Anticoagulant proteins from snake venoms: Structure, function and mechanism

Biochemical Journal

Volumn 397, Issue 3, 2006, Pages 377-387

  Kini, R Manjunatha ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Anticoagulant; C type lectin; Metalloproteinase; Phospholipase A2; Snake venom; Three finger toxin

Indexed keywords

COAGULATION; DRUG DOSAGE; ENZYMES; HEMODYNAMICS; MEDICAL APPLICATIONS; PATIENT MONITORING; PULMONARY DISEASES; TOXIC MATERIALS;

ANTICOAGULANT; C-TYPE LECTIN; METALLOPROTEINASE; PHOSPHOLIPASE A2; SNAKE VENOM; THREE-FINGER TOXIN;

PROTEINS;

AMINO ACID OXIDASE; ANCROD; ANTICOAGULANT PROTEIN; BATROXOBIN; BINDING PROTEIN; BOTHROALTERNIN; BOTHROJARACIN; C TYPE LECTIN RELATED PROTEIN; CARDIOTOXIN; FIX BINDING PROTEIN; FX BINDING PROTEIN; HEMEXTIN A; HEMEXTIN B; LECTIN; METALLOPROTEINASE; PHOSPHOLIPASE A2; PROTEIN CM 1; PROTEIN CM 2; PROTEIN CM 4; SERINE PROTEINASE; SNAKE VENOM; THROMBIN; UNCLASSIFIED DRUG; VENOMBIN A;

BLOOD CLOTTING; CIRCULATION; DRUG INHIBITION; DRUG ISOLATION; DRUG PURIFICATION; ENZYME ACTIVITY; HEMOSTASIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; STRUCTURE ACTIVITY RELATION; THROMBOSIS;

ANIMALS; ANTICOAGULANTS; BLOOD COAGULATION; ENZYMES; PROTEINS; SNAKE VENOMS; STRUCTURE-ACTIVITY RELATIONSHIP; THROMBOSIS; TOXINS, BIOLOGICAL;

EID: 33746885464     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060302     Document Type: Review

References (171)

1. Tu, A. T. (1991) Reptile Venoms and Toxins, Marcel Decker, New York
2. Harvey, A. L. (1991) Snake Toxins, Pergamon Press, New York
3. Pirkle, H. and Markland, Jr, F. S. (1987) Hemostasis and Animal Venoms, Marcel Decker, New York
4. Hutton, R. A. and Warrell, D. A. (1993) Action of snake venom components on the haemostatic system. Blood Rev. 7, 176-189
5. Lu, Q., Clemetson, J. M. and Clemetson, K. J. (2005) Snake venoms and hemostasis. J. Thromb. Haemostasis 3, 1791-1799
6. Markland, F. S. (1998) Snake venoms and the hemostatic system. Toxicon 36, 1749-1800
7. Meier, J. and Stocker, K. (1991) Effects of snake venoms on hemostasis. Crit. Rev. Toxicol. 21, 171-182
8. Braud, S., Bon, C. and Wisner, A. (2000) Snake venom proteins acting on hemostasis. Biochimie 82, 851-859
9. Kini, R. M. (2004) Platelet aggregation and exogenous factors from animal sources. Curr. Drug Targets Cardiovasc. Haematol. Disord. 4, 301-325
10. Scarborough, R. M., Naughton, M. A., Teng, W., Rose, J. W., Phillips, D. R., Nannizzi, L., Artsten, A., Campbell, A. M. and Charo, I. F. (1993) Design of potent and specific integrin antagonists. Peptide antagonists with high specificity for glycoprotein IIb-IIIa. J. Biol. Chem. 268, 1066-1073
11. Phillips, D. R. and Scarborough, R. M. (1997) Clinical pharmacology of eptifibatide. Am. J. Cardiol. 80 (suppl. 4A), 11B-20B
12. Kornalik, F. (1991) The influence of snake venom proteins on blood coagulation. In Snake Toxins (Harvey, A. L., ed.), pp. 323-383, Pergamon Press, New York
13. Kini, R. M., Rao, V. S. and Joseph, J. S. (2002) Procoagulant proteins from snake venoms. Haemostasis 31, 218-224
14. Kini, R. M., Joseph, J. S. and Rao, V. S. (2002) Prothrombin activators from snake venoms. In Perspectives in Molecular Toxinology (Menez, A., ed.), pp. 341-355, John Wiley, Chichester
15. Joseph, J. S. and Kini, R. M. (2004) Snake venom prothrombin activators similar to blood coagulation factor Xa. Curr. Drug Targets Cardiovasc. Haematol. Disord. 4, 397-416
16. 2 Enzymes: Structure, Function and Mechanism (Kini, R. M., ed.), pp. 29-71, John Wiley, Chichester
17. Tan, P. T. J., Khan, M. A. and Brusic, V. (2003) Bioinformatics for venom and toxin sciences. Brief. Bioinform. 4, 53-62
18. 2 enzymes from snake venoms. Toxicon 45, 1147-1161
19. Harris, J. B. (1985) Phospholipases in snake venoms and their effects on nerve and muscle. Pharmacol. Ther. 31, 79-102
20. Rosenberg, P. (1990) Phospholipases. In Handbook of Toxinology (Shier, W. T. and Mebs, D., eds.), pp. 667-677, Marcel Dekker, New York
21. 2 Enzymes: Structure, Function and Mechanism (Kini, R. M., ed.), pp. 1-28, John Wiley, Chichester
22. 2 with anticoagulant activity. II. Inhibition of the phospholipid activity in coagulation. Biochim. Biophys. Acta 429, 839-852
23. 2. Eur. J. Biochem. 112, 25-32
24. 2. In Natural Toxins (Eaker, D. and Walstrom, T., eds.), pp. 131-138, Pergamon Press, Oxford
25. 2. J. Biol. Chem. 255, 3793-3797
26. 2. J. Biol. Chem. 262, 14402-14407
27. 2. Toxicon 27, 613-635
28. 2 enzymes. Toxicon 42, 827-840
29. 2 Enzymes: Structure, Function and Mechanism (Kini, R. M., ed.), pp. 389-412, John Wiley, Chichester
30. 2 isoenzymes from Naja nigricollis venom. Thromb. Res. 55, 481-491
31. Kini, R. M. and Banerjee, Y. (2005) Dissection approach: a simple strategy for identification of the step of action of anticoagulant agents in the blood coagulation cascade. J. Thromb. Haemostas. 3, 170-171
32. 2 from Naja nigricollis venom. Ph.D. Thesis, Virginia Commonwealth University, Richmond, VA, U.S.A.
33. 2 from Naja nigricollis venom inhibits the prothrombinase complex by a novel nonenzymatic mechanism. Biochemistry 29, 7742-7746
34. 2 from Naja nigricollis venom binds to coagulation factor Xa to inhibit the prothrombinase complex. Arch. Biochem. Biophys. 389, 107-113
35. 2 isoenzymes from Naja nigricollis venom. Toxicon 33, 1585-1590
36. 2. Toxicon 19, 705-720
37. 2: effects on enzymatic activity, lethality and some pharmacological properties. Toxicon 21, 209-218
38. 2. A fluorescent study of their binding to phospholipid vesicles. Correlation with their anticoagulant activities. J. Biol. Chem. 255, 7734-7739
39. 2. Toxicon 36, 75-92
40. 2 from Agkistrodon halys Pallas: implications for its association, hemolytic and anticoagulant activities. Toxicon 38, 901-916
41. 2 from common krait (Bungarus caeruleus) at 2.4 Å resolution: identification and characterization of its pharmacological sites. J. Mol. Biol. 307, 1049-1059
42. Walker, F. J., Scandella, D. and Fay, P. J. (1990) Identification of the binding site for activated protein C on the light chain of factors V and VIII. J. Biol. Chem. 265, 1484-1489
43. Nesheim, M. E., Canfield, W. M., Kisiel, W. and Mann, K. G. (1982) Studies of the capacity of factor Xa to protect factor Va from inactivation by activated protein C. J. Biol. Chem. 257, 1443-1447
44. 2 Enzymes: Structure, Function and Mechanism (Kini, R. M., ed.), pp. 353-368, John Wiley, Chichester
45. 2 on cell-free prothrombinase complex. J. Biol. Chem. 269, 26338-26343
46. 2 involves binding to factor Xa. J. Biol. Chem. 273, 23764-23772
47. 2. Eur. J. Biochem. 267, 4960-4969
48. 2 from Vipera ammodytes ammodytes, are critical for binding to factor Xa and for anticoagulant effect. Biochimie 88, 69-76
49. Bjarnason, J. B. and Fox, J. W. (1995) Snake venom metalloproteinases: reprolysins. Methods Enzymol. 248, 345-368
50. Fox, J. W. and Serrano, S. M. T. (2005) Structural considerations of the snake venom metalloproteinases, key members of the M12 reprolysin family of metalloproteinases. Toxicon 45, 969-985
51. Ouyang, C. and Teng, C. M. (1976) Fibrinogenolytic enzymes of Trimeresurus venom. Biochim. Biophys. Acta 420, 298-308
52. Kini, R. M. (2005) Serine proteases affecting blood coagulation and fibrinolysis from snake venoms. Pathophysiol. Haemostasis Thromb. 34, 200-204
53. Fay, W. P. and Owen, W. G. (1989) Platelet plasminogen activator inhibitor: purification and characterization of interaction with plasminogen activators and activated protein C. Biochemistry 28, 5773-5778
54. Moniwa, N. (1996) Relationship of urokinase type plasminogen activator, plasminogen activator inhibitor type 1 and activated protein C in fibrinolysis of human placenta. Pol. J. Pharmacol. 48, 215-220
55. Sakamoto, T., Ogawa, H., Takazoe, K., Yoshimura, M., Shimomura, H., Moriyama, Y., Arai, H. and Okajima, K. (2003) Effect of activated protein C on plasma plasminogen activator inhibitor activity in patients with acute myocardial infarction treated with alteplase: comparison with unfractionated heparin. J. Am. Coll. Cardiol. 42, 1389-1394
56. Klein, J. D. and Walker, F. J. (1986) Purification of a protein C activator from the venom of the southern copperhead snake (Agkistrodon contortrix contortrix). Biochemistry 25, 4175-4179
57. Kisiel, W., Kondo, S., Smith, K. J., McMullen, B. A. and Smith, L. F. (1987) Characterization of a protein C activator from Agkistrodon contortrix contortrix venom. J. Biol. Chem. 262, 12607-12613
58. Bakker, H. M., Tans, G., Yukelson, L. Y., Janssen-Claessen, T. W., Bertina, R. M., Hemker, H. C. and Rosing, J. (1993) Protein C activation by an activator purified from the venom of Agkistrodon halys halys. Blood Coagulation Fibrinolysis 4, 605-614
59. McMullen, B. A., Fujikawa, K. and Kisiel, W. (1989) Primary structure of a protein C activator from Agkistrodon contortrix contortrix venom. Biochemistry 28, 674-679
60. Stocker, K., Fischer, H., Meier, J., Brogli, M. and Svendsen, L. (1986) Protein C activators in snake venoms. Behring Inst. Mitt. 79, 37-47
61. Stocker, K., Fischer, H., Meier, J., Brogli, M. and Svendsen, L. (1987) Characterization of the protein C activator Protac from the venom of the southern copperhead (Agkistrodon contortrix) snake. Toxicon 25, 239-252
62. Kogan, A. E., Bashkov, G. V., Bobruskin, I. D., Romanova, E. P., Makarov, V. A. and Strukova, S. M. (1993) Protein C activator from the venom of Agkistrodon blomhoffi ussuriensis retards thrombus formation in the arterio-venous shunt in rats. Thromb. Res. 70, 385-393
63. Pirkle, H. and Stocker, K. (1991) Thrombin-like enzymes from snake venoms; an inventory. Thromb. Haemostasis 65, 444-450
64. Bell, Jr, W. R. (1997) Defibrinogenating enzymes. Drugs 54 (suppl. 3), 18-30
65. Pirkle, H. and Theodor, I. (1998) Thrombin-like enzymes. In Enzymes from Snake Venom (Bailey, G. S., ed.), pp. 39-69, Alaken Inc., Fort Collins, CO
66. Au, L. C., Lin, S. B., Chou, J. S., Teh, G. W., Chang, K. J. and Shin, C. M. (1993) Molecular cloning and sequence analysis of the cDNA for ancrod, a thrombin-like enzyme from the venom of Calloselasma rhodostoma. Biochem. J. 294, 387-390
67. Aronson, D. L. (1976) Comparison of the actions of thrombin and the thrombin-like venom enzymes ancrod and batroxobin. Thromb. Haemostasis 36, 1-13
68. Yamamoto, C., Tsuru, D., Oda-Ueda, N., Ohno, M., Hattori, S. and Kim, S. T. (2002) Flavoxobin, a serine protease from Trimeresurus flavoviridis (habu snake) venom, independently cleaves Arg726-Ser727 of human C3 and acts as a novel, heterologous C3 convertase. Immunology 107, 111-117
69. Stocker, K. and Barlow, G. H. (1976) The coagulant enzyme from Bothrops atrox venom (batroxobin). Methods Enzymol. 45, 214-223
70. Stocker, K. (1998) Research, diagnostic and medicinal uses of snake venom enzymes. In Enzymes from Snake Venom (Bailey, G. S., ed.), pp. 705-736, Alaken Inc., Fort Collins, CO
71. Siigur, E., Aaspollu, A. and Siigur, J. (2003) Anticoagulant serine fibrinogenases from Vipera lebetina venom: structure-function relationships. Thromb. Haemostasis 89, 826-831
72. Siigur, E., Mahar, A. and Siigur, J. (1991) β-Fibrinogenase from the venom of Vipera lebetina. Toxicon 29, 107-118
73. Mahar, A., Siigur, E. and Siigur, J. (1987) Purification and properties of a proteinase from Vipera lebetina (snake) venom. Biochim. Biophys. Acta 925, 272-281
74. Samuel, M., Subbi, J., Siigur, E. and Siigur, J. (2002) Biochemical characterization of fibrinogenolytic serine proteinases from Vipera lebetina snake venom. Toxicon 40, 51-54
75. Matsui, T., Fujimura, Y. and Titani, K. (2000) Snake venom proteases affecting hemostasis and thrombosis. Biochim. Biophys. Acta 1477, 146-156
76. Serrano, S. M. and Maroun, R. C. (2005) Snake venom serine proteinases: sequence homology vs. substrate specificity, a paradox to be solved. Toxicon 45, 1115-1132
77. 2. Thromb. Haemostasis 48, 277-282
78. Li, Z. Y., Yu, T. F. and Lian, E. C. (1994) Purification and characterization of L-amino acid oxidase from king cobra (Ophiophagus hannah) venom and its effects on human platelet aggregation. Toxicon 32, 1349-1358
79. Ali, S. A., Stoeva, S., Abbasi, A., Alam, J. M., Kayed, R., Faigle, M., Neumeister, B. and Voelter, W. (2000) Isolation, structural, and functional characterization of an apoptosis-inducing L-amino acid oxidase from leafnosed viper (Eristocophis macmahoni) snake venom. Arch. Biochem. Biophys. 384, 216-265
80. Sakurai, Y., Takatsuka, H., Yoshioka, A., Matsui, T., Suzuki, M., Titani, K. and Fujimura, Y. (2001) Inhibition of human platelet aggregation by L-amino acid oxidase purified from Naja naja kaouthia venom. Toxicon 39, 1827-1833
81. Sakurai, Y., Shima, M., Matsumoto, T., Takatsuka, H., Nishiya, K., Kasuda, S., Fujimura, Y. and Yoshioka, A. (2003) Anticoagulant activity of M-LAO, L-amino acid oxidase purified from Agkistrodon halys blomhoffii, through selective inhibition of factor IX. Biochim. Biophys. Acta 1649, 51-57
82. Drickamer, K. (1999) C-type lectin-like domains. Curr. Opin. Struct. Biol. 9, 585-590
83. Morita, T. (2004) C-type lectin-related proteins from snake venoms. Curr. Drug Targets Cardiovasc. Hematol. Disord. 4, 357-373
84. Ogawa, T., Chijiwa, T., Oda-Ueda, N. and Ohno, M. (2005) Molecular diversity and accelerated evolution of C-type lectin-like proteins from snake venom. Toxicon 45, 1-14
85. Takeya, H., Nishida, S., Miyata, T., Kawada, S., Saisaka, Y., Morita, T. and Iwanaga, S. (1992) Coagulation factor X activating enzyme from Russell's viper venom (RVV-X). A novel metalloproteinase with disintegrin (platelet aggregation inhibitor)-like and C-type lectin-like domains. J. Biol. Chem. 267, 14109-14117
86. Gowda, D. C., Jackson, C. M., Hensley, P. and Davidson, E. A. (1994) Factor X-activating glycoprotein of Russell's viper venom. Polypeptide composition and characterization of the carbohydrate moieties. J. Biol. Chem. 269, 10644-10650
87. Yamada, D., Sekiya, F. and Morita, T. (1996) Isolation and characterization of carinactivase, a novel prothrombin activator in Echis carinatus venom with a unique catalytic mechanism. J. Biol. Chem. 271, 5200-5207
88. 2+-dependent prothrombin activator, multactivase, from the venom of Echis multisquamatus. J. Biochem. (Tokyo) 122, 991-997
89. Morita, T. (1998) Proteases which activate factor X. In Snake Venom Enzymes (Bailey, G. S., ed.), pp. 179-208, Alaken Inc., Fort Collins, CO
90. Ouyang, C. and Teng, C. M. (1972) Purification and properties of the anticoagulant principle of Agkistrodon acutus venom. Biochim. Biophys. Acta 278, 155-162
91. Ouyang, C. and Yang, F. Y. (1975) Purification and properties of the anticoagulant principle of Trimeresurus gramineus venom. Biochim. Biophys. Acta 386, 479-492
92. Ouyang, C. and Teng, C. M. (1973) The effect of the purified anticoagulant principle of Agkistrodon acutus venom on blood coagulation. Toxicon 11, 287-292
93. Teng, C. M. and Seegers, W. H. (1981) Agkistrodon acutus snake venom inhibits prothrombinase complex formation. Thromb. Res. 23, 255-263
94. Atoda, H. and Morita, T. (1989) A novel blood coagulation factor IX/factor X-binding protein with anticoagulant activity from the venom of Trimeresurus flavoviridis (Habu snake): isolation and characterization. J. Biochem. (Tokyo) 106, 808-813
95. Atoda, H., Hyuga, M. and Morita, T. (1991) The primary structure of coagulation factor IX/factor X-binding protein isolated from the venom of Trimeresurus flavoviridis. Homology with asialoglycoprotein receptors, proteoglycan core protein, tetranectin, and lymphocyte Fc3 receptor for immunoglobulin E. J. Biol. Chem. 266, 14903-14911
96. Atoda, H. and Morita, T. (1993) Arrangement of the disulfide bridges in a blood coagulation factor IX/factor X-binding protein from the venom of Trimeresurus flavoviridis. J. Biochem. (Tokyo) 113, 159-163
97. Atoda, H., Ishikawa, M., Yoshihara, E., Sekiya, F. and Morita, T. (1995) Blood coagulation factor IX-binding protein from the venom of Trimeresurus flavoviridis: purification and characterization. J. Biochem. (Tokyo) 118, 965-973
98. Atoda, H., Ishikawa, M., Mizuno, H. and Morita, T. (1998) Coagulation factor X-binding protein from Deinagkistrodon acutus venom is a Gla domain-binding protein. Biochemistry 37, 17361-17370
99. Mizuno, H., Fujimoto, Z., Koizumi, M., Kano, H., Atoda, H. and Morita, T. (1997) Structure of coagulation factors IX/X-binding protein, a heterodimer of C-type lectin domains. Nat. Struct. Biol. 4, 438-441
100. Mizuno, H., Fujimoto, Z., Koizumi, M., Kano, H., Atoda, H. and Morita, T. (1999) Crystal structure of coagulation factor IX-binding protein from habu snake venom at 2.6 Å: implication of central loop swapping based on deletion in the linker region. J. Mol. Biol. 289, 103-112
101. Weis, W. I., Kahn, R., Fourme, R., Drickamer, K. and Hendrickson, W. A. (1991) Structure of the calcium-dependent lectin domain from a rat mannose-binding protein determined by MAD phasing. Science 254, 1608-1615
102. Weis, W. I., Drickamer, K. and Hendrickson, W. A. (1992) Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature (London) 360, 127-134
103. Fukuda, K., Mizuno, H., Atoda, H. and Morita, T. (2000) Crystal structure of flavocetin-A, a platelet glycoprotein Ib-binding protein, reveals a novel cyclic tetramer of C-type lectin-like heterodimers. Biochemistry 39, 1915-1923
104. Sen, U., Vasudevan, S., Subbarao, G., McClintock, R. A., Celikel, R., Ruggeri, Z. M. and Varughese, K. I. (2001) Crystal structure of the von Willebrand factor modulator botrocetin. Biochemistry 40, 345-352
105. Hirotsu, S., Mizuno, H., Fukuda, K., Qi, M. C., Matsui, T., Hamako, J., Morita, T. and Titani, K. (2001) Crystal structure of bitiscetin, a von Willebrand factor-dependent platelet aggregation inducer. Biochemistry 40, 13592-13597
106. Batuwangala, T., Leduc, M., Gibbins, J. M., Bon, C. and Jones, E. Y. (2004) Structure of the snake-venom toxin convulxin. Acta Crystallogr. Sect. D: Biol. Crystallogr. 60, 46-53
107. Liu, Y. and Eisenberg, D. (2002) 3D domain swapping: as domains continue to swap. Protein Sci. 11, 1285-1299
108. Mizuno, H., Fujimoto, Z., Atoda, H. and Morita, T. (2001) Crystal structure of an anticoagulant protein in complex with the Gla domain of factor X. Proc. Natl. Acad. Sci. U.S.A. 98, 7230-7234
109. 2+-bound Gla domain of factor IX complexed with binding protein. J. Biol. Chem. 278, 24090-24094
110. Zingali, R. B., Jandrot-Perrus, M., Guillin, M. C. and Bon, C. (1993) Bothrojaracin, a new thrombin inhibitor isolated from Bothrops jararaca venom: characterization and mechanism of thrombin inhibition. Biochemistry 32, 10794-10802
111. Arocas, V., Zingali, R. B., Guillin, M. C., Bon, C. and Jandrot-Perrus, M. (1996) Bothrojaracin: a potent two-site-directed thrombin inhibitor. Biochemistry 35, 9083-9089
112. Castro, H. C., Dutra, D. L., Oliveira-Carvalho, A. L. and Zingali, R. B. (1998) Bothroalternin, a thrombin inhibitor from the venom of Bothrops alternatus. Toxicon 36, 1903-1912
113. Arocas, V., Castro, H. C., Zingali, R. B., Guillin, M. C., Jandrot-Perrus, M., Bon, C. and Wisner, A. (1997) Molecular cloning and expression of bothrojaracin, a potent thrombin inhibitor from snake venom. Eur. J. Biochem. 248, 550-557
114. Monteiro, R. Q., Carlini, C. R., Guimaraes, J. A., Bon, C. and Zingali, R. B. (1997) Distinct bothrojaracin isoforms produced by individual jararaca (Bothrops jararaca) snakes. Toxicon 35, 649-657
115. Monteiro, R. Q., Yamanouye, N., Carlini, C. R., Guimaraes, J. A., Bon, C. and Zingali, R. B. (1998) Variability of bothrojaracin isoforms and other venom principles in individual jararaca (Bothrops jararaca) snakes maintained under seasonally invariant conditions. Toxicon 36, 153-163
116. Monteiro, R. Q., Dutra, D. L., Machado, O. L., Carlini, C. R., Guimaraes, J. A., Bon, C. and Zingali, R. B. (1998) Bothrops jararaca snakes produce several bothrojaracin isoforms following an individual pattern. Comp. Biochem. Physiol. Part B. Biochem. Mol. Biol. 120, 791-798
117. Castro, H. C., Fernandes, M. and Zingali, R. B. (1999) Identification of bothrojaracin-like proteins in snake venoms from Bothrops species and Lachesis muta. Toxicon 37, 1403-1416
118. Arocas, V., Lemaire, C., Bouton, M. C., Bezeaud, A., Bon, C., Guillin, M. C. and Jandrot-Perrus, M. (1998) Inhibition of thrombin-catalyzed factor V activation by bothrojaracin. Thromb. Haemostasis 79, 1157-1161
119. Monteiro, R. Q. and Zingali, R. B. (2000) Inhibition of prothrombin activation by bothrojaracin, a C-type lectin from Bothrops jararaca venom. Arch. Biochem. Biophys. 382, 123-128
120. Monteiro, R. Q. and Zingali, R. B. (2002) Bothrojaracin, a proexosite I ligand, inhibits factor Va-accelerated prothrombin activation. Thromb. Haemostasis 87, 288-293
121. Monteiro, R. Q., Bock, P. E., Bianconi, M. L. and Zingali, R. B. (2001) Characterization of bothrojaracin interaction with human prothrombin. Protein Sci. 10, 1897-1904
122. Monteiro, R. Q., Foguel, D., Castro, H. C. and Zingali, R. B. (2003) Subunit dissociation, unfolding, and inactivation of bothrojaracin, a C-type lectin-like protein from snake venom. Biochemistry 42, 509-515
123. Monteiro, R. Q., Raposo, J. G., Wisner, A., Guimaraes, J. A., Bon, C. and Zingali, R. B. (1999) Allosteric changes of thrombin catalytic site induced by interaction of bothrojaracin with anion-binding exosites I and II. Biochem. Biophys. Res. Commun. 262, 819-822
124. Dufton, M. T. and Hider, R. C. (1988) Structure and pharmacology of elapid cytotoxins. Pharmacol. Ther. 36, 1-40
125. Endo, T. and Tamiya, N. (1991) Structure-function relationships of postsynaptic neurotoxins from snake venoms. In Snake Toxins (Harvey, A. L., ed.), pp. 165-222, Pergamon Press, New York
126. Fry, B. G., Lumsden, N. G., Wüster, W., Wickramaratna, J. C., Hodgson, W. C. and Kini, R. M. (2003) Isolation of a neurotoxin (α-colubritoxin) from a 'non-venomous' colubrid: evidence for early origin of venom in snakes. J. Mol. Evol. 57, 446-452
127. Fry, B. G., Wuster, W., Ramjan, R. S. F., Jackson, T., Martelli, P. and Kini, R. M. (2003) Analysis of Colubroidea snake venoms by liquid chromatography with mass spectrometry: evolutionary and toxinological implications. Rapid Commun. Mass Spectrom. 17, 2047-2062
128. Lumsden, N. G., Fry, B. G., Kini, R. M. and Hodgson, W. C. (2004) In vitro neuromuscular activity of 'colubrid' venoms: clinical and evolutionary implications. Toxicon 43, 819-827
129. Mackessy, S. P. (2002) Biochemistry and pharmacology of colubrid snake venoms. J. Toxicol. Toxin Rev. 21, 43-83
130. Lumsden, N. G., Fry, B. G., Ventura, S., Kini, R. M. and Hodgson, W. C. (2005) Pharmacological characterisation of a neurotoxin from the venom of Boiga dendrophila (Mangrove snake). Toxicon 45, 329-334
131. Fry, B. G., Wüster, W., Kini, R. M., Brusic, V, Khan, A., Venkataraman, D. and Rooney, A. P. (2003) Molecular evolution and phylogeny of elapid snake venom three finger toxins. J. Mol. Evol. 57, 110-129
132. Menez, A. (1998) Functional architectures of animal toxins: a clue to drug design? Toxicon 36, 1557-1572
133. Tsetlin, V. (1999) Snake venom α-neurotoxins and other 'three-finger' proteins, Eur. J. Biochem. 264, 281-286
134. Chang, C. C. (1979) The action of snake venoms on nerve and muscle. Handb. Exp. Pharmacol. 52, 309-376
135. Changeux, J. P. (1990) The TiPS lecture. The nicotinic acetylcholine receptor: an allosteric protein prototype of ligand-gated ion channels. Trends Pharmacol. Sci. 11, 485-492
136. Grant, G. A. and Chiappinelli, V. A. (1985) κ-Bungarotoxin: complete amino acid sequence of a neuronal nicotinic receptor probe. Biochemistry 24, 1532-1537
137. Jerusalinsky, D. and Harvey, A. L. (1994) Toxins from mamba venoms: small proteins with selectivities for different subtypes of muscarinic acetylcholine receptors. Trends Pharmacol. Sci. 15, 424-430
138. Cervenansky, C., Dajas, F., Harvey, A. L. and Karlsson, E. (1991) Fasciculins, anticholinesterase toxins from mamba venoms: biochemistry and pharmacology. In Snake Toxins (Harvey, A. L., ed.), pp. 303-321, Pergamon Press, New York
139. De Weille, J. R., Schweitz, H., Maes, P., Tartar, A. and Lazdunski, M. (1991) Calciseptine, a peptide isolated from black mamba venom, is a specific blocker of the L-type calcium channel. Proc. Natl Acad. Sci. U.S.A. 88, 2437-2440
140. Albrand, J. P., Blackledge, M. J., Pascaud, F., Hollecker, M. and Marion, D. (1995) NMR and restrained molecular dynamics study of the three-dimensional solution structure of toxin FS2, a specific blocker of the L-type calcium channel, isolated from black mamba venom. Biochemistry 34, 5923-5937
141. Bilwes, A., Rees, B., Moras, D., Menez, R. and Menez, A. (1994) X-ray structure at 1.55 Å of toxin γ, a cardiotoxin from Naja nigricollis venom. Crystal packing reveals a model for insertion into membranes. J. Mol. Biol. 239, 122-136
142. McDowell, R. S., Dennis, M. S., Louie, A., Shuster, M., Mulkerrin, M. G. and Lazarus, R. A. (1992) Mambin, a potent glycoprotein IIb-IIIa antagonist and platelet aggregation inhibitor structurally related to the short neurotoxins. Biochemistry 31, 4766-4772
143. Kini, R. M., Stefansson, S. and Evans, H. J. (1987) Non-phospholipase anticoagulants from Naja nigricollis venom. In Progress in Venom and Toxin Research (Gopalakrishnakone, P. and Tan, C. K., eds.), pp. 175-185, National University of Singapore, Singapore
144. Kini, R. M., Haar, N. C. and Evans, H. J. (1988) Non-enzymatic inhibitors of coagulation and platelet aggregation from Naja nigricollis venom are cardiotoxins. Biochem. Biophys. Res. Commun. 150, 1012-1016
145. Banerjee, Y., Mizuguchi, J., Iwanaga, S. and Kini, R. M. (2005) Hemextin AB complex, a unique anticoagulant protein complex from Hemachatus haemacnatus (African Ringhals cobra) venom that inhibits clot initiation and factor VIIa activity. J. Biol. Chem. 280, 42601-42611
146. Kini, R. M. (2002) Molecular molds with multiple missions: functional sites in three-finger toxins. Clin. Exp. Pharmacol. Physiol. 29, 815-822
147. Fleming, T. J., O'hUigin, C. and Malek, T. R. (1993) Characterization of two novel Ly-6 genes. Protein sequence and potential structural similarity to α-bungarotoxin and other neurotoxins. J. Immunol. 150, 5379-5390
148. Ploug, M. and Ellis, V. (1994) Structure-function relationships in the receptor for urokinase-type plasminogen activator. Comparison to other members of the Ly-6 family and snake venom α-neurotoxins. FEBS Lett. 349, 163-168
149. Gumley, T. P., McKenzie, I. F. C. and Sandrin, M. S. (1995) Tissue expression, structure and function of the murine Ly-6 family of molecules. Immunol. Cell Biol. 73, 277-296
150. Miwa, J. M., Ibanez-Tallon, I., Crabtree, G. W., Sanchez, R., Sali, A., Role, L. W. and Heintz, N. (1999) lynx1, an endogenous toxin-like modulator of nicotinic acetylcholine receptors in the mammalian CNS. Neuron 23, 105-114
151. Cordero-Erausquin, M., Marubio, L. M., Klink, R. and Changeux, J. P. (2000) Nicotinic receptor function: new perspectives from knockout mice. Trends Pharmacol. Sci. 21, 211-217
152. Kini, R. M. and Evans, H. J. (1988) Mechanism of platelet effects of cardiotoxins from Naja nigricollis crawshawii (spitting cobra) snake venom. Thromb. Res. 52, 185-195
153. Kini, R. M. and Evans, H. J. (1989) A common cytolytic region in myotoxins, hemolysins, cardiotoxins and antibacterial peptides. Int. J. Pept. Protein Res. 34, 277-286
154. Kini, R. M. and Evans, H. J. (1989) Role of cationic amino acid residues in cytolytic activity. Modifications of lysine residues in the cardiotoxin from Naja nigricollis venom and correlation between cytolytic and antiplatelet activities. Biochemistry 28, 9209-9215
155. Takahashi, H., Iwanaga, S. and Suzuki, T. (1974) Distribution of proteinase inhibitors in snake venoms. Toxicon 12, 193-197
156. Hokama, Y., Iwanaga, S., Tatsuki, T. and Suzuki, T. (1976) Snake venom proteinase inhibitors. III. Isolation of five polypeptide inhibitors from the venoms of Hemachatus haemachatus (Ringhal's corbra) and Naja nivea (Cape cobra) and the complete amino acid sequences of two of them. J. Biochem. (Tokyo) 79, 559-578
157. Strydom, D. J. (1976) Snake venom toxins. Purification and properties of low-molecular-weight polypeptides of Dendroaspis polylepis polylepis (black mamba) venom. Eur. J. Biochem. 69, 169-176
158. Ritonja, A., Turk, V. and Gubensek, F. (1983) Serine proteinase inhibitors from Vipera ammodytes venom. Isolation and kinetic studies. Eur. J. Biochem. 133, 427-432
159. Harvey, A. L. (2001) Twenty years of dendrotoxins. Toxicon 39, 15-26
160. Harvey, A. L. and Robertson, B. (2004) Dendrotoxins: structure-activity relationships and effects on potassium ion channels. Curr. Med. Chem. 11, 3065-3072
161. 2+ channels with a high affinity for L-type channels in cerebellar granule neurons. Proc. Natl. Acad. Sci. U.S.A. 91, 878-882
162. Stotz, S. C., Spaetgens, R. L. and Zamponi, G. W. (2000) Block of voltage-dependent calcium channel by the green mamba toxin calcicludine. J. Membr. Biol. 174, 157-165
163. Arseniev, A. S., Wider, G., Joubert, F. J. and Wuthrich, K. (1982) Assignment of the H nuclear magnetic resonance spectrum of the trypsin inhibitor E from Dendroaspis polylepis polylepis. Two-dimensional nuclear magnetic resonance at 500 MHz. J. Mol. Biol. 159, 323-351
164. 1H nuclear magnetic resonance spectrum of the trypsin inhibitor homologue K from Dendroaspis polylepis polylepis. Two-dimensional nuclear magnetic resonance at 360 and 500 MHz. J. Mol. Biol. 163, 623-646
165. Chen, C., Hsu, C. H., Su, N. Y., Lin, Y. C., Chiou, S. H. and Wu, S. H. (2001) Solution structure of a Kunitz-type chymotrypsin inhibitor isolated from the elapid snake Bungarus fasciatus. J. Biol. Chem. 276, 45079-45087
166. 2+ channel blocker calcicludine. Proteins 34, 520-532
167. Masci, P. P., Whitaker, A. N., Sparrow, L. G., de Jersey, J., Winzor, D. J., Watters, D. J., Lavin, M. F. and Gaffney, P. J. (2000) Textilinins from Pseudonaja textilis textilis. Characterization of two plasmin inhibitors that reduce bleeding in an animal model. Blood Coagulation Fibrinolysis 11, 385-393
168. Flight, S., Johnson, L., Trabi, M., Gaffney, P., Lavin, M., de Jersey, J. and Masci, P. (2006) Pathophysiol. Haemostasis Thromb. 34, 188-193
169. Torres, A. M., Wong, H. Y., Desai, M., Moochhala, S., Kuchel, P. W. and Kini, R. M. (2003) Identification of a novel family of proteins in snake venoms: purification and structural characterization of nawaprin from Naja nigricollis snake venom. J. Biol. Chem. 278, 40097-40104
170. Gustafsson, D., Bylund, R., Antonsson, T., Nilsson, L., Nystrom, J. E., Eriksson, U., Bredberg, U. and Teger-Nilsson, A. C. (2004) A new oral anticoagulant: the 50-year challenge. Nat. Rev. Drug Discov. 3, 649-659
171. 2 in a complex with a transition-state analogue. Science 250, 1560-1563