Potential Implications for Designing Drugs Against the Brown Spider Venom Phospholipase-D

Journal of Cellular Biochemistry

Volumn 118, Issue 4, 2017, Pages 726-738

  Chaves Moreira, Daniele ^a   de Moraes, Fábio Rogério ^b   Caruso, Ícaro Putinhon ^b   Chaim, Olga Meiri ^a   Senff Ribeiro, Andrea ^a   Ullah, Anwar ^b,c   da Silva, Luciane Sussuchi ^b   Chahine, Jorge ^b   Arni, Raghuvir K ^b   Veiga, Silvio Sanches ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c COMSATS Institute of Information Technology ^*  (Pakistan)

Author keywords

BROWN SPIDER; INHIBITOR; LOXOSCELES INTERMEDIA; RECOMBINANT TOXIN; VENOM PHOSPHOLIPASE D

Indexed keywords

PHOSPHOLIPASE D; SPIDER VENOM ANTISERUM; ARTHROPOD PROTEIN; BENZIMIDAZOLE DERIVATIVE; DERMONECROTIC TOXIN, LOXOSCELES INTERMEDIA; ENZYME INHIBITOR; LIGAND; LOXOSCELES VENOM; N-(2-(4-(2-OXO-2,3-DIHYDRO-1H-BENZO(D)IMIDAZOL-1-YL)PIPERIDIN-1-YL)ETHYL)-2-NAPHTHAMIDE; PHOSPHODIESTERASE; PIPERIDINE DERIVATIVE; RECOMBINANT PROTEIN; SPIDER VENOM; SURAMIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOASSAY; CONTROLLED STUDY; DRUG DESIGN; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; HEMOLYSIS; IN VITRO STUDY; INFLAMMATION; LIGAND BINDING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; SKIN NECROSIS; ANIMAL; ANTAGONISTS AND INHIBITORS; BROWN RECLUSE SPIDER; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; HUMAN; KINETICS; LEPORIDAE; NECROSIS; PATHOGENICITY; PATHOLOGY; PRECLINICAL STUDY; SKIN; SPIDER BITES;

ANIMALS; ARTHROPOD PROTEINS; BENZIMIDAZOLES; BROWN RECLUSE SPIDER; DRUG DESIGN; DRUG EVALUATION, PRECLINICAL; ENZYME INHIBITORS; HEMOLYSIS; HUMANS; KINETICS; LIGANDS; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; NECROSIS; PHOSPHOLIPASE D; PHOSPHORIC DIESTER HYDROLASES; PIPERIDINES; RABBITS; RECOMBINANT PROTEINS; SKIN; SPIDER BITES; SPIDER VENOMS; SURAMIN;

EID: 84997733305     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25678     Document Type: Article

References (53)

1. Angulo J, Enriquez-Navas PM, Nieto PM. 2010. Ligand-receptor binding affinities from saturation transfer difference (STD) NMR spectroscopy: The binding isotherm of STD initial growth rates. Chemistry 16:7803–7812.
2. Appel MH, da Silveira RB, Gremski W, Veiga SS. 2005. Insights into brown spider and loxoscelism. ISJ 2:152–158.
3. 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.
4. Bieri M, Kwan AH, Mobli M, King GF, Mackay JP, Gooley PR. 2011. Macromolecular NMR spectroscopy for the non-spectroscopist: Beyond macromolecular solution structure determination. FEBS J 278:704–715.
5. Boularot A, Giglione C, Petit S, Duroc Y, Alves de Sousa R, Larue V, Cresteil T, Dardel F, Artaud I, Meinnel T. 2007. Discovery and refinement of a new structural class of potent peptide deformylase inhibitors. J Med Chem 50:10–20.
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. Chaim OM, da Silveira RB, Trevisan-Silva D, Ferrer VP, Sade YB, Boia-Ferreira M, Gremski LH, Gremski W, Senff-Ribeiro A, Takahashi HK, Toledo MS, Nader HB, Veiga SS. 2011a. Phospholipase-D activity and inflammatory response induced by brown spider dermonecrotic toxin: Endothelial cell membrane phospholipids as targets for toxicity. Biochim Biophys Acta 1811:84–96.
8. Chaim OM, Trevisan-Silva D, Chaves-Moreira D, Wille AC, Ferrer VP, Matsubara FH, Mangili OC, da Silveira RB, Gremski LH, Gremski W, Senff-Ribeiro A, Veiga SS. 2011b. Brown spider (Loxosceles genus) venom toxins: Tools for biological purposes. Toxins (Basel) 3:309–344.
9. Chaves-Moreira D, Chaim OM, Sade YB, Paludo KS, Gremski LH, Donatti L, de Moura J, Mangili OC, Gremski W, da Silveira RB, Senff-Ribeiro A, Veiga SS. 2009. Identification of a direct hemolytic effect dependent on the catalytic activity induced by phospholipase-D (dermonecrotic toxin) from brown spider venom. J Cell Biochem 107:655–666.
10. Chaves-Moreira D, Trevisan-Silva D, Gremski LH, Veiga SS. 2014. Brown spider venom: The identification and biotechnological potential of venom toxins. In: Gopalakrishnakone P, editor. Venom genomics and proteomics. Netherlands: Springer. pp 1–22.
11. Cooper A, Nutley MA, Wadood A. 2000. Differential scanning microcalorimetry. In: Harding SE, Chowdhry BZ, editors. Protein-ligand interactions: Hydrodynamics and calorimetry. Oxford: Oxford University Press. pp 287–318.
12. Coronado MA, Ullah A, da Silva LS, Chaves-Moreira D, Vuitika L, Chaim OM, Veiga SS, Chahine J, Murakami MT, Arni RK. 2015. Structural insights into substrate binding of brown spider venom class II phospholipases D. Curr Protein Pept Sci 16(8): 768-774
13. da Silva PH, da Silveira RB, Appel MH, Mangili OC, Gremski W, Veiga SS. 2004. Brown spiders and loxoscelism. Toxicon 44:693–709.
14. 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.
15. da Silveira RB, Pigozzo RB, Chaim OM, Appel MH, Silva DT, Dreyfuss JL, Toma L, Dietrich CP, Nader HB, Veiga SS, Gremski W. 2007. Two novel dermonecrotic toxins LiRecDT4 and LiRecDT5 from brown spider (Loxosceles intermedia) venom: From cloning to functional characterization. Biochimie 89:289–300.
16. de Giuseppe PO, Ullah A, Silva DT, Gremski LH, Wille AC, Chaves Moreira D, Ribeiro AS, Chaim OM, Murakami MT, Veiga SS, Arni RK. 2011. Structure of a novel class II phospholipase D: Catalytic cleft is modified by a disulphide bridge. Biochem Biophys Res Commun 409:622–627.
17. Fernandes-Pedrosa F, Junqueira de Azevedo Ide L, Goncalves-de-Andrade RM, van den Berg CW, Ramos CR, Ho PL, Tambourgi DV. 2002. Molecular cloning and expression of a functional dermonecrotic and haemolytic factor from Loxosceles laeta venom. Biochem Biophys Res Commun 298:638–645.
18. Ganesan R, Mahankali M, Alter G, Gomez-Cambronero J. 2014. Two sites of action for PLD2 inhibitors: The enzyme catalytic center and an allosteric, phosphoinositide biding pocket. Biochim Biophys Acta 1851:261–272.
19. Gremski LH, da Silveira RB, Chaim OM, Probst CM, Ferrer VP, Nowatzki J, Weinschutz HC, Madeira HM, Gremski W, Nader HB, Senff-Ribeiro A, Veiga SS. 2010. A novel expression profile of the Loxosceles intermedia spider venomous gland revealed by transcriptome analysis. Mol Biosyst 6(12):2403–2416.
20. Gremski LH, Trevisan-Silva D, Ferrer VP, Matsubara FH, Meissner GO, Wille AC, Vuitika L, Dias-Lopes C, Ullah A, de Moraes FR, Chavez-Olortegui C, Barbaro KC, Murakami MT, Arni RK, Senff-Ribeiro A, Chaim OM, Veiga SS. 2014. Recent advances in the understanding of brown spider venoms: From the biology of spiders to the molecular mechanisms of toxins. Toxicon 83:91–120.
21. Hogan CJ, Barbaro KC, Winkel K. 2004. Loxoscelism: Old obstacles, new directions. Ann Emerg Med 44:608–624.
22. Horta CC, Oliveira-Mendes BB, do Carmo AO, Siqueira FF, Barroca TM, dos Santos Nassif Lacerda SM, de Almeida Campos PH, Jr., de Franca LR, Ferreira RL, Kalapothakis E. 2013. Lysophosphatidic acid mediates the release of cytokines and chemokines by human fibroblasts treated with loxosceles spider venom. J Invest Dermatol 133:1682–1685.
23. Isbister GK, Fan HW. 2011. Spider bite. Lancet 378:2039–2047.
24. Janowski PA, Liu C, Deckman J, Case DA. 2016. Molecular dynamics simulation of triclinic lysozyme in a crystal lattice. Protein Sci 25(1):87–102.
25. Lajoie DM, Zobel-Thropp PA, Kumirov VK, Bandarian V, Binford GJ, Cordes MH. 2013. Phospholipase D toxins of brown spider venom convert lysophosphatidylcholine and sphingomyelin to cyclic phosphates. PLoS ONE 8:e72372.
26. Lajoie DM, Roberts SA, Zobel-Thropp PA, Delahaye JL, Bandarian V, Binford GJ, Cordes MH. 2015. Variable substrate preference among phospholipase d toxins from sicariid spiders. J Biol Chem 290:10994–11007.
27. Lee S, Lynch KR. 2005. Brown recluse spider (Loxosceles reclusa) venom phospholipase D (PLD) generates lysophosphatidic acid (LPA). Biochem J 391:317–323.
28. Li P, Roberts BP, Chakravorty DK, Merz KM, J. 2013. Rational design of particle mesh ewald compatible lennard-Jones parameters for +2 metal cations in explicit solvent. J Chem Theory Comput 9:2733–2748.
29. Lindae A, Eberle RJ, Caruso IP, Coronado MA, de Moraes FR, Azevedo V, Arni RK. 2015. Expression, purification and characterization of cold shock protein A of Corynebacterium pseudotuberculosis. Protein Expr Purif 112:15–20.
30. Lomize MA, Pogozheva ID, Joo H, Mosberg HI, Lomize AL. 2012. OPM database and PPM web server: Resources for positioning of proteins in membranes. Nucleic Acids Res 40:D370–D376.
31. Malaque CMS, Chaim OM, Entres M, Barbaro KC. 2016. Loxosceles and loxoscelism: Biology, venom, envenomation and treatment, Part III. Netherlands: Springer Science Spider Venoms, pp 419–444.
32. Mayer M, Meyer B. 2001. Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor. J Am Chem Soc 123:6108–6117.
33. McCain DF, Wu L, Nickel P, Kassack MU, Kreimeyer A, Gagliardi A, Collins DC, Zhang ZY. 2004. Suramin derivatives as inhibitors and activators of protein-tyrosine phosphatases. J Biol Chem 279:14713–14725.
34. McGeary RP, Bennett AJ, Tran QB, Cosgrove KL, Ross BP. 2008. Suramin: Clinical uses and structure-activity relationships. Mini Rev Med Chem 8:1384–1394.
35. Milhas D, Clarke CJ, Hannun YA. 2009. Sphingomyelin metabolism at the plasma membrane: Implications for bioactive sphingolipids. FEBS Lett 584:1887–1894.
36. Morris GM, Huey R, Olson AJ. 2008. Using AutoDock for ligand-receptor docking. Curr Protoc Bioinformatics 14:1–8.
37. Murakami MT, Arruda EZ, Melo PA, Martinez AB, Calil-Elias S, Tomaz MA, Lomonte B, Gutierrez JM, Arni RK. 2005a. Inhibition of myotoxic activity of Bothrops asper myotoxin II by the anti-trypanosomal drug Suramin. J Mol Biol 350:416–426.
38. Murakami MT, Fernandes-Pedrosa MF, Tambourgi DV, Arni RK. 2005b. Structural basis for metal ion coordination and the catalytic mechanism of sphingomyelinases D. J Biol Chem 280:13658–13664.
39. 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.
40. Nauseef WM. 2014. Myeloperoxidase in human neutrophil host defence. Cell Microbiol 16:1146–1155.
41. Peterson ME. 2006. Brown spider envenomation. Clin Tech Small Anim Pract 21:191–193.
42. Pettus BJ, Chalfant CE, Hannun YA. 2004. Sphingolipids in inflammation: Roles and implications. Curr Mol Med 4:405–418.
43. Platinick NI. 2013. The World Spider Catalog. The American Museum of Natural History 14.5.
44. Privalov PL, Potekhin SA. 1986. Scanning microcalorimetry in studying temperature-induced changes in proteins. Methods Enzymol 131:4–51.
45. Rusakov AA, Frisch MJ, Scuseria GE. 2013. Space group symmetry applied to SCF calculations with periodic boundary conditions and Gaussian orbitals. J Chem Phys 139:114110.
46. Scalmani G, Frisch MJ. 2011. Comment on “A smooth, nonsingular, and faithful discretization scheme for polarizable continuum models: The switching/gaussian approach” [J. Chem. Phys. 133, 244111 (2010)]. J Chem Phys 134:117101; author reply 117102.
47. Selvy PE, Lavieri RR, Lindsley CW, Brown HA. 2011. Phospholipase D: Enzymology, functionality, and chemical modulation. Chem Rev 111:6064–6119.
48. Senff-Ribeiro A, Henrique da Silva P, Chaim OM, Gremski LH, Paludo KS, Bertoni da Silveira R, Gremski W, Mangili OC, Veiga SS. 2008. Biotechnological applications of brown spider (Loxosceles genus) venom toxins. Biotechnol Adv 26:210–218.
49. Swanson DL, Vetter RS. 2006. Loxoscelism. Clin Dermatol 24:213–221.
50. Tsujishita H, Hiramatsu Y, Kondo N, Ohmoto H, Kondo H, Kiso M, Hasegawa A. 1997. Selectin-ligand interactions revealed by molecular dynamics simulation in solution. J Med Chem 40:362–369.
51. van Meeteren LA, Frederiks F, Giepmans BN, Pedrosa MF, Billington SJ, Jost BH, Tambourgi DV, Moolenaar WH. 2004. Spider and bacterial sphingomyelinases D target cellular lysophosphatidic acid receptors by hydrolyzing lysophosphatidylcholine. J Biol Chem 279:10833–10836.
52. Vieira DS, Aragao EA, Lourenzoni MR, Ward RJ. 2009. Mapping of Suramin binding sites on the group IIA human secreted phospholipase A2. Bioorg Chem 37:41–45.
53. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA. 2004. Development and testing of a general amber force field. J Comput Chem 25:1157–1174.