por abelhas e vespas. In:  Cardoso JLC,  França FOS,  Wen FH,  Málaque CMS,  Haddad V editor. Animais peçonhentos no Brasil. São Paulo: Sarvier; 2003;
  54. França FOS, Benvenuti LA, Fan HW, Dos Santos DR, Hain SH, Picchi-Martins FR, et al. Severe and fatal mass attacks by “killer” bees (Africanized honey bees—Apis mellifera scutellata) in Brazil: clinicopathological studies with measurement of serum venom concentrations. QJM. 1994;87:269–282
  55. Marsh NA, Whaler BC. The effects of honey bee (Apis mellifera L) venom and two of its components, mellitin and phospholipase A2, on cardiovascular system of the rat. Toxicon. 1980;18:427–435
  56. Okamoto T, Isoda H, Kubota N, Takahata K, Takahashi T, Kishi T, et al. Melittin cardiotoxicity in cultured mouse cardiac myocytes and its correlation with calcium overload. Toxicol Appl Pharmacol. 1995;133:150–163
  57. Vetter RS, Visscher PK, Camazine S. Mass envenomations by honey bees and wasps. West J Med. 1999;170:223–227
  58. Daher EF, Silva GB, Bezerra GP, Pontes LB, Martins AMC, Guimarães JA. Acute renal failure after massive honey bee stings. Rev Inst Med Trop Sao Paulo. 2003;45:45–50
  59. Bresolin NL, Carvalho FLC, Goes JEC, Fernandes VR, Barotto AM. Acute renal failure following massive attack by Africanized bee stings. Pediatr Nephrol. 2002;17:625–627
  60. Gabriel DP, Rodrigues AG, Barsante RC, dos Santos Silva V, Caramori JT, Martim LC, et al. Severe acute renal failure after massive attack of Africanized bees. Nephrol Dial Transplant. 2004;19:2680
  61. Vikrant S, Patial RK. Acute renal failure following multiple honeybee stings. Indian J Med Sci. 2006;60:202–209
  62. Guimarães JV, Costa RS, Machado BH, dos Reis MA. Cardiovascular profile after intravenous injection of Africanized bee venom in awake rats. Rev Inst Med Trop Sao Paulo. 2004;46:55–58
  63. Grisotto LSD, Mendes GE, Castro I, Baptista MASF, Alves VA, Yu L, et al. Mechanisms of bee venom-induced acute renal failure. Toxicon. 2006;48:44–54
  64. dos Reis MA, Costa RS, Coimbra TM, Teixeira VP. Acute renal failure in experimental envenomation with Africanized bee venom. Renal Fail. 1998;20:39–51
  65. dos Reis MA, Costa RS, Coimbra TM, Dantas M, Gomes UA. Renal changes induced by envenomation with Africanized bee venom in female Wistar rats. Kidney Blood Press Res. 1997;20:271–277
  66. Oliveira EC, Pedroso PMO, Meirelles AEWB, Pescador CA, Gouvêa AS, Driemeier D. Pathological findings in dogs after multiple Africanized bee stings. Toxicon. 2007;49:1214–1218
  67. Betten DP, Richardson WH, Tong TC, Clark RF. Massive honey bee envenomation-induced rhabdomyolysis in an adolescent. Pediatrics. 2006;117:231–235
  68. Visscher PK, Vetter RS, Camazine S. Removing bee stings. Lancet. 1996;348:301–302
  69. Ministério da Saúde. Manual de diagnóstico e tratamento de acidentes por animais peçonhentos. Brasília: FUNASA; 1998;
  70. Sezerino UM, Zannin M, Coelho LK, Gonçalves J, Grando M, Mattosinho SG, et al. A clinical and epidemiological study of Loxosceles spider envenoming in Santa Catarina, Brazil. Trans R Soc Trop Med Hyg. 1998;92:546–548
  71. Málaque CMS, Castro-Valencia JE, Cardoso JLC, França FOS, Barbaro KC, Fan HW. Clinical and epidemiological features of definitive and presumed loxoscelism in São Paulo, Brazil. Rev Inst Med Trop Sao Paulo. 2002;44:139–143
  72. França FO, Barbaro KC, Abdulkader RC. Rhabdomyolysis in presumed viscero-cutaneous loxoscelism: report of two cases. Trans R Soc Trop Med Hyg. 2002;96:287–290
  73. Schenone H, Saavedra T, Rojas A, Villarroel F. Loxoscelismo en Chile (Estudios epidemiologicos, clinicos y experimentales). Rev Inst Med Trop Sao Paulo. 1989;31:403–415
  74. Barbaro KC, Ferreira ML, Cardoso DF, Eickstedt VRD, Mota I. Identification and neutralization of biological activities in the venoms of Loxosceles spiders. Braz J Med Biol Res. 1996;29:1491–1497
  75. Ospedal KZ, Appel MH, Neto JF, Mangili OC, Veiga SS, Gremski W. Histopathological findings in rabbits after experimental acute exposure to the Loxosceles intermedia (brown spider) venom. Int J Exp Pathol. 2002;84:287–294
  76. Lucato RV, Mendes GEF, Castro I, Barbaro K, Abdulkader R, Yu L, et al. Loxosceles-venom (LV) induced renal injury—in vivo and in vitro studies. J Am Soc Nephrol. 2005;16:315A
  77. Chaim OM, Sade YB, da Silveira RB, Toma L, Kalapothakis E, Chávez-Olórtegui C, et al. Brown spider dermonecrotic toxin directly induces nephrotoxicity. Toxicol Appl Pharmacol. 2006;211:64–77
  78. Veiga AB, Blochtein B, Guimarães JA. Structures involved production, secretion, and injection of the venom produced by the caterpillars Lonomia obliqua (Lepdoptera, Saturniidae). Toxicon. 2001;39:1343–1351
  79. Seibert CS, Shinohara EMG, Sano-Martins IS. In vitro hemolytic of Lonomia obliqua caterpillar bristle extract on human and Wistar rat erythrocytes. Toxicon. 2003;41:831–839
  80. Zannin M, Lourenço DM, Motta G, Dalla Costa LR, Grando M, Gamborgi GP, et al. Blood coagulation and fibrinolytic factors in 105 patients with hemorrhagic syndrome caused by accidental contact with Lonomia obliqua caterpillar in Santa Catarina, Southern Brazil. Thromb Haemost. 2003;89:355–364
  81. Gamborgi GP, Metcalf EB, Barros EJB. Acute renal failure provoked by toxin from caterpillars of the species Lonomia obliqua. Toxicon. 2006;47:68–74
  82. Garcia CM, Danni-Oliveira IM. Occurrence of accidents caused by Lonomia oblique walker, in the state of Paraná between 1989 and 2001. Rev Soc Bras Med Trop. 2007;40:242–246
  83. Alvarenga ZA. Taturana. Paper presented at: VIII Congresso Brasileiro de Medicina Cirúrgica. 1912;II:132–135Belo Horizonte, MG.
  84. Duarte AC, Caovilla JJ, Lorini JD, Mantovani G, Sumida J, Manfre PC, et al. Insuficiência renal aguda por acidentes com lagartas. J Bras Nefrol. 1990;12:184–187
  85. Duarte ACL, Crusius PS, Pires CAL, Schiling MA, Fan HW. Intracerebral haemorrhage after contact with Lonomia caterpillars. Lancet. 1996;348:1033
  86. Caovilla JJ, Barros EJG. Efficacy of two different doses of antilonomic serum in the resolution of hemorrhagic syndrome resulting from envenoming by Lonomia obliqua caterpillars: a randomized controlled trial. Toxicon. 2004;43:811–818
  87. Wolff JL, Moraes RHP, Kitagima E, Leal ES, Zanotto PMA. Identification and characterization of baculovirus from Lonomia obliqua (Lepidoptera: Saturniidae). J Invertebr Pathol. 2003;79:137–145
  88. Kelen EMA, Picarelli ZP, Duarte AC. Hemorrhagic syndrome induced by contact with caterpillars of the genus Lonomia (Saturnidae, hemileucinae). J Toxicol Toxin Rev. 1995;14:283–308
  89. Duarte AC, Crusius PS, Pires CAL. Insuficiência renal aguda nos acidentes com Lonomia obliqua. Nefrol Latin Am. 1994;1:38–40
  90. Burdmann EA, Antunes L, Saldanha LB, Abdulkader RCMR. Severe acute renal failure induced by the venom of Lonomia caterpillars. Clin Nephrol. 1996;46:337–339
  91. Fan HW, Cardoso JLC, Olmo RD, Almeida FJ, Viana RP, Martinez APP. Hemorrhagic syndrome and acute renal failure in a pregnant woman after contact with Lonomia caterpillars; a case report. Rev Inst Med Trop Sao Paulo. 1998;40:1–5
  92. Brazilian Ministry of Health. [cited 2007 November 5] http://dtr2004.saude.gov.br/sinanweb/index.php?name=Tnet

 Supported in part by grants from the Foundation for the Support of Research in the State of São Paulo (Fundação de Amparo à Pesquisa do Estado de São Paulo) and from the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico) (E.A.B. and K.C.B.).

PII: S0270-9295(08)00084-3

doi: 10.1016/j.semnephrol.2008.04.006

Seminars in Nephrology
Volume 28, Issue 4 , Pages 373-382 , July 2008

Article Tools

* Image Usage & Resolution