NPP-BJ, a nucleotide pyrophosphatase/phosphodiesterase from Bothrops jararaca snake venom, inhibits platelet aggregation

Toxicon

Volumn 54, Issue 4, 2009, Pages 499-512

  Santoro, Marcelo L ^a   Vaquero, Tais S ^a   Paes Leme, Adriana F ^a   Serrano, Solange M T ^a  

^a INSTITUTO BUTANTAN   (Brazil)

Author keywords

5 Nucleotidase; ADPase; ATPase; DNase; Nucleotidase; Phosphodiesterase; Platelet aggregation

Indexed keywords

ADENOSINE DIPHOSPHATE; DITHIOTHREITOL; EDETIC ACID; NUCLEOTIDE PYROPHOSPHATASE PHOSPHODIESTERASE BJ; PHOSPHODIESTERASE; SNAKE VENOM; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BOTHROPS JARARACA; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; LD 50; MALE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POISONOUS SNAKE; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; SEQUENCE HOMOLOGY; THROMBOCYTE AGGREGATION INHIBITION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; BOTHROPS; CHROMATOGRAPHY, GEL; CROTALID VENOMS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PHOSPHORIC DIESTER HYDROLASES; PLATELET AGGREGATION; PLATELET AGGREGATION INHIBITORS; PYROPHOSPHATASES; RABBITS; SEQUENCE ALIGNMENT;

BOTHROPS JARARACA; MAMMALIA;

EID: 67650253837     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2009.05.016     Document Type: Article

References (66)

1. Aird S.D. Ophidian envenomation strategies and the role of purines. Toxicon 40 (2002) 335-393
2. Andrews P. Estimation of the molecular weights of proteins by Sephadex gel-filtration. Biochem. J. 91 (1964) 222-233
3. Baykov A.A., Evtushenko O.A., and Avaeva S.M. A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Anal. Biochem 171 (1988) 266-270
4. Belayev L., Khoutorova L., Deisher T.A., Belayev A., Busto R., Zhang Y., Zhao W., and Ginsberg M.D. Neuroprotective effect of SolCD39, a novel platelet aggregation inhibitor, on transient middle cerebral artery occlusion in rats. Stroke 34 (2003) 758-763
5. Björk W. Purification of phosphodiesterase from Bothrops atrox venom, with special consideration of the elimination of monophosphatases. J. Biol. Chem. 238 (1963) 2487-2490
6. Blum H., Beier H., and Gross H.J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8 (1987) 93-99
7. Bollen M., Gijsbers R., Ceulemans H., Stalmans W., and Stefan C. Nucleotide pyrophosphatases/phosphodiesterases on the move. Crit. Rev. Biochem. Mol. Biol. 35 (2000) 393-432
8. Boman H.G. On the specificity of the snake venom phosphodiesterase. Ann.. N.Y. Acad. Sci 81 (1959) 800-803
9. Buergler J.M., Maliszewski C.R., Broekman M.J., Kaluza G.L., Schulz D.G., Marcus A.J., Raizner A.E., Kleiman N.S., and Ali N.M. Effects of SolCD39, a novel inhibitor of platelet aggregation, on platelet deposition and aggregation after PTCA in a porcine model. J. Thromb. Thrombolysis 19 (2005) 115-122
10. de Roodt A.R., Litwin S., and Angel S.O. Hydrolysis of DNA by 17 snake venoms. Comp. Biochem. Physiol. C Toxicol. Pharmacol 135 (2003) 469-479
11. de Roodt A.R., Litwin S., and Vidal J.C. Hemorrhagic activity of Bothrops venoms determined by two different methods and relationship with proteolytic activity on gelatin and lethality. Toxicon 41 (2003) 949-958
12. Dolapchiev L.B., Vassileva R.A., and Koumanov K.S. Venom exonuclease. II. Amino acid composition and carbohydrate, metal ion and lipid content in the Crotalus adamanteus venom exonuclease. Biochim. Biophys. Acta 622 (1980) 331-336
13. Enjyoji K., Sevigny J., Lin Y., Frenette P.S., Christie P.D., Esch II J.S., Imai M., Edelberg J.M., Rayburn H., Lech M., Beeler D.L., Csizmadia E., Wagner D.D., Robson S.C., and Rosenberg R.D. Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nat. Med 5 (1999) 1010-1017
14. Faudry E., Lozzi S.P., Santana J.M., D'Souza-Ault M., Kieffer S., Felix C.R., Ricart C.A., Sousa M.V., Vernet T., and Teixeira A.R. Triatoma infestans apyrases belong to the 5′-nucleotidase family. J. Biol. Chem. 279 (2004) 19607-19613
15. Frischauf A.M., and Eckstein F. Purification of a phosphodiesterase from Bothrops atrox venom by affinity chromatography. Eur. J. Biochem 32 (1973) 479-485
16. 2A adenosine receptors in human peripheral blood cells. Br. J. Pharmacol 129 (2000) 2-11
17. Gijsbers R., Ceulemans H., and Bollen M. Functional characterization of the non-catalytic ectodomains of the nucleotide pyrophosphatase/phosphodiesterase NPP1. Biochem. J. 371 (2003) 321-330
18. Goding J.W., Grobben B., and Slegers H. Physiological and pathophysiological functions of the ecto-nucleotide pyrophosphatase/phosphodiesterase family. Biochim. Biophys. Acta 1638 (2003) 1-19
19. Goetz U., Da Prada M., and Pletscher A. Adenine-, guanine- and uridine-5′-phosphonucleotides in blood platelets and storage organelles of various species. J. Pharmacol. Exp. Ther 178 (1971) 210-215
20. Halim H.Y., Shaban E.A., Hagag M.M., Daoud E.W., and el-Asmar M.F. Purification and characterization of phosphodiesterase (exonuclease) from Cerastes cerastes (Egyptian sand viper) venom. Toxicon 25 (1987) 1199-1207
21. Hanna S.L., Sherman N.E., Kinter M.T., and Goldberg J.B. Comparison of proteins expressed by Pseudomonas aeruginosa strains representing initial and chronic isolates from a cystic fibrosis patient: an analysis by 2-D gel electrophoresis and capillary column liquid chromatography-tandem mass spectrometry. Microbiology 146 (2000) 2495-2508
22. Haslam R., and Cusak N. Blood platelet receptors for ADP and for adenosine. In: Burnstock G. (Ed). Purinergic Receptors (1981), Chapman and Hall, London 221-285
23. Ho N.W., and Gilham P.T. The analysis of polydeoxyribonucleotides by digestion with phosphatase and phosphodiesterases. Biochim. Biophys. Acta 308 (1973) 53-58
24. Holley R.W. The nucleotide sequence of a nucleic acid. Sci. Am. 214 (1966) 30-39
25. Kelly S.J., Dardinger D.E., and Butler L.G. Hydrolysis of phosphonate esters catalyzed by 5′-nucleotide phosphodiesterase. Biochemistry 14 (1975) 4983-4988
26. Kinlough-Rathbone R.L., Packham M.A., Reimers H.J., Cazenave J.P., and Mustard J.F. Mechanisms of platelet shape change, aggregation, and release induced by collagen, thrombin, or A23,187. J. Lab. Clin. Med 90 (1977) 707-719
27. Koszalka P., Ozuyaman B., Huo Y., Zernecke A., Flögel U., Braun N., Buchheiser A., Decking U.K., Smith M.L., Sévigny J., Gear A., Weber A.A., Molojavyi A., Ding Z., Weber C., Ley K., Zimmermann H., Gödecke A., and Schrader J. Targeted disruption of cd73/ecto-5′-nucleotidase alters thromboregulation and augments vascular inflammatory response. Circ. Res. 95 (2004) 814-821
28. Kunapuli S.P., Dorsam R.T., Kim S., and Quinton T.M. Platelet purinergic receptors. Curr. Opin. Pharmacol 3 (2003) 175-180
29. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
30. Lira M.S., Furtado M.F., Martins L.M., Lopes-Ferreira M., Santoro M.L., and Barbaro K.C. Enzymatic and immunochemical characterization of Bothrops insularis venom and its neutralization by polyspecific Bothrops antivenom. Toxicon 49 (2007) 982-994
31. Mackessy S.P. Phosphodiesterases, ribonucleases and deoxyribonucleases. In: Bailey G.S. (Ed). Enzymes from Snake Venom (1998), Alaken, Fort Collins 361-404
32. McKinney M.M., and Parkinson A. A simple, non-chromatographic procedure to purify immunoglobulins from serum and ascites fluid. J. Immunol. Meth. 96 (1987) 271-278
33. Mori N., Nikai T., and Sugihara H. Phosphodiesterase from the venom of Crotalus ruber ruber. Int. J. Biochem 19 (1987) 115-119
34. Ogawa Y., Kanai-Azuma M., Akimoto Y., Kawakami H., and Yanoshita R. Exosome-like vesicles in Gloydius blomhoffii blomhoffii venom. Toxicon 51 (2008) 984-993
35. Oka J., Ueda K., and Hayaishi O. Snake venom phosphodiesterase: simple purification with blue sepharose and its application to poly(ADP-ribose) study. Biochem. Biophys. Res. Commun 80 (1978) 841-848
36. Ouyang C., and Huang T.F. Platelet aggregation inhibitors from Agkistrodon acutus snake venom. Toxicon 24 (1986) 1099-1106
37. Packham M.A., Guccione M.A., Perry D.W., Kinlough-Rathbone R.L., and Mustard J.F. AMP inhibition of reactions of ADP with washed platelets from humans and rabbits. Am J Physiol 223 (1972) 419-424
38. Packham M.A., Guccione M.A., Perry D.W., and Mustard J.F. Interactions of nucleoside di- and triphosphates with rabbit platelets. Am. J. Physiol 227 (1974) 1143-1148
39. 14C-serotonin during initial platelet changes induced by thrombin, collagen, or A23187. Blood 50 (1977) 915-926
40. 2+ in the suspending medium on the responses of human and rabbit platelets to aggregating agents. Thromb. Haemost 62 (1989) 968-976
41. Pahari S., Mackessy S.P., and Kini R.M. The venom gland transcriptome of the Desert Massasauga rattlesnake (Sistrurus catenatus edwardsii): towards an understanding of venom composition among advanced snakes (Superfamily Colubroidea). BMC Mol. Biol. 8 (2007) 115
42. Philipps G.R. Purification and characterization of phosphodiesterase I from Bothrops atrox. Biochim. Biophys. Acta 432 (1976) 237-244
43. Pinsky D.J., Broekman M.J., Peschon J.J., Stocking K.L., Fujita T., Ramasamy R., Connolly Jr. E.S., Huang J., Kiss S., Zhang Y., Choudhri T.F., McTaggart R.A., Liao H., Drosopoulos J.H., Price V.L., Marcus A.J., and Maliszewski C.R. Elucidation of the thromboregulatory role of CD39/ectoapyrase in the ischemic brain. J. Clin. Invest 109 (2002) 1031-1040
44. Ralevic V., and Burnstock G. Receptors for purines and pyrimidines. Pharmacol. Rev. 50 (1998) 413-492
45. Redinbaugh M.G., and Turley R.B. Adaptation of the bicinchoninic acid protein assay for use with microtiter plates and sucrose gradient fractions. Anal. Biochem 153 (1986) 267-271
46. Russell F.E., Buess F.W., and Woo M.Y. Zootoxicological properties of venom phosphodiesterase. Toxicon 1 (1963) 99-108
47. Sales P.B., and Santoro M.L. Nucleotidase and DNase activities in Brazilian snake venoms. Comp. Biochem. Physiol. C Toxicol. Pharmacol 147 (2008) 85-95
48. Sano-Martins, I.S., Santoro, M.L., 2003. Distúrbios hemostáticos em envenenamentos por animais peçonhentos no Brasil. In: Cardoso, J.L.C., França, F.O.S., Fan, H.W., Málaque, C.M.S., Haddad Jr., V. (Eds.), Animais peçonhentos no Brasil, Sarvier, São Paulo, pp. 289-309.
49. Sano-Martins I.S., Santoro M.L., Castro S.C.B., Fan H.W., Cardoso J.L.C., and Theakston R.D.G. Platelet aggregation in patients bitten by the Brazilian snake Bothrops jararaca. Thromb. Res. 87 (1997) 183-195
50. Santoro M.L., and Sano-Martins I.S. Platelet dysfunction during Bothrops jararaca snake envenomation in rabbits. Thromb. Haemost 92 (2004) 369-383
51. Santoro M.L., Sousa-e-Silva M.C., Gonçalves L.R., Almeida-Santos S.M., Cardoso D.F., Laporta-Ferreira I.L., Saiki M., Peres C.A., and Sano-Martins I.S. Comparison of the biological activities in venoms from three subspecies of the South American rattlesnake (Crotalus durissus terrificus, C. durissus cascavella and C. durissus collilineatus). Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol 122 (1999) 61-73
52. Santoro M.L., Sano-Martins I.S., Fan H.W., Cardoso J.L.C., Theakston R.D.G., Warrell D.A., and Biasg. Haematological evaluation of patients bitten by the jararaca, Bothrops jararaca, in Brazil. Toxicon 51 (2008) 1440-1448
53. Soslau G., and Youngprapakorn D. A possible dual physiological role of extracellular ATP in the modulation of platelet aggregation. Biochim. Biophys. Acta 1355 (1997) 131-140
54. Stefan C., Jansen S., and Bollen M. NPP-type ectophosphodiesterases: unity in diversity. Trends Biochem. Sci. 30 (2005) 542-550
55. Stefan C., Jansen S., and Bollen M. Modulation of purinergic signaling by NPP-type ectophosphodiesterases. Purinergic Signal 2 (2006) 361-370
56. Stoynov S.S., Bakalova A.T., Dimov S.I., Mitkova A.V., and Dolapchiev L.B. Single-strand-specific DNase activity is an inherent property of the 140-kDa protein of the snake venom exonuclease. FEBS Lett. 409 (1997) 151-154
57. Sugihara H., Nikai T., Naruse M., Kishida M., and Mori N. Purification and characterization of phosphodiesterase from the venom of Trimeresurus mucrosquamatus. Int. J. Biochem 18 (1986) 203-207
58. Sulkowski E., Björk W., and Laskowski M. A specific and nonspecific alkaline monophosphatase in the venom of Bothrops atrox and their occurrence in the purified venom phosphodiesterase. J. Biol. Chem. 238 (1963) 2477-2490
59. Suwansrinon K., Khow O., Mitmoonpitak C., Daviratanasilpa S., Chaiyabutr N., and Sitprija V. Effects of Russell's viper venom fractions on systemic and renal hemodynamics. Toxicon 49 (2007) 82-88
60. Takatsuka H., Sakurai Y., Yoshioka A., Kokubo T., Usami Y., Suzuki M., Matsui T., Titani K., Yagi H., Matsumoto M., and Fujimura Y. Molecular characterization of L-amino acid oxidase from Agkistrodon halys blomhoffii with special reference to platelet aggregation. Biochim. Biophys. Acta 1544 (2001) 267-277
61. Tan N.H., and Ponnudurai G. A comparative study of the biological properties of some venoms of snakes of the genus Bothrops (American Lance-Headed Viper). Comp. Biochem. Physiol 100B (1991) 361-365
62. Teixeira-Ferreira A., and Alves E.W. Characterization of a novel ADPase in Bothrops jararaca snake venom involved in nucleotide hydrolysis. Protein Pept. Lett 14 (2007) 395-495
63. Valério A.A., Corradini A.C., Panunto P.C., Mello S.M., and Hyslop S. Purification and characterization of a phosphodiesterase from Bothrops alternatus snake venom. J. Protein Chem. 21 (2002) 495-503
64. Vollmayer P., Clair T., Goding J.W., Sano K., Servos J., and Zimmermann H. Hydrolysis of diadenosine polyphosphates by nucleotide pyrophosphatases/phosphodiesterases. Eur. J. Biochem 270 (2003) 2971-2978
65. Williams E.J., Sung S.C., and Laskowski Sr. M. Action of venom phosphodiesterase on deoxyribonucleic acid. J. Biol. Chem. 236 (1961) 1130-1134
66. Yegutkin G.G. Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signaling cascade. Biochim. Biophys. Acta 1783 (2008) 673-694