Two parallel prothrombin activator systems in Australian rough-scaled snake, Tropidechis carinatus

Md. Abu Reza; Sanjay Swarup; Manjunatha R. Kini

doi:10.1160/TH04-07-0435

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2005; 93(01): 40-47
DOI: 10.1160/TH04-07-0435

Blood Coagulation, Fibrinolysis and Cellular Haemostasis

Schattauer GmbH

Two parallel prothrombin activator systems in Australian rough-scaled snake, Tropidechis carinatus

Structural comparison of venom prothrombin activator with blood coagulation factor X

Authors

Md. Abu Reza

¹Protein Science Laboratory, Department of Biological Sciences, Faculty of Science, National University of Singapore, Singapore
Sanjay Swarup

¹Protein Science Laboratory, Department of Biological Sciences, Faculty of Science, National University of Singapore, Singapore
Manjunatha R. Kini

¹Protein Science Laboratory, Department of Biological Sciences, Faculty of Science, National University of Singapore, Singapore

²Department of Biochemistry and Molecular Biophysics, Medical College of Virginia, Virginia Commonwealth University, Richmond, Virginia USA

Abstract

Full Text

PDF Download

Keywords

Prothrombin activation - factor X - haemostasis - snake venom

References

References
1 Suttie JW, Jackson CM. Prothrombin structure, activation, and biosynthesis. Physiol Rev 1977; 57: 1-70.
2 Mann KG. The assembly of blood clotting complexes on membranes. Trends Biochem Sci 1987; 12: 229-33.
3 Rosing J, Tans G, Govers-Riemslag JW. et al The role of phospholipids and factor Va in the prothrombinase complex. J Biol Chem 1980; 255: 274-83.
4 Mann KG, Krishnaswamy S, Lawson JH. Surfacedependent hemostasis. Semin Hematol 1992; 29: 213-26.
5 van Rijn JL, Govers-Riemslag JW, Zwaal RF. et al Kinetic studies of prothrombin activation: effect of factor Va and phospholipids on the formation of the enzyme-substrate complex. Biochemistry 1984; 23: 4557-64.
6 Markland Jr FS. Snake venoms. Drugs 1997; 54 (Suppl. 03) 1-10.
7 Hutton RA, Warrell DA. Action of snake venom components on the haemostatic system. Blood Rev 1993; 7: 176-89.
8 Manjunatha KR, Morita T, Rosing J. Classification and nomenclature of prothrombin activators isolated from snake venoms. Thromb Haemost 2001; 86: 710-11.
9 Joseph JS, Chung MC, Jeyaseelan K. et al Amino acid sequence of trocarin, a prothrombin activator from Tropidechis carinatus venom: its structural similarity to coagulation factor Xa. Blood 1999; 94: 621-31.
10 Joseph JS, Kini RM. Snake venom prothrombin activators homologous to blood coagulation factor Xa. Haemostasis 2001; 31: 234-40.
11 Rao VS, Joseph JS, Kini RM. Group D prothrombin activators from snake venom are structural homologues of mammalian blood coagulation factor Xa. Biochem J 2003; 369 Pt (03) 635-42.
12 Rosing J, Tans G. Structural and functional properties of snake venom prothrombin activators. Toxicon 1992; 30: 1515-27.
13 Tans G, Govers-Riemslag JW, van Rijn JL. et al Purification and properties of a prothrombin activator from the venom of Notechis scutatus scutatus . J Biol Chem 1985; 260: 9366-72.
14 Archer RK. The Haemostatic Mechanism In Man And Other Animals. In Macfarlane RG. editor Blood coagulation in non-human vertebrates. Academic Press; 1970. 121 32.
15 Bahnak BR, Howk R, Morrissey JH. et al Steady state levels of factor X mRNA in liver and Hep G2 cells. Blood 1987; 69: 224-30.
16 Miao CH, Leytus SP, Chung DW. et al Liver-specific expression of the gene coding for human factor X, a blood coagulation factor. J Biol Chem 1992; 267: 7395-01.
17 Rotenberg D, Bamberger ES, Kochva E. Studies on ribonucleic acid synthesis in the venom glands of Vipera palaestinae (Ophidia, Reptilia). Biochem J 1971; 121: 609-12.
18 Paine MJ, Desmond HP, Theakston RD. et al Gene expression in Echis carinatus (carpet viper) venom glands following milking. Toxicon 1992; 30: 379-86.
19 von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 1986; 14: 4683-90.
20 Ulrich MM, Furie B, Jacobs MR. et al Vitamin K-dependent carboxylation. A synthetic peptide based upon the gamma-carboxylation recognition site sequence of the prothrombin propeptide is an active substrate for the carboxylase in vitro. J Biol Chem 1988; 263: 9697-02.
21 Bristol JA, Furie BC, Furie B. Propeptide processing during factor IX biosynthesis. Effect of point mutations adjacent to the propeptide cleavage site. J Biol Chem 1993; 268: 7577-84.
22 Wasley LC, Rehemtulla A, Bristol JA. et al PACE/ furin can process the vitamin K-dependent pro-factor IX precursor within the secretory pathway. J Biol Chem 1993; 268: 8458-65.
23 Fung MR, Campbell RM, MacGillivray RT. Blood coagulation factor X mRNA encodes a single polypeptide chain containing a prepro leader sequence. Nucleic Acids Res 1984; 12: 4481-92.
24 Lawson JH, Mann KG. Cooperative activation of human factor IX by the human extrinsic pathway of blood coagulation. J Biol Chem 1991; 266: 11317-27.
25 Wesselschmidt R, Likert K, Huang Z. et al Structural requirements for tissue factor pathway inhibitor interactions with factor Xa and heparin. Blood Coagul Fibrinolysis 1993; 4: 661-69.
26 Ahmad SS, Rawala-Sheikh R, Walsh PN. Components and assembly of the factor X activating complex. Semin Thromb Hemost 1992; 18: 311-23.
27 Rao VS, Swarup S, Kini RM. The catalytic subunit of pseutarin C, a group C prothrombin activator from the venom of Pseudonaja textilis, is structurally similar to mammalian blood coagulation factor Xa. Thromb Haemost 2004; 92: 509-21.
28 Jagadeeswaran P, Sheehan JP. Analysis of blood coagulation in the zebrafish. Blood Cells Mol Dis 1999; 25: 239-49.
29 Padmanabhan K, Padmanabhan KP, Tulinsky A. et al Structure of human des(1–45) factor Xa at 2.2 A resolution. J Mol Biol 1993; 232: 947-66.
30 Mizuno H, Fujimoto Z, Atoda H. et al Crystal structure of an anticoagulant protein in complex with the Gla domain of factor X. Proc Natl Acad Sci U S A 2001; 98: 7230-34.
31 Nelsestuen GL, Broderius M, Martin G. Role of gamma-carboxyglutamic acid. Cation specificity of prothrombin and factor X-phospholipid binding. J Biol Chem 1976; 251 (22) 6886-93.
32 Nelsestuen GL, Zytkovicz TH, Howard JB. The mode of action of vitamin K. Identification of gammacarboxyglutamic acid as a component of prothrombin. J Biol Chem 1974; 249: 6347-50.
33 Prendergast FG, Mann KG. Differentiation of metal ion-induced transitions of prothrombin fragment 1. J Biol Chem 1977; 252: 840-50.
34 Borowski M, Furie BC, Bauminger S. et al Prothrombin requires two sequential metal-dependent conformational transitions to bind phospholipid. Conformation- specific antibodies directed against the phospholipid-binding site on prothrombin. J Biol Chem 1986; 261: 14969-75.
35 Soriano-Garcia M, Padmanabhan K, de Vos AM. et al The Ca2+ ion and membrane binding structure of the Gla domain of Ca-prothrombin fragment 1. Biochemistry 1992; 31: 2554-66.
36 Furie B, Furie BC. Molecular basis of vitamin K-dependent gamma-carboxylation. Blood 1990; 75: 1753-62.
37 Drakenberg T, Fernlund P, Roepstorff P. et al beta- Hydroxyaspartic acid in vitamin K-dependent protein C. Proc Natl Acad Sci U S A 1983; 80: 1802-06.
38 Stenflo J, Lundwall A, Dahlback B. beta-Hydroxyasparagine in domains homologous to the epidermal growth factor precursor in vitamin K-dependent protein S. Proc Natl Acad Sci U S A 1987; 84: 368-72.
39 McMullen BA, Fujikawa K, Kisiel W. et al Complete amino acid sequence of the light chain of human blood coagulation factor X: evidence for identification of residue 63 as beta-hydroxyaspartic acid. Biochemistry 1983; 22: 2875-84.
40 Fujikawa K, Titani K, Davie EW. Activation of bovine factor X (Stuart factor): conversion of factor Xaalpha to factor Xabeta. Proc Natl Acad Sci U S A 1975; 72: 3359-63.
41 Walsh MT, Watzlawick H, Putnam FW. et al Effect of the carbohydrate moiety on the secondary structure of beta 2-glycoprotein. I. Implications for the biosynthesis and folding of glycoproteins. Biochemistry 1990; 29: 6250-57.
42 Rudd PM, Joao HC, Coghill E. et al Glycoforms modify the dynamic stability and functional activity of an enzyme. Biochemistry 1994; 33: 17-22.
43 Kobata A. Structures and functions of the sugar chains of glycoproteins. Eur J Biochem 1992; 209: 483-01.
44 Wang C, Eufemi M, Turano C. et al Influence of the carbohydrate moiety on the stability of glycoproteins. Biochemistry 1996; 35: 7299-307.
45 Inoue K, Morita T. Identification of O-linked oligosaccharide chains in the activation peptides of blood coagulation factor X. The role of the carbohydrate moieties in the activation of factor X. Eur J Biochem 1993; 218: 153-63.
46 Sinha U, Wolf DL. Carbohydrate residues modulate the activation of coagulation factor X. J Biol Chem 1993; 268: 3048-51.
47 Joseph JS, Valiyaveettil M, Gowda DC. et al Occurrence of O-linked Xyl-GlcNAc and Xyl-Glc disaccharides in trocarin, a factor Xa homolog from snake venom. J Thromb Haemost 2003; 1: 545-50.
48 Speijer H, Govers-Riemslag JW, Zwaal RF. et al Prothrombin activation by an activator from the venom of Oxyuranus scutellatus (Taipan snake). J Biol Chem 1986; 261: 13258-67.
49 Hasson SS, Theakston RD, Harrison RA. Cloning of a prothrombin activator-like metalloproteinase from the West African saw-scaled viper, Echis ocellatus . Toxicon 2003; 42: 629-34.
50 Gao R, Manjunatha KR, Gopalakrishnakone P. A novel prothrombin activator from the venom of Micropechis ikaheka: isolation and characterization. Arch Biochem Biophys 2002; 408: 87-92.
51 Silva MB, Schattner M, Ramos CR. et al A prothrombin activator from Bothrops erythromelas (jararaca- da-seca) snake venom:characterization and molecular cloning. Biochem J 2003; 369: 129-39.
52 Davidson CJ, Tuddenham EG, McVey JH. 450 million years of hemostasis. J Thromb Haemost 2003; 1: 1487-94.
53 Jiang Y, Doolittle RF. The evolution of vertebrate blood coagulation as viewed from a comparison of puffer fish and sea squirt genomes. Proc Natl Acad Sci U S A 2003; 100: 7527-32.
54 Doolittle RF, Feng DF. Reconstructing the evolution of vertebrate blood coagulation from a consideration of the amino acid sequences of clotting proteins. Cold Spring Harb Symp Quant Biol 1987; 52: 869-74.
55 Hackett E, Hann C. Slow clotting of reptile bloods. J Comp Pathol 1967; 77: 175-80.
56 Rowley AF, Hill DJ, Ray CE. et al Haemostasis in fish--an evolutionary perspective. Thromb Haemost 1997; 77: 227-33.
57 Frost CL, Naude RJ, Oelofsen W. et al Comparative blood coagulation studies in the ostrich. Immunopharmacology 1999; 45: 75-81.
58 Joseph JS, Chung MC, Mirtschin PJ. et al Effect of snake venom procoagulants on snake plasma: implications for the coagulation cascade of snakes. Toxicon 2002; 40: 175-83.
59 Racchi M, Watzke HH, High KA. et al Human coagulation factor X deficiency caused by a mutant signal peptide that blocks cleavage by signal peptidase but not targeting and translocation to the endoplasmic reticulum. J Biol Chem 1993; 268: 5735-40.