Identification of a direct hemolytic effect dependent on the catalytic activity induced by phospholipase-D (dermonecrotic toxin) from brown spider venom

Journal of Cellular Biochemistry

Volumn 107, Issue 4, 2009, Pages 655-666

  Chaves Moreira, Daniele ^a   Chaim, Olga M ^a,b   Sade, Youssef B ^a   Paludo, Kátia S ^a,b   Gremski, Luiza H ^a,b   Donatti, Lucélia ^a   De Moura, Juliana ^a   Mangili, Oldemir C ^a   Gremski, Waldemiro ^a,c   Da Silveira, Rafael B ^d   Senff Ribeiro, Andrea ^a   Veiga, Silvio S ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c PONTIFICAL CATHOLIC UNIVERSITY OF PARANÁ   (Brazil)

^d STATE UNIVERSITY OF PONTA GROSSA   (Brazil)

Author keywords

Brown spider; Catalysis; Hemolysis; Phospholipase D; Venom

Indexed keywords

LIPOCORTIN 5; MAGNESIUM; PHOSPHOLIPASE D; SERINE PROTEINASE INHIBITOR; SPIDER VENOM;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ERYTHROCYTE MEMBRANE; ERYTHROCYTE SHAPE; ERYTHROCYTE VOLUME; HEMOLYSIS; HORSE; HUMAN; HUMAN CELL; LIPID RAFT; MEMBRANE BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RABBIT; SHEEP;

ANIMALS; CATALYSIS; CELL SHAPE; CELL SIZE; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; HEMOLYSIS; HUMANS; PHOSPHOLIPASE D; RABBITS; SHEEP; SPIDER VENOMS;

ARANEAE; EQUIDAE; ORYCTOLAGUS CUNICULUS; OVIS ARIES;

EID: 67650076245     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22148     Document Type: Article

References (48)

1. Anliker B, Chun J. 2004. Lysophospholipid G protein-coupled receptors. J Biol Chem 279:20555-20558.
2. Appel MH, da Silveira RB, Chaim OM, Paludo KS, Silva DT, Chaves DM, da Silva PH, Mangili OC, Senff-Ribeiro A, Gremski W, Nader HB, Veiga SS. 2008. Identification, cloning and functional characterization of a novel dermonecrotic toxin (phospholipase D) from brown spider (Loxosceles intermedia) venom. Biochim Biophys Acta 1780:167-178.
3. Barbaro KC, Cardoso JL, Eickstedt VR, Mota I. 1992. Dermonecrotic and lethal components of Loxosceles gaucho spider venom. Toxicon 30:331-338.
4. Barbaro KC, Eickstedt VR, Mota I. 1994. Antigenic cross-reactivity of venoms from medically important Loxosceles (Araneae) species in Brazil. Toxicon 32:113-120. (Pubitemid 24047967)
5. Barbaro KC, Knysak I, Martins R, Hogan C, Winkel K. 2005. Enzymatic characterization, antigenic cross-reactivity and neutralization of dermonecrotic activity of five Loxosceles spider venoms of medical importance in the Americas. Toxicon 45:489-499. (Pubitemid 40269939)
6. Chaim OM, Sade YB, da Silveira RB, Toma L, Kalapothakis E, Chavez-Olortegui C, Mangili OC, Gremski W, von Dietrich CP, Nader HB, Sanches Veiga S. 2006. Brown spider dermonecrotic toxin directly induces nephrotoxicity. Toxicol Appl Pharmacol 211:64-77.
7. Chung SM, Bae ON, Lim KM, Noh JY, Lee MY, Jung YS, Chung JH. 2007. Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol 27:414-421. (Pubitemid 46143059)
8. Closse C, Dachary-Prigent J, Boisseau MR. 1999. Phosphatidylserine- related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 107:300-302. (Pubitemid 29530214)
9. da Silva PH, da Silveira RB, Appel MH, Mangili OC, Gremski W, Veiga SS. 2004. Brown spiders and loxoscelism. Toxicon 44:693-709.
10. da Silveira RB, Pigozzo RB, Chaim OM, Appel MH, Dreyfuss JL, Toma L, Mangili OC, Gremski W, Dietrich CP, Nader HB, Veiga SS. 2006. Molecular cloning and functional characterization of two isoforms of dermonecrotic toxin from Loxosceles intermedia (brown spider) venom gland. Biochimie 88:1241-1253.
11. da Silveira RB, Chaim OM, Mangili OC, Gremski W, Dietrich CP, Nader HB, Veiga SS. 2007a. Hyaluronidases in Loxosceles intermedia (Brown spider) venom are endo-beta-N-acetyl-d-hexosaminidases hydrolases. Toxicon 49:758-768.
12. da Silveira RB, Pigozzo RB, Chaim OM, Appel MH, Silva DT, Dreyfuss JL, Toma L, Dietrich CP, Nader HB, Veiga SS, Gremski W. 2007b. Two novel dermonecrotic toxins LiRecDT4 and LiRecDT5 from brown spider (Loxosceles intermedia) venom: From cloning to functional characterization. Biochimie 89:289-300.
13. da Silveira RB, Wille AC, Chaim OM, Appel MH, Silva DT, Franco CR, Toma L, Mangili OC, Gremski W, Dietrich CP, Nader HB, Veiga SS. 2007c. Identification, cloning, expression and functional characterization of an astacin-like metalloprotease toxin from Loxosceles intermedia (brown spider) venom. Biochem J 406:355-363.
14. de Castro CS, Silvestre FG, Araujo SC, Gabriel de MY, Mangili OC, Cruz I, Chavez-Olortegui C, Kalapothakis E. 2004. Identification and molecular cloning of insecticidal toxins from the venom of the brown spider Loxosceles intermedia. Toxicon 44:273-280. (Pubitemid 39078343)
15. de Souza AL, Malaque CM, Sztajnbok J, Romano CC, Duarte AJ, Seguro AC. 2008. Loxosceles venom-induced cytokine activation, hemolysis, and acute kidney injury. Toxicon 51:151-156.
16. Feitosa L, Gremski W, Veiga SS, Elias MC, Graner E, Mangili OC, Brentani RR. 1998. Detection and characterization of metalloproteinases with gelatinolytic, fibronectinolytic and fibrinogenolytic activities in brown spider (Loxosceles intermedia) venom. Toxicon 36:1039-1051. (Pubitemid 28305397)
17. Forrester LJ, Barrett JT, Campbell BJ. 1978. Red blood cell lysis induced by the venom of the brown recluse spider: The role of sphingomyelinase D. Arch Biochem Biophys 187:355-365. (Pubitemid 8335748)
18. França FO, Barbaro KC, Abdulkader RC. 2002. Rhabdomyolysis in presumed viscero-cutaneous loxoscelism: Report of two cases. Trans R Soc Trop Med Hyg 96:287-290. (Pubitemid 34785067)
19. Futrell JM. 1992. Loxoscelism. Am J Med Sci 304:261-267.
20. Harris F, Phoenix DA. 1997. An investigation into the ability of C-terminal homologues of Escherichia coli low molecular mass penicillin-binding proteins 4, 5 and 6 to undergo membrane interaction. Biochimie 79:171-174. (Pubitemid 27302871)
21. Ingraham LM, Burns CP, Boxer LA, Baehner RL, Haak RA. 1981. Fluidity properties and liquid composition of erythrocyte membranes in Chediak-Higashi syndrome. J Cell Biol 89:510-516. (Pubitemid 11035958)
22. Kalapothakis E, Chatzaki M, Goncalves-Dornelas H, de Castro CS, Silvestre FG, Laborne FV, de Moura JF, Veiga SS, Chavez-Olortegui C, Granier C, Barbaro KC. 2007. The Loxtox protein family in Loxosceles intermedia (Mello-Leitao) venom. Toxicon 50:938-946. (Pubitemid 350026575)
23. Kalfa TA, Pushkaran S, Mohandas N, Hartwig JH, Fowler VM, Johnson JF, Joiner CH, Williams DA, Zheng Y. 2006. Rac GTPases regulate the morphology and deformability of the erythrocyte cytoskeleton. Blood 108:3637-3645. (Pubitemid 44864539)
24. Kurpiewski G, Forrester LJ, Barrett JT, Campbell BJ. 1981. Platelet aggregation and sphingomyelinase D activity of a purified toxin from the venom of Loxosceles reclusa. Biochim Biophys Acta 678:467-476. (Pubitemid 12170689)
25. Kusma J, Chaim OM, Wille AC, Ferrer VP, Sade YB, Donatti L, Gremski W, Mangili OC, Veiga SS. 2008. Nephrotoxicity caused by brown spider venom phospholipase-D (dermonecrotic toxin) depends on catalytic activity. Biochimie 90:1722-1736.
26. Lang KS, Lang PA, Bauer C, Duranton C, Wieder T, Huber SM, Lang F. 2005. Mechanisms of suicidal erythrocyte death. Cell Physiol Biochem 15:195-202.
27. Lang F, Huber SM, Szabo I, Gulbins E. 2007. Plasma membrane ion channels in suicidal cell death. Arch Biochem Biophys 462:189-194. (Pubitemid 46856316)
28. Lee S, Lynch KR. 2005. Brown recluse spider (Loxosceles reclusa) venom phospholipase D (PLD) generates lysophosphatidic acid (LPA). Biochem J 391:317-323.
29. Luciano MN, da Silva PH, Chaim OM, dos Santos VL, Franco CR, Soares MF, Zanata SM, Mangili OC, Gremski W, Veiga SS. 2004. Experimental evidence for a direct cytotoxicity of Loxosceles intermedia (brown spider) venom in renal tissue. J Histochem Cytochem 52:455-467.
30. Lung JM, Mallory SB. 2000. A child with spider bite and glomerulonephritis: A diagnostic challenge. Int J Dermatol 39:287-289. (Pubitemid 30260808)
31. Machado LF, Laugesen S, Botelho ED, Ricart CA, Fontes W, Barbaro KC, Roepstorff P, Sousa MV. 2005. Proteome analysis of brown spider venom: Identification of loxnecrogin isoforms in Loxosceles gaucho venom. Proteomics 5:2167-2176. (Pubitemid 40770580)
32. Mitsutake S, Igarashi Y. 2007. Transbilayer movement of ceramide in the plasma membrane of live cells. Biochem Biophys Res Commun 359:622-627. (Pubitemid 46898996)
33. Moolenaar WH, van Meeteren LA, Giepmans BN. 2004. The ins and outs of lysophosphatidic acid signaling. Bioessays 26:870-881. (Pubitemid 39128101)
34. Murakami MT, Fernandes-Pedrosa MF, Tambourgi DV, Arni RK. 2005. Structural basis for metal ion coordination and the catalytic mechanism of sphingomyelinases D. J Biol Chem 280:13658-13664. (Pubitemid 40517260)
35. Murakami MT, Fernandes-Pedrosa MF, de Andrade SA, Gabdoulkhakov A, Betzel C, Tambourgi DV, Arni RK. 2006. Structural insights into the catalytic mechanism of sphingomyelinases D and evolutionary relationship to glycerophosphodiester phosphodiesterases. Biochem Biophys Res Commun 342:323-329. (Pubitemid 43247394)
36. Ochi S, Oda M, Nagahama M, Sakurai J. 2003. Clostridium perfringens alpha-toxin-induced hemolysis of horse erythrocytes is dependent on Ca2+ uptake. Biochim Biophys Acta 1613:79-86. (Pubitemid 36776511)
37. Ochi S, Oda M, Matsuda H, Ikari S, Sakurai J. 2004. Clostridium perfringens alpha-toxin activates the sphingomyelin metabolism system in sheep erythrocytes. J Biol Chem 279:12181-12189. (Pubitemid 38445783)
38. Oda M, Matsuno T, Shiihara R, Ochi S, Yamauchi R, Saito Y, Imagawa H, Nagahama M, Nishizawa M, Sakurai J. 2008. The relationship between the metabolism of sphingomyelin species and the hemolysis of sheep erythrocytes induced by Clostridium perfringens alpha-toxin. J Lipid Res 49:1039-1047.
39. Ramos-Cerrillo B, Olvera A, Odell GV, Zamudio F, Paniagua-Solis J, Alagon A, Stock RP. 2004. Genetic and enzymatic characterization of sphingomyelinase D isoforms from the North American fiddleback spiders Loxosceles boneti and Loxosceles reclusa. Toxicon 44:507-514. (Pubitemid 39278373)
40. Ribeiro RO, Chaim OM, da Silveira RB, Gremski LH, Sade YB, Paludo KS, Senff-Ribeiro A, de Moura J, Chavez-Olortegui C, Gremski W, Nader HB, Veiga SS. 2007. Biological and structural comparison of recombinant phospholipase D toxins from Loxosceles intermedia (brown spider) venom. Toxicon 50:1162-1174.
41. Sakurai J, Nagahama M, Oda M. 2004. Clostridium perfringens alpha-toxin: Characterization and mode of action. J Biochem 136:569-574. (Pubitemid 40364178)
42. Soares AM, Oshima-Franco Y, Vieira CA, Leite GB, Fletcher JE, Jiang MS, Cintra AC, Giglio JR, Rodrigues-Simioni L. 2002. Mn(2+) ions reduce the enzymatic and pharmacological activities of bothropstoxin-I, a myotoxic Lys49 phospholipase A(2) homologue from Bothrops jararacussu snake venom. Int J Biochem Cell Biol 34:668-677.
43. Swanson DL, Vetter RS. 2006. Loxoscelism. Clin Dermatol 24:213-221.
44. Tokumura A. 2004. Metabolic pathways and physiological and pathological significances of lysolipid phosphate mediators. J Cell Biochem 92:869-881. (Pubitemid 44264238)
45. Udden MM. 2005. Effects of diethylene glycol butyl ether and butoxyethoxyacetic acid on rat and human erythrocytes. Toxicol Lett 156:95-101. (Pubitemid 40221766)
46. Williams ST, Khare VK, Johnston GA, Blackall DP. 1995. Severe intravascular hemolysis associated with brown recluse spider envenomation. A report of two cases and review of the literature. Am J Clin Pathol 104:463-467.
47. Wood BL, Gibson DF, Tait JF. 1996. Increased erythrocyte phosphatidylserine exposure in sickle cell disease: Flow-cytometric measurement and clinical associations. Blood 88:1873-1880. (Pubitemid 26307087)
48. Young AR, Pincus SJ. 2001. Comparison of enzymatic activity from three species of necrotising arachnids in Australia: Loxosceles rufescens, Badumna insignis and Lampona cylindrata. Toxicon 39:391-400. (Pubitemid 30649088)