Biochemical characterization and comparative analysis of two distinct serine proteases from Bothrops pirajai snake venom

Biochimie

Volumn 94, Issue 12, 2012, Pages 2545-2558

  Menaldo, Danilo Luccas ^a   Bernardes, Carolina Petri ^a   Santos Filho, Norival Alves ^a   Moura, Laura De Andrade ^b   Fuly, André Lopes ^b   Arantes, Eliane Candiani ^a   Sampaio, Suely Vilela ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

Author keywords

Bothrops pirajai; Glycoproteins; Isoforms; Serine proteases; Snake venoms; Thrombin like enzymes

Indexed keywords

FIBRIN; FIBRINOGEN; PLASMIN; SERINE PROTEINASE; SNAKE VENOM; THROMBIN;

ADULT; AMINO ACID SEQUENCE; ARTICLE; BIOCHEMISTRY; BOTHROPS PIRAJAI; CONTROLLED STUDY; DENATURATION; DOSE RESPONSE; ENZYME ACTIVITY; GLYCOSYLATION; HUMAN; IN VITRO STUDY; MASS SPECTROMETRY; MOLECULAR WEIGHT; POLYACRYLAMIDE GEL ELECTROPHORESIS; SNAKE; STRUCTURE ACTIVITY RELATION; THROMBOCYTE AGGREGATION;

ADULT; AMINO ACID SEQUENCE; ANIMALS; BIOCATALYSIS; BLOOD COAGULATION; BOTHROPS; CATTLE; DIPEPTIDES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME STABILITY; FEMALE; FIBRINOLYSIS; HUMANS; ISOELECTRIC FOCUSING; ISOENZYMES; MALE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PLATELET AGGREGATION; SEQUENCE HOMOLOGY, AMINO ACID; SERINE PROTEASES; SNAKE VENOMS; SUBSTRATE SPECIFICITY; TEMPERATURE; YOUNG ADULT;

BOTHROPS PIRAJAI; BOVINAE;

EID: 84868207826     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.07.007     Document Type: Article

References (76)

1. F.S. Markland Snake venoms and the hemostatic system Toxicon 36 1998 1749 1800 (Pubitemid 28532757)
2. E.A. Varanda, and M.J.S. Giannini Bioquímica de venenos de serpentes B. Barravieira, Venenos. Aspectos clínicos e terapêuticos dos acidentes por animais peçonhentos 1999 EPUB Rio de Janeiro 205 223
3. D. Mebs Snake venom composition and evolution of Viperidae Kaupia 8 1999 145 148
4. S.P. Mackessy The field of reptile toxinology: snakes, lizards, and their venoms S.P. Mackessy, Handbook of Venoms and Toxins of Reptiles 2009 CRC Press Boca Raton 3 23
5. A.S. Kamiguti, and J.L.C. Cardoso Haemostatic changes caused by the venoms of South American snakes Toxicon 27 1989 955 963 (Pubitemid 19226949)
6. S. Braud, C. Bon, and A. Wisner Snake venom acting on hemostasis Biochimie 82 2000 851 859
7. S.M. Serrano, and R.C. Maroun Snake venom serine proteinases: sequence homology vs. substrate specificity, a paradox to be solved Toxicon 45 2005 1115 1132 (Pubitemid 40732585)
8. A. Amaral New genera and species of snakes Proc. New Engl. Zool. Club. 8 1923 85 105
9. A.J.S. Argolo Bothrops pirajai IUCN 2011, IUCN Red List of Threatened Species. Version 2011.2 2000 http://www.iucnredlist.org/apps/redlist/details/ 39902/0 Downloaded on 23 February 2012
10. N. Marsh, and V. Williams Pratical applications of snake venom toxins in haemostasis Toxicon 45 2005 1171 1181 (Pubitemid 40732589)
11. D.C. Koh, A. Armugam, and K. Jeyaseelan Snake venom components and their applications in biomedicine Cell. Mol. Life Sci. 63 2006 3030 3041 (Pubitemid 46072306)
12. E.E. Gardiner, and R.K. Andrews The cut of the clot(h): snake venom fibrinogenases as therapeutic agents J. Thromb. Haemost. 6 2008 1360 1362 (Pubitemid 352016317)
13. S.P. Mackessy Thrombin-like enzymes in snake venoms R.M. Kini, M.A. McLane, K. Clemetson, F.S. Markland, T. Morita, Toxins and Hemostasis: From Bench to Bedside 2010 Springer-Verlag Heidelberg 519 557
14. W.H. Dascombe, G. Dumanian, C. Hong, B.V. Heil, K. Labadie, B. Hessel, B. Blombäck, and P.C. Johnson Application of thrombin based fibrin glue and non-thrombin based batroxobin glue on intact human blood vessels: evidence for transmural thrombin activity Thromb. Haemost. 78 1997 947 951 (Pubitemid 27365598)
15. L.C. Barros, R.S. Ferreira Jr., S.R. Barraviera, H.O. Stolf, I.A. Thomazini-Santos, M.J. Mendes-Giannini, E. Toscano, and B. Barraviera A new fibrin sealant from Crotalus durissus terrificus venom: applications in medicine J. Toxicol. Environ. Health 12B 2009 553 571
16. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
17. O. Vesterberg Isoelectric focusing of proteins in polyacrylamide gels Biochim. Biophys. Acta 257 1972 11 19
18. E.C. Arantes, W.A. Prado, S.V. Sampaio, and J.R. Giglio A simplified procedure for the fractionation of Tityus serrulatus venom: isolation and partial characterization of TsTX-IV, a new toxin Toxicon 8 1989 907 916 (Pubitemid 19210679)
19. P. Edman, and G. Begg A protein sequenator Eur. J. Biochem. 1 1967 80 91
20. B.C.W. Hummel A modified spectrophotometric determination of chymotrypsin, trypsin and thrombin Can. ft. Biochem. Physiol. 37 1959 1393 1399
21. W. Edgar, and C.R.M. Prentice The proteolytic action of ancrod on human fibrinogen and its polypeptide chains Thromb. Res. 2 1973 85 95
22. V.M. Rodrigues, A.M. Soares, R. Guerra-Sá, V. Rodrigues, M.R.M. Fontes, and J.R. Giglio Structural and functional characterization of neuwiedase, a nonhemorrhagic fibrinogenolytic metalloprotease from Bothrops neuwiedi snake venom Arch. Biochem. Biophys. 381 2000 213 224 (Pubitemid 32260307)
23. D.P. Leitão, A.C. Polizello, and Z. Rothschild Coagulation and fibrinolysis in capybara (Hydrochaeris hydrocaeris), a close relative of the guinea-pig (Cavia porcellus) Comp. Biochem. Physiol. A Mol. Integr. Physiol. 125 2000 113 120 (Pubitemid 30211730)
24. R.D. Theakston, and H.A. Reid Development of simple standard assay procedures for the characterization of snake venom Bull. World Health Organ. 61 1983 949 956 (Pubitemid 14181614)
25. C.R. Carlini, J.A. Guimarães, and J.M. Ribeiro Platelet release reaction and aggregation induced by canatoxin, a convulsant protein: evidence for the involvement of the platelet lipoxygenase pathway Br. J. Pharmacol. 84 1985 551 560 (Pubitemid 15169245)
26. 2 isoenzyme isolated from Lachesis muta snake venom Biochem. Pharmacol. 63 2002 1589 1597 (Pubitemid 34457998)
27. S.M. Serrano, Y. Hagiwara, N. Murayama, S. Higuchi, R. Mentele, C.A. Sampaio, A.C. Camargo, and E. Fink Purification and characterization of a kinin-releasing and fibrinogen-clotting serine proteinase (KN-BJ) from the venom of Bothrops jararaca, and molecular cloning and sequence analysis of its cDNA Eur. J. Biochem. 251 1998 845 853 (Pubitemid 28108981)
28. S.M. Serrano, C.A. Sampaio, R. Mentele, A.C. Camargo, and E. Fink A novel fibrinogen-clotting enzyme, TL-BJ, from the venom of the snake Bothrops jararaca: purification and characterization Thromb. Haemost. 83 2000 438 444 (Pubitemid 30148359)
29. S.M. Serrano, M.F. Matos, F.R. Mandelbaum, and C.A. Sampaio Basic proteinases from Bothrops moojeni (caissaca) venom-I. Isolation and activity of two serine proteinases, MSP 1 and MSP 2, on synthetic substrates and on platelet aggregation Toxicon 31 1993 471 481
30. J.H. Petretski, M. Kanashiro, C.P. Silva, E.W. Alves, and T.L. Kipnis Two related thrombin-like enzymes present in Bothrops atrox venom Braz. J. Med. Biol. Res. 33 2000 1293 1300
31. K. Saguchi, Y. Hagiwara-Saguchi, N. Murayama, H. Ohi, Y. Fujita, A.C. Camargo, S.M. Serrano, and S. Higuchi Molecular cloning of serine proteinases from Bothrops jararaca venom gland Toxicon 46 2005 72 83 (Pubitemid 40825070)
32. M. Ohler, D. Georgieva, J. Seifert, M. von Bergen, R.K. Arni, N. Genov, and C. Betzel The venomics of Bothrops alternatus is a pool of acidic proteins with predominant hemorrhagic and coagulopathic activities J. Proteome Res. 9 2010 2422 2437
33. M. Deshimaru, T. Ogawa, K. Nakashima, I. Nobuhisa, T. Chijiwa, Y. Shimohigashi, Y. Fukumaki, M. Niwa, I. Yamashina, S. Hattori, and M. Ohno Accelerated evolution of crotalinae snake venom gland serine proteases FEBS Lett. 397 1996 83 88 (Pubitemid 26380179)
34. G.L. Zaganelli, M.G.M. Zaganelli, A. Magalhães, C.R. Diniz, and M.E. Lima Purification and characterization of a fibrinogen-clotting enzyme from the venom of jararacuçu (Bothrops jararacussu) Toxicon 34 1996 807 819 (Pubitemid 26242776)
35. R.K. Bortoleto, M.T. Murakami, L. Watanabe, A.M. Soares, and R.K. Arni Purification, characterization and crystallization of Jararacussin-I, a fibrinogen-clotting enzyme isolated from the venom of Bothrops jararacussu Toxicon 40 2002 1307 1312 (Pubitemid 35239901)
36. S.H. Andrião-Escarso, S.V. Sampaio, O.A.B. Cunha, S. Marangoni, B. Oliveira, and J.R. Giglio Isolation and characterization of a new clotting factor from Bothrops jararacussu (jararacuçu) venom Toxicon 35 1997 1043 1052 (Pubitemid 27304191)
37. C.D. Sant'Ana, F.K. Ticli, L.L. Oliveira, J.R. Giglio, C.G.V. Rechia, A.L. Fuly, H.S. Selistre-de-Araújo, J.J. Franco, R.G. Stábeli, A.M. Soares, and S.V. Sampaio BjussuSP-I: a new thrombin-like enzyme isolated from Bothrops jararacussu snake venom Comp. Biochem. Physiol. 151A 2008 443 454
38. L.A. Ponce-Soto, V.L. Bonfim, J.C. Novello, R. Navarro Oviedo, A. Yarlequé Chocas, and S. Marangoni Isolation and characterization of a serine protease, BaIII-4, from Peruvian Bothrops atrox venom Protein J. 26 2007 387 394 (Pubitemid 47351807)
39. F.L. Costa, R.S. Rodrigues, L.F. Izidoro, D.L. Menaldo, A. Hamaguchi, M.I. Homsi-Brandeburgo, A.L. Fuly, S.G. Soares, H.S. Selistre-de-Araújo, B. Barraviera, A.M. Soares, and V.M. Rodrigues Biochemical and functional properties of a thrombin-like enzyme isolated from Bothrops pauloensis snake venom Toxicon 54 2009 725 735
40. F. Oliveira, V.M. Rodrigues, M.H. Borges, A.M. Soares, A. Hamaguchi, J.R. Giglio, and M.I. Homsi-Brandeburgo Purification and partial characterization of a new proteolytic enzyme from the venom of Bothrops moojeni (caissaca) Biochem. Mol. Biol. Int. 47 1999 1069 1077 (Pubitemid 29308745)
41. D.F. Vieira, L. Watanabe, C.D. Sant'Ana, S. Marcussi, S.V. Sampaio, A.M. Soares, and R.K. Arni Purification and characterization of jararassin-I, a thrombin-like enzyme from Bothrops jararaca snake venom Acta Biochim. Biophys. Sin. 36 2004 798 802 (Pubitemid 40395028)
42. S.M. Serrano, R. Mentele, C.A. Sampaio, and E. Fink Purification, characterization, and amino acid sequence of a serine proteinase, PA-BJ, with platelet-aggregating activity from the venom of Bothrops jararaca Biochemistry 34 1995 7186 7193
43. T. Matsui, Y. Fujimura, and K. Titani Snake venom proteases affecting hemostasis and thrombosis Biochim. Biophys. Acta 1477 2000 146 156 (Pubitemid 30119898)
44. N. Murayama, K. Saguchi, R. Mentele, M.T. Assakura, H. Ohi, Y. Fujita, A.C. Camargo, S. Higuchi, and S.M. Serrano The unusual high molecular mass of Bothrops protease A, a trypsin-like serine peptidase from the venom of Bothrops jararaca, is due to its high carbohydrate content Biochim. Biophys. Acta 1652 2003 1 6 (Pubitemid 38234539)
45. F.P. Silva-Junior, H.L. Guedes, L.C. Garvey, A.S. Aguiar, S.C. Bourguignon, E. Di Cera, and S. Giovanni-de-Simone BJ-48, a novel thrombin-like enzyme from the Bothrops jararacussu venom with high selectivity for Arg over Lys in P1: role of N-glycosylation in thermostability and active site accessibility Toxicon 50 2007 18 31 (Pubitemid 46836712)
46. J.A. Valeriano-Zapana, F.S. Segovia-Cruz, J.M. Rojas-Hualpa, D. Martins-de-Souza, L.A. Ponce-Soto, and S. Marangoni Functional and structural characterization of a new serine protease with thrombin-like activity TLBan from Bothrops andianus (Andean lancehead) snake venom Toxicon 59 2012 231 240
47. A.L. Tarentino, C.M. Gómez, and T.H. Plummer Deglycosylation of asparagine-linked glycans by peptide:N-glycosidase F Biochemistry 24 1985 4665 4671 (Pubitemid 15233719)
48. S.G. Soares, and L.L. Oliveira Venom-sweet-venom: N-linked glycosylation in snake venom toxins Protein Pept. Lett. 16 2009 913 919
49. C.D. Sant'Ana, C.P. Bernardes, L.F. Izidoro, M.V. Mazzi, S.G. Soares, A.L. Fuly, R.B. Zingali, A.J. Magro, A.S.K. Braz, M.R.M. Fontes, R.G. Stábeli, S.V. Sampaio, and A.M. Soares Molecular characterization of BjussuSP-I, a new thrombin-like enzyme with procoagulant and kallikrein-like activity isolated from Bothrops jararacussu snake venom Biochimie 90 2008 500 507 (Pubitemid 351246710)
50. Z. Zhu, Z. Liang, T. Zhang, Z. Zhu, W. Xu, M. Teng, and L. Niu Crystal structures and amidolytic activities of two glycosylated snake venom serine proteinases J. Biol. Chem. 280 2005 10524 10529 (Pubitemid 40395912)
51. Y. Komori, and T. Nikai Chemistry and biochemistry of kallikrein-like enzyme from snake venoms J. Toxicol. Toxin Rev. 17 1998 261 277 (Pubitemid 28438337)
52. H.C. Castro, R.B. Zingali, M.G. Albuquerque, M. Pujol-Luz, and C.R. Rodrigues Snake venom thrombin-like enzymes: from reptilase to now Cell. Mol. Life Sci. 61 2004 843 856 (Pubitemid 38651003)
53. S. Swenson, and F.S. Markland Jr. Snake venom fibrin(ogen)olytic enzymes Toxicon 45 2005 1021 1039 (Pubitemid 40732578)
54. A. Mahar, E. Siigur, and J. Siigur Purification and properties of a proteinase from Vipera lebetina (snake) venom Biochim. Biophys. Acta 925 1987 272 281
55. E. Siigur, A. Mahar, and J. Siigur Beta-fibrinogenase from the venom of Vipera lebetina Toxicon 29 1991 107 118
56. J.W. Lee, J.H. Seu, I.K. Rhee, I. Jin, Y. Kawamura, and W. Park Purification and characterization of brevinase, a heterogeneous two-chain fibrinolytic enzyme from the venom of Korean snake, Agkistrodon blomhoffii brevicaudus Biochem. Biophys. Res. Commun. 260 1999 665 670 (Pubitemid 29371108)
57. R. Tatematsu, Y. Komori, and T. Nikai A new thrombin-like enzyme, flavoviridiobin from the venom of Trimeresurus flavoviridis (habu) J. Nat. Toxins 9 2000 327 339
58. A. Magalhães, H.P.B. Magalhães, M. Richardson, S. Gontijo, R.N. Ferreira, A.P. Almeida, and E.F. Sanchez Purification and properties of a coagulant thrombin-like enzyme from the venom of Bothrops leucurus Comp. Biochem. Physiol. 146A 2007 565 575 (Pubitemid 46341902)
59. S.Y. Cho, B.S. Hahn, Y.K. Yang, and Y.S. Kim Purification and characterization of calobin II, a second type of thrombin-like enzyme from Agkistrodon caliginosus (Korean viper) Toxicon 39 2001 499 506
60. S. Liu, M.Z. Sun, C. Sun, B. Zhao, F.T. Greenaway, and Q. Zheng A novel serine protease from the snake venom of Agkistrodon blomhoffii ussurensis Toxicon 52 2008 760 768
61. A. Vilca-Quispe, L.A. Ponce-Soto, F.V. Winck, and S. Marangoni Isolation and characterization of a new serine protease with thrombin-like activity (TLBm) from the venom of the snake Bothrops marajoensis Toxicon 55 2010 745 753
62. A.F. Paes-Leme, B.C. Prezoto, E.T. Yamashiro, L. Bertholim, A.K. Tashima, C.F. Klitzke, A.C. Camargo, and S.M. Serrano Bothrops protease A, a unique highly glycosylated serine proteinase, is a potent, specific fibrinogenolytic agent J. Thromb. Haemost. 6 2008 1363 1372 (Pubitemid 352016318)
63. K. Stocker, and G.H. Barlow The coagulant enzyme from Bothrops atrox venom (batroxobin) Meth. Enzymol. 45 1976 214 223
64. S. Nishida, Y. Fujimura, S. Miura, Y. Ozaki, Y. Usami, M. Suzuki, K. Titani, E. Yoshida, M. Sugimoto, and A. Yoshioka Purification and characterization of bothrombin, a fibrinogen-clotting serine protease from the venom of Bothrops jararaca Biochemistry 33 1994 1843 1849 (Pubitemid 24089714)
65. J.O. Costa, K.C. Fonseca, C.C. Mamede, M.E. Beletti, N.A. Santos-Filho, A.M. Soares, E.C. Arantes, S.N. Hirayama, H.S. Selistre-de-Araújo, F. Fonseca, F. Henrique-Silva, N. Penha-Silva, and F. de Oliveira Bhalternin: functional and structural characterization of a new thrombin-like enzyme from Bothrops alternatus snake venom Toxicon 55 2010 1365 1377
66. R.H. Herzig, O.D. Ratnoff, and J.R. Shainoff Studies on a procoagulant fraction of southern copperhead snake venom: the preferential release of fibrinopeptide B J. Lab. Clin. Med. 76 1970 451 465
67. R. Gao, Y. Zhang, Q.X. Meng, W.H. Lee, D.S. Li, Y.L. Xiong, and W.Y. Wang Characterization of three fibrinogenolytic enzymes from Chinese green tree viper (Trimeresurus stejnegeri) venom Toxicon 36 1998 457 467 (Pubitemid 28238070)
68. A.V. Pérez, A. Rucavado, L. Sanz, J.J. Calvete, and J.M. Gutiérrez Isolation and characterization of a serine proteinase with thrombin-like activity from the venom of the snake Bothrops asper Braz. J. Med. Biol. Res. 41 2008 12 17 (Pubitemid 351425864)
69. Y. Zhang, A. Wisner, Y. Xiong, and C. Bon A novel plasminogen activator from snake venom: purification and characterization, and molecular cloning J. Biol. Chem. 270 1995 10246 10255
70. D. Park, H. Kim, K. Chung, D.S. Kim, and Y. Yun Expression and characterization of a novel plasminogen activator from Agkistrodon halys venom Toxicon 36 1998 1807 1819 (Pubitemid 28532759)
71. E.F. Sanchez, C.I. Santos, A. Magalhaes, C.R. Diniz, S. Figueiredo, J. Gilroy, and M. Richardson Isolation of a proteinase with plasminogen-activating activity from Lachesis muta muta (bushmaster) snake venom Arch. Biochem. Biophys. 378 2000 131 141 (Pubitemid 30350473)
72. M.B. Feinstein, and C. Fraser Human platelet secretion and aggregation induced by calcium ionophores. Inhibition by PGE1 and dibutyryl cyclic AMP J. Gen. Physiol. 66 1975 561 581
73. D. Phillips, I. Charo, L. Parise, and L. Fitzgerald The platelet membrane glycoprotein IIb-IIIa complex Blood 71 1988 831 843
74. S. Niewiarowski, E.P. Kirby, T.M. Brudzynski, and K. Stocker Thrombocytin, a serine protease from Bothrops atrox venom. 2. Interaction with platelets and plasma-clotting factors Biochemistry 18 1979 3570 3577 (Pubitemid 9255095)
75. N. Marrakchi, R. Barbouche, R.B. Zingali, S. Guermazi, H. Karoui, C. Bon, and M. el Ayeb Purification and characterization of two serine-proteases from the venom of Cerastes cerastes, cerastocytin and cerastotin Toxicon 33 1995 1127 1128
76. Y. Jin, Q.M. Lu, J.F. Wei, D.S. Li, W.Y. Wang, and Y.L. Xiong Purification and characterization of jerdofibrase, a serine protease from the venom of Trimeresurus jerdonii snake Toxicon 39 2001 1203 1210 (Pubitemid 32295888)