Volume 28, Issue 2 (July 2021)
J Birjand Univ Med Sci. 2021, 28(2): 88-105 |
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Babaie M. Snake venom proteins and coagulopathy caused by snakebite. J Birjand Univ Med Sci. 2021; 28 (2) :88-105
URL: http://journal.bums.ac.ir/article-1-2837-en.html
URL: http://journal.bums.ac.ir/article-1-2837-en.html
Razi Vaccine and Serum Research Institute, Agricultural Research Education and Extension Organization, Karaj, Iran , m.babaie47@yahoo.com
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ABSTRACT
Snakebite affects around 3 or 4 million humans annually leading to more than 100,000 deaths. Coagulopathy is one of the significant causes of both morbidity and mortality in these patients. Accordingly, it is of utmost importance to diagnose and treat coagulation disorder due to bites; in addition, it is accompanied by various clinical aspects, such as pre-coagulation, fibrinogen coagulation time, fibrinolytic, platelet activation, anticoagulant, thrombotic, and bleeding. The main cause of coagulopathy caused by snakebite is the presence of compounds found in snake venom. These compounds are mostly proteins with enzymatic activity and high stability; moreover, they rapidly react with factors in the blood circulatory system and disrupt their correct functioning. Regarding the snake venom compounds, especially their proteins, it should be mentioned that different snakes' venoms have different proteins, which can have a role in coagulation or anticoagulation depending on its amount. The coagulant proteins are subclassified as clotting factor activators and thrombin-like enzymes. The anticoagulant proteins can prevent blood clotting leading to coagulopathy and include phospholipases A2, fibrinolytic, protein C activator, and L-amino acid oxidase (enzymatic anticoagulants) or C-type lectin-like proteins, three-finger toxins (TFTs), and proteinase inhibitors (nonenzymatic anticoagulants). All of these factors cause coagulopathy due to snake bites, which is a clinically important phenomenon and should be carefully examined; otherwise, it would be difficult to make the diagnosis and treatment process. If untreated, coagulopathy can develop quickly and lead to the patient's death.
1- Babaie M, Salmanizadeh H, Zolfagharian H. Blood Coagulation induced by Iranian saw-scaled viper (Echis Carinatus) venom: Identification, purification and characterization of a prothrombin activator. Iran J Basic Med Sci. 2013; 16(11): 1145-50. DOI: 10.22038/IJBMS.2013.1931
2- Braud S, Bon C, Wisner A. Snake venom proteins acting on hemostasis. Biochimie. 2000; 82(9-10): 851-9. DOI: 10.1016/S0300-9084(00)01178-0
3- Lu Q, Clemetson JM, Clemetson KJ. Snake venoms and hemostasis. J Thromb Haemost 2005; 3: 1791-9. DOI: 10.1111/j.1538-7836.2005.01358.x
4- Salmanizadeh H, Zolfagharian H, Babaie M. Coagulopathy caused by the main anticoagulant fractions of Echis carinatus snake venom on blood. Int J Nano Stud Technol. 2015; 4(4): 93-99. DOI: 10.19070/2167-8685-1500018
5- Marsh N, Williams V. Practical applications of snake venom toxins in haemostasis. Toxicon. 2005; 45: 1171-81. DOI: 10.1016/j.toxicon.2005.02.016.
6- Barton CA. Treatment of coagulopathy related to hepatic insufficiency. Crit Care Med. 2016; 44(10): 1927-33. DOI: 10.1097/CCM.0000000000001998.
7- Zolfagharian H, Mohammadpour Dounighi N. Progress and improvement of the manufacturing process of snake antivenom. Arch Razi Ins. 2013; 68(1): 1-10. DOI: 10.7508/ARI.2013.01.001
8- White J. Snake venoms and coagulopathy. Toxicon. 2005; 45: 951-67. DOI: 10.1016/j.toxicon.2005.02.0309- Babaie M, Salmanizadeh H, Zolfagharian H, Alizadeh H. Properties of biological and biochemical effects of the Iranian saw-scaled viper (Echis carinatus) venom. Bratisl Lek Listy. 2014; 115(7): 434-438. DOI: 10.4149/bll_2014_085
10- Maduwage K, Isbister GK. Current treatment for venom-induced consumption coagulopathy resulting from snakebite. PLoS Negl Trop Dis. 2014; 8(10): e3220. DOI: 10.1371/journal.pntd.0003220
11- Babaie M. Proteins separation and purification methods with focus on chromatography: A review study. J Ardabil Univ Med Sci. 2021; 20(2): 151-75. Link
12- Babaie M, Zolfagharian H, Salmanizadeh H, Zare Mirakabadi A, Alizadeh H. Effect of a protrombin activator isolated from Iranian Echis carinatus venom on hemostasis. Sci J Iran Blood Transfus Organ. 2013; 10(2): 173-81. Link
13- Silva BC, Nonato CM, Albuquerque S, Ho LP, Junqueira de Azevedo, et al. Isolation and biochemical, functional and structural characterization of a novel L-amino acid oxidase from Lachesis muta snake venom. Toxicon. 2012; 60: 1263-76. DOI: 10.1016/j.toxicon.2012.08.008
14- Huang QQ, Teng MK, Niu LW. Purification and characterization of two fibrinogen-clotting enzymes from five-pace snake (Agkistrodon acutus) venom. Toxicon. 1999; 37: 999-1013. DOI: 10.1016/s0041-0101(98)00228-1
15- Kini RM. Anticoagulant proteins from snake venoms: Structure, function and mechanism. Biochem. 2006; 397: 377-87. DOI: 10.1042/BJ20060302
16- Zolfagharian H, Mohajeri M, Babaie M. Bee venom (Apis Mellifera) an effective potential alternative to gentamicin for specific bacteria strains: Bee venom an effective potential for bacteria. J Pharmacopuncture. 2016; 19(3): 225-30. DOI: 10.3831/KPI.2016.19.023
17- Verheij HM, Boffa MC, Rothen C, Bryckert MC, Verger R, De Haas GH. Correlation of enzymatic activity and anticoagulant properties of phospholipase A2. Eur J Biochem.1980; 112: 25-32. DOI: 10.1111/j.1432-1033.1980.tb04982.x
18- Izidoro LF, Ribeiro MC, Souza GR, Sant'Ana CD, Hamaguchi A, Homsi-Brandeburgo MI, et al. Biochemical and functional characterization of an L-amino acid oxidase isolated from Bothrops pirajai snake venom. Bioorg Med Chem. 2006; 14: 7034-43. DOI: 10.1016/j.bmc.2006.06.025
19- Samel M, Vija H, Rönnholm G, Siigur J, Kalkkinen N, Siigur E. Isolation and characterization of an apoptotic and platelet aggregation inhibiting L-amino acid oxidase from Vipera berus (common viper) venom. Biochim Biophys Acta. 2006; 1764; 707-14. DOI: 10.1016/j.bbapap.2006.01.021
20- Torii S, Naito M, Tsuruo T. Apoxin I, a novel apoptosis-inducing factor with l-amino acid oxidase activity purified from Western diamondback rattlesnake venom. J Biol Chem. 1997; 272: 9539-42. DOI: 10.1074/jbc.272.14.9539
21- Matsui T, Fujimura Y, Titani K. Snake venom proteases affecting hemostasis and thrombosis. Biochim Biophys Acta. 2000; 1477: 146-56. DOI: 10.1016/s0167-4838(99)00268-x
22- Howesa JM, Kamiguti AS, Theakston RDG, Wilkinson MC, Laing GD. Effects of three novel metalloproteinases from the venom of the West African saw-scaled viper, Echis ocellatus on blood coagulation and platelets. Biochim Biophys Acta. 2005; 1724: 194-202. DOI: 10.1016/j.bbagen.2005.03.011
23- Fox JW, Serrano SM. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS J. 2008; 275: 3016-30. DOI: 10.1111/j.1742-4658.2008.06466.x
24- Gutiérrez JM, Rucavado A. Snake venom metalloproteinases: their role in the pathogenesis of local tissue damage. Biochimie. 2000; 82: 841-50. DOI: 10.1016/s0300-9084(00)01163-9
25- Swenson S, Markland FS Jr. Snake venom fibrin (ogen)olytic enzymes. Toxicon. 2005; 45(8): 1021-39. 10.1016/j.toxicon.2005.02.027
26- Serrano SM, Maroun RC. Snake venom serine proteinases: sequence homology vs. substrate specificity, a paradox to be solved. Toxicon. 2005; 45: 1115-32. DOI: 10.1016/j.toxicon.2005.02.020
27- Vilca-Quispe A, Ponce-Soto LA, Winck FV, Marangoni S. Isolation and characterization of a new serine protease with thrombin-like activity (TLBm) from the venom of the snake Bothrops marajoensis. Toxicon. 2010; 55: 745-53. DOI: 10.1016/j.toxicon.2009.11.006
28- Oyama E, Takahashi H. Purification and characterization of a thrombin-like enzyme, elegaxobin, from the venom of Trimeresurus elegans (Sakishima habo). Toxicon. 2000; 38: 1087-100. DOI: 10.1016/s0041-0101(99)00220-2
29- Oyama E, Takahashi H. Purification and characterization of a thrombin-like enzyme, elegaxobin II, with lys-bradykinin releasing activity from the venom of Trimeresurus elegans (Sakishima-habo). Toxicon. 2003; 41: 559-68. DOI: 10.1016/s0041-0101(02)00363-x
30- Castro HC, Rodrigues CR. Current status of snake venom thrombin-like enzymes. Toxin Rev. 2006; 25(3): 291-318. DOI: 10.1080/15569540600567321
31- Castro HC, Zingali RB, Albuquerque MG, Pujol-Luz M, Rodrigues CR. Snake venom thrombin-like enzymes: from Reptilase to now. Cell Mol Life Sci. 2004; 61(7-8): 843-56. DOI: 10.1007/s00018-003-3325-z
32- Sant'Ana CD, Ticli FK, Oliveira LL, Giglio JR, Rechia CG, Fuly AL, et al. BjussuSP-I: A new thrombin-like enzyme isolated from Bothrops jararacussu snake venom. Comp Biochem Physiol A Mol Integr Physiol. 2008; 151(3): 443-454. DOI: 10.1016/j.cbpa.2007.02.036
33- Matsui T, Shakurai Y, Fujimura Y, Hayashi I, Ohishi S, Suzuki M, et al. Purification and amino acid sequence of halystase from snake venom of Agkistrodon halys blomhofi, a serine protease that cleaves specially fibrinogen and kininogen. Eur J Biochem. 1998; 252: 569-75. DOI: 10.1046/j.1432-1327.1998.2520569.x
34- Liu S, Sun MZ, Sun C, Zhao B, Greenaway FT, Zheng Q. A novel serine protease from the snake venom of Agkistrodon blomhoffii ussurensis. Toxicon. 2008; 52(7): 760-8. DOI: 10.1016/j.toxicon.2008.08.012
35- Perera L, Foley C, Darden TA, Stafford D, Mather T, Esmon CT, et al. Modeling Zymogen Protein C. Biophys J. 2000; 79(6): 2925-43. DOI: 10.1016/S0006-3495(00)76530-1
36- Murakami MT, Arni RK. Thrombomodulin-independent activation of protein C and specificity of hemostatically active snake venom serine proteinases: crystal structures of native and inhibited Agkistrodon contortrix contortrix protein C activator. J Biol Chem. 2005; 280(47): 39309-15. DOI: 10.1074/jbc.M508502200
37- Mann KG, Kalafatis M. Factor V: A combination of Dr Jekyll and Mr Hyde. Blood. 2003; 101(1): 20-30. DOI: 10.1182/blood-2002-01-0290
38- Rosing J, Govers-Riemslag JW, Yukelson L, Tans G. Factor V activation and inactivation by venom proteases. Haemostasis. 2001; 31(3-6): 241-6. DOI: 10.1159/000048069
39- Nicolau CA, Prorock A, Bao Y, Neves-Ferreira AGDC, Valente RH, Fox JW. Revisiting the therapeutic potential of Bothrops jararaca venom: Screening for novel activities using connectivity mapping. Toxins (Basel). 2018; 10(2): 69. DOI: 10.3390/toxins10020069
40- Tans G, Rosing J. Snake venom activators of factor X: an overview. Haemostasis. 2001; 31(3-6): 225-33. DOI: 10.1159/000048067
41- Lee WH, Zhang Y, Wang WY, Xiong YL, Gao R. Isolation and properties of a blood coagulation factor X activator from the venom of king cobra (hannah Ophiophagus). Toxicon. 1995; 33(10): 1263-76. DOI: 10.1016/0041-0101(95)00077-y
42- Zhang Y, Xiong YL, Bon C. An activator of blood coagulation factor X from the venom of Bungarus fasciatus. Toxicon. 1995; 33(10): 1277-88. DOI: 10.1016/0041-0101(95)00070-3
43- Siigur J, Siigur E. Factor X activating proteases from snake venoms. Tox Rev. 2006; 25: 235-55. DOI: 10.1080/15569540600567305
44- Fay PJ. Factor VIII structure and function. Int J Hematol. 2006; 83(2): 103-8. DOI: 10.1532/IJH97.05113
45- Lövgren A. Recombinant snake venom prothrombin activators. Bioengineered. 2013; 4(3): 153-7. DOI: 10.4161/bioe.22676
46- Camire RM. A new look at blood coagulation factor V. Curr Opin Hematol. 2011; 18(5): 338-42. DOI: 10.1097/MOH.0b013e3283497ebc
47- Law RH, Abu-Ssaydeh D, Whisstock JC. New insights into the structure and function of the plasminogen/plasmin system. Curr Opin Struct Biol. 2013; 23(6): 836-41. DOI: 10.1016/j.sbi.2013.10.006
48- Zhang Y, Wisner A, Xiong Y, Bon C. A novel plasminogen activator from snake venom. Purification, characterization, and molecular cloning. J Biol Chem. 1995; 270(17): 10246-55. DOI: 10.1074/jbc.270.17.10246
49- Park D, Kim H, Chung, K, Kim DS, Yun Y. Expression and characterization of a novel plasminogen activator from Agkistrodon halys venom. Toxicon. 1998; 36(12): 1807-19. DOI: 10.1016/s0041-0101(98)00090-7
50- Hermogenes AL, Richardson M, Magalhaes A, Yarleque A, Rodriguez E, Sanchez EF. Interaction of a plasminogen activator proteinase, LV-PA with human a2-macroglobulin. Toxicon. 2006; 47(4): 490-4. DOI: 10.1016/j.toxicon.2005.12.009
51- Dhananjaya BL, D Souza CJ. An overview on nucleases (DNase, RNase, and phosphodiesterase) in snake venoms. Biochemistry (Mosc). 2010; 75(1): 1-6. DOI: 10.1134/s0006297910010013
52- Chandrashekar V. Dilute Russell's viper venom and activated partial thromboplastin time in lupus anticoagulant diagnosis: is mixing essential? Blood Coagul Fibrinolysis. 2016; 27(4): 408-11. DOI: 10.1097/MBC.0000000000000463
53- Matsui T, Hamako J. Structure and function of snake venom toxins interacting with human von Willebrand factor. Toxicon. 2005; 45(8): 1075-87. DOI: 10.1016/j.toxicon.2005.02.023
54- Babaie M, Zolfagharian H, Salmanizadeh H, Zare MA, Alizadeh H. Isolation and partial purification of anticoagulant fractions from the venom of the Iranian snake Echis carinatus. Acta bichimica plonica 2013; 60(1): 17-20. Link
55- Andrews RK, Berndt MC. Snake venom modulators of platelet adhesion receptors and their ligands. Toxicon. 2000; 38(6): 775-91. DOI: 10.1016/s0041-0101(99)00187-7
56- Janssen M, Meier J, Freyvogel TA. Purification and characterization of an antithrombin III inactivating enzyme from the venom of the African night adder (Causus rhombeatus). Toxicon. 1992; 30(9): 985-99. DOI: 10.1016/0041-0101(92)90043-5
57- Berling I, Brown SG, Miteff F, Levi C, Isbister GK. Intracranial haemorrhages associated with venom induced consumption coagulopathy in Australian snakebites (ASP-21). Toxicon. 2015; 102: 8-13. DOI: 10.1016/j.toxicon.2015.05.012
58- Wu WB, Huang TF. Activation of MMP-2, cleavage of matrix proteins, and adherens junctions during a snake venom metalloproteinase- induced endothelial cell apoptosis. Exp Cell Res. 2003; 288(1): 143-57. DOI: 10.1016/s0014-4827(03)00183-6
59- Gutiérrez JM, Rucavado A, Escalante T, Díaz C. Hemorrhage induced by snake venom metalloproteinases: biochemical and biophysical mechanisms involved in microvessel damage. Toxicon. 2005; 45(8): 997-1011. DOI: 10.1016/j.toxicon.2005.02.029
60- Gutiérrez JM, Núñez J, Escalante T, Rucavado A. Blood flow is required for rapid endothelial cell damage induced by a snake venom hemorrhagic metalloproteinase. Microvasc Res. 2005; 71(1): 55-63. DOI: 10.1016/j.mvr.2005.10.007
61- Kini RM. The intriguing world of prothrombin activators from snake venom. Toxicon. 2005; 45(8); 1133-45. DOI: 10.1016/j.toxicon.2005.02.019
62- Salmanizadeh H, Babaie M, Zolfagharian H. In vivo evaluation of homeostatic effects of Echis carinatus snake venom in Iran. J Venom Anim Toxins incl Trop Dis. 2013; 19(3): 21-9. DOI: 10.1186/1678-9199-19-3
63- Patra A, Kalita B, Chanda A, Mukherjee AK. Proteomics and antivenomics of Echis carinatus carinatus venom: Correlation with pharmacological properties and pathophysiology of envenomation. Sci Rep. 2017; 7(1): 17119. DOI: 10.1038/s41598-017-17227-y
64- Rao VS, Kini RM. Pseutarin C, a prothrombin activator from Pseudonaja textilis venom: its structural and functional similarity to mammalian coagulation factor Xa-Va complex. Thromb Haemost. 2002; 88(4): 611-9. Link
65- Rao VS, Swarup S, Kini RM. The nonenzymatic subunit of pseutarin C, a prothrombin activator from eastern brown snake (Pseudonaja textilis) venom, shows structural similarity to mammalian coagulation factor V. Blood. 2003; 102(4): 1347-54. DOI: 10.1182/blood-2002-12-3839
66- Joseph JS, Chung MC, Jeyaseelan K, Kini RM. Amino acid sequence of trocarin, a prothrombin activator from Tropidechis carinatus venom: its structural similarity to coagulation factor Xa. Blood. 1999; 94(2): 621-31. Link
67- Zolfagharian H, Mohajeri M, Babaie M. Honey bee venom (Apis mellifera) contains anticoagulation factors and increases the blood-clotting time. J Pharmacopuncture. 2015; 18(4): 7-11. DOI: 10.3831/KPI.2015.18.031
68- Babaie M, Zolfagharian H, Zolfaghari M, Jamili S. Biochemical, hematological effects and complications of Pseudosynanceia melanostigma envenoming. J Pharmacopuncture. 2019; 22(3): 140-46. DOI: 10.3831/KPI.2015.18.031
69- Babaie M, Ghaempanah A. Evaluation of hemolytic activity and biochemical properties of Apis mellifera bee venom on NIH laboratory mice. J Neyshabur Univ Med Sci. 2020; 8(3): 23-34. Link
70- Babaie M, Ghaempanah A, Mehrabi Z, Mollaei A. Partial purification and characterization of antimicrobial effects from snake (Echis carinatus), scorpion (Mesosobuthus epues) and bee (Apis mellifera) venoms. Iran J Med Microbiol. 2020; 14(5): 460-77. DOI: 10.30699/ijmm.14.5.460
71- Borojeni SK, Zolfagharian H, Babaie M, Javadi I. Cytotoxic effect of bee (A. mellifera) venom on cancer cell lines. J Pharmacopuncture. 2020; 23(4): 212-19. DOI: 10.3831/KPI.2020.23.4.212
2- Braud S, Bon C, Wisner A. Snake venom proteins acting on hemostasis. Biochimie. 2000; 82(9-10): 851-9. DOI: 10.1016/S0300-9084(00)01178-0
3- Lu Q, Clemetson JM, Clemetson KJ. Snake venoms and hemostasis. J Thromb Haemost 2005; 3: 1791-9. DOI: 10.1111/j.1538-7836.2005.01358.x
4- Salmanizadeh H, Zolfagharian H, Babaie M. Coagulopathy caused by the main anticoagulant fractions of Echis carinatus snake venom on blood. Int J Nano Stud Technol. 2015; 4(4): 93-99. DOI: 10.19070/2167-8685-1500018
5- Marsh N, Williams V. Practical applications of snake venom toxins in haemostasis. Toxicon. 2005; 45: 1171-81. DOI: 10.1016/j.toxicon.2005.02.016.
6- Barton CA. Treatment of coagulopathy related to hepatic insufficiency. Crit Care Med. 2016; 44(10): 1927-33. DOI: 10.1097/CCM.0000000000001998.
7- Zolfagharian H, Mohammadpour Dounighi N. Progress and improvement of the manufacturing process of snake antivenom. Arch Razi Ins. 2013; 68(1): 1-10. DOI: 10.7508/ARI.2013.01.001
8- White J. Snake venoms and coagulopathy. Toxicon. 2005; 45: 951-67. DOI: 10.1016/j.toxicon.2005.02.0309- Babaie M, Salmanizadeh H, Zolfagharian H, Alizadeh H. Properties of biological and biochemical effects of the Iranian saw-scaled viper (Echis carinatus) venom. Bratisl Lek Listy. 2014; 115(7): 434-438. DOI: 10.4149/bll_2014_085
10- Maduwage K, Isbister GK. Current treatment for venom-induced consumption coagulopathy resulting from snakebite. PLoS Negl Trop Dis. 2014; 8(10): e3220. DOI: 10.1371/journal.pntd.0003220
11- Babaie M. Proteins separation and purification methods with focus on chromatography: A review study. J Ardabil Univ Med Sci. 2021; 20(2): 151-75. Link
12- Babaie M, Zolfagharian H, Salmanizadeh H, Zare Mirakabadi A, Alizadeh H. Effect of a protrombin activator isolated from Iranian Echis carinatus venom on hemostasis. Sci J Iran Blood Transfus Organ. 2013; 10(2): 173-81. Link
13- Silva BC, Nonato CM, Albuquerque S, Ho LP, Junqueira de Azevedo, et al. Isolation and biochemical, functional and structural characterization of a novel L-amino acid oxidase from Lachesis muta snake venom. Toxicon. 2012; 60: 1263-76. DOI: 10.1016/j.toxicon.2012.08.008
14- Huang QQ, Teng MK, Niu LW. Purification and characterization of two fibrinogen-clotting enzymes from five-pace snake (Agkistrodon acutus) venom. Toxicon. 1999; 37: 999-1013. DOI: 10.1016/s0041-0101(98)00228-1
15- Kini RM. Anticoagulant proteins from snake venoms: Structure, function and mechanism. Biochem. 2006; 397: 377-87. DOI: 10.1042/BJ20060302
16- Zolfagharian H, Mohajeri M, Babaie M. Bee venom (Apis Mellifera) an effective potential alternative to gentamicin for specific bacteria strains: Bee venom an effective potential for bacteria. J Pharmacopuncture. 2016; 19(3): 225-30. DOI: 10.3831/KPI.2016.19.023
17- Verheij HM, Boffa MC, Rothen C, Bryckert MC, Verger R, De Haas GH. Correlation of enzymatic activity and anticoagulant properties of phospholipase A2. Eur J Biochem.1980; 112: 25-32. DOI: 10.1111/j.1432-1033.1980.tb04982.x
18- Izidoro LF, Ribeiro MC, Souza GR, Sant'Ana CD, Hamaguchi A, Homsi-Brandeburgo MI, et al. Biochemical and functional characterization of an L-amino acid oxidase isolated from Bothrops pirajai snake venom. Bioorg Med Chem. 2006; 14: 7034-43. DOI: 10.1016/j.bmc.2006.06.025
19- Samel M, Vija H, Rönnholm G, Siigur J, Kalkkinen N, Siigur E. Isolation and characterization of an apoptotic and platelet aggregation inhibiting L-amino acid oxidase from Vipera berus (common viper) venom. Biochim Biophys Acta. 2006; 1764; 707-14. DOI: 10.1016/j.bbapap.2006.01.021
20- Torii S, Naito M, Tsuruo T. Apoxin I, a novel apoptosis-inducing factor with l-amino acid oxidase activity purified from Western diamondback rattlesnake venom. J Biol Chem. 1997; 272: 9539-42. DOI: 10.1074/jbc.272.14.9539
21- Matsui T, Fujimura Y, Titani K. Snake venom proteases affecting hemostasis and thrombosis. Biochim Biophys Acta. 2000; 1477: 146-56. DOI: 10.1016/s0167-4838(99)00268-x
22- Howesa JM, Kamiguti AS, Theakston RDG, Wilkinson MC, Laing GD. Effects of three novel metalloproteinases from the venom of the West African saw-scaled viper, Echis ocellatus on blood coagulation and platelets. Biochim Biophys Acta. 2005; 1724: 194-202. DOI: 10.1016/j.bbagen.2005.03.011
23- Fox JW, Serrano SM. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS J. 2008; 275: 3016-30. DOI: 10.1111/j.1742-4658.2008.06466.x
24- Gutiérrez JM, Rucavado A. Snake venom metalloproteinases: their role in the pathogenesis of local tissue damage. Biochimie. 2000; 82: 841-50. DOI: 10.1016/s0300-9084(00)01163-9
25- Swenson S, Markland FS Jr. Snake venom fibrin (ogen)olytic enzymes. Toxicon. 2005; 45(8): 1021-39. 10.1016/j.toxicon.2005.02.027
26- Serrano SM, Maroun RC. Snake venom serine proteinases: sequence homology vs. substrate specificity, a paradox to be solved. Toxicon. 2005; 45: 1115-32. DOI: 10.1016/j.toxicon.2005.02.020
27- Vilca-Quispe A, Ponce-Soto LA, Winck FV, Marangoni S. Isolation and characterization of a new serine protease with thrombin-like activity (TLBm) from the venom of the snake Bothrops marajoensis. Toxicon. 2010; 55: 745-53. DOI: 10.1016/j.toxicon.2009.11.006
28- Oyama E, Takahashi H. Purification and characterization of a thrombin-like enzyme, elegaxobin, from the venom of Trimeresurus elegans (Sakishima habo). Toxicon. 2000; 38: 1087-100. DOI: 10.1016/s0041-0101(99)00220-2
29- Oyama E, Takahashi H. Purification and characterization of a thrombin-like enzyme, elegaxobin II, with lys-bradykinin releasing activity from the venom of Trimeresurus elegans (Sakishima-habo). Toxicon. 2003; 41: 559-68. DOI: 10.1016/s0041-0101(02)00363-x
30- Castro HC, Rodrigues CR. Current status of snake venom thrombin-like enzymes. Toxin Rev. 2006; 25(3): 291-318. DOI: 10.1080/15569540600567321
31- Castro HC, Zingali RB, Albuquerque MG, Pujol-Luz M, Rodrigues CR. Snake venom thrombin-like enzymes: from Reptilase to now. Cell Mol Life Sci. 2004; 61(7-8): 843-56. DOI: 10.1007/s00018-003-3325-z
32- Sant'Ana CD, Ticli FK, Oliveira LL, Giglio JR, Rechia CG, Fuly AL, et al. BjussuSP-I: A new thrombin-like enzyme isolated from Bothrops jararacussu snake venom. Comp Biochem Physiol A Mol Integr Physiol. 2008; 151(3): 443-454. DOI: 10.1016/j.cbpa.2007.02.036
33- Matsui T, Shakurai Y, Fujimura Y, Hayashi I, Ohishi S, Suzuki M, et al. Purification and amino acid sequence of halystase from snake venom of Agkistrodon halys blomhofi, a serine protease that cleaves specially fibrinogen and kininogen. Eur J Biochem. 1998; 252: 569-75. DOI: 10.1046/j.1432-1327.1998.2520569.x
34- Liu S, Sun MZ, Sun C, Zhao B, Greenaway FT, Zheng Q. A novel serine protease from the snake venom of Agkistrodon blomhoffii ussurensis. Toxicon. 2008; 52(7): 760-8. DOI: 10.1016/j.toxicon.2008.08.012
35- Perera L, Foley C, Darden TA, Stafford D, Mather T, Esmon CT, et al. Modeling Zymogen Protein C. Biophys J. 2000; 79(6): 2925-43. DOI: 10.1016/S0006-3495(00)76530-1
36- Murakami MT, Arni RK. Thrombomodulin-independent activation of protein C and specificity of hemostatically active snake venom serine proteinases: crystal structures of native and inhibited Agkistrodon contortrix contortrix protein C activator. J Biol Chem. 2005; 280(47): 39309-15. DOI: 10.1074/jbc.M508502200
37- Mann KG, Kalafatis M. Factor V: A combination of Dr Jekyll and Mr Hyde. Blood. 2003; 101(1): 20-30. DOI: 10.1182/blood-2002-01-0290
38- Rosing J, Govers-Riemslag JW, Yukelson L, Tans G. Factor V activation and inactivation by venom proteases. Haemostasis. 2001; 31(3-6): 241-6. DOI: 10.1159/000048069
39- Nicolau CA, Prorock A, Bao Y, Neves-Ferreira AGDC, Valente RH, Fox JW. Revisiting the therapeutic potential of Bothrops jararaca venom: Screening for novel activities using connectivity mapping. Toxins (Basel). 2018; 10(2): 69. DOI: 10.3390/toxins10020069
40- Tans G, Rosing J. Snake venom activators of factor X: an overview. Haemostasis. 2001; 31(3-6): 225-33. DOI: 10.1159/000048067
41- Lee WH, Zhang Y, Wang WY, Xiong YL, Gao R. Isolation and properties of a blood coagulation factor X activator from the venom of king cobra (hannah Ophiophagus). Toxicon. 1995; 33(10): 1263-76. DOI: 10.1016/0041-0101(95)00077-y
42- Zhang Y, Xiong YL, Bon C. An activator of blood coagulation factor X from the venom of Bungarus fasciatus. Toxicon. 1995; 33(10): 1277-88. DOI: 10.1016/0041-0101(95)00070-3
43- Siigur J, Siigur E. Factor X activating proteases from snake venoms. Tox Rev. 2006; 25: 235-55. DOI: 10.1080/15569540600567305
44- Fay PJ. Factor VIII structure and function. Int J Hematol. 2006; 83(2): 103-8. DOI: 10.1532/IJH97.05113
45- Lövgren A. Recombinant snake venom prothrombin activators. Bioengineered. 2013; 4(3): 153-7. DOI: 10.4161/bioe.22676
46- Camire RM. A new look at blood coagulation factor V. Curr Opin Hematol. 2011; 18(5): 338-42. DOI: 10.1097/MOH.0b013e3283497ebc
47- Law RH, Abu-Ssaydeh D, Whisstock JC. New insights into the structure and function of the plasminogen/plasmin system. Curr Opin Struct Biol. 2013; 23(6): 836-41. DOI: 10.1016/j.sbi.2013.10.006
48- Zhang Y, Wisner A, Xiong Y, Bon C. A novel plasminogen activator from snake venom. Purification, characterization, and molecular cloning. J Biol Chem. 1995; 270(17): 10246-55. DOI: 10.1074/jbc.270.17.10246
49- Park D, Kim H, Chung, K, Kim DS, Yun Y. Expression and characterization of a novel plasminogen activator from Agkistrodon halys venom. Toxicon. 1998; 36(12): 1807-19. DOI: 10.1016/s0041-0101(98)00090-7
50- Hermogenes AL, Richardson M, Magalhaes A, Yarleque A, Rodriguez E, Sanchez EF. Interaction of a plasminogen activator proteinase, LV-PA with human a2-macroglobulin. Toxicon. 2006; 47(4): 490-4. DOI: 10.1016/j.toxicon.2005.12.009
51- Dhananjaya BL, D Souza CJ. An overview on nucleases (DNase, RNase, and phosphodiesterase) in snake venoms. Biochemistry (Mosc). 2010; 75(1): 1-6. DOI: 10.1134/s0006297910010013
52- Chandrashekar V. Dilute Russell's viper venom and activated partial thromboplastin time in lupus anticoagulant diagnosis: is mixing essential? Blood Coagul Fibrinolysis. 2016; 27(4): 408-11. DOI: 10.1097/MBC.0000000000000463
53- Matsui T, Hamako J. Structure and function of snake venom toxins interacting with human von Willebrand factor. Toxicon. 2005; 45(8): 1075-87. DOI: 10.1016/j.toxicon.2005.02.023
54- Babaie M, Zolfagharian H, Salmanizadeh H, Zare MA, Alizadeh H. Isolation and partial purification of anticoagulant fractions from the venom of the Iranian snake Echis carinatus. Acta bichimica plonica 2013; 60(1): 17-20. Link
55- Andrews RK, Berndt MC. Snake venom modulators of platelet adhesion receptors and their ligands. Toxicon. 2000; 38(6): 775-91. DOI: 10.1016/s0041-0101(99)00187-7
56- Janssen M, Meier J, Freyvogel TA. Purification and characterization of an antithrombin III inactivating enzyme from the venom of the African night adder (Causus rhombeatus). Toxicon. 1992; 30(9): 985-99. DOI: 10.1016/0041-0101(92)90043-5
57- Berling I, Brown SG, Miteff F, Levi C, Isbister GK. Intracranial haemorrhages associated with venom induced consumption coagulopathy in Australian snakebites (ASP-21). Toxicon. 2015; 102: 8-13. DOI: 10.1016/j.toxicon.2015.05.012
58- Wu WB, Huang TF. Activation of MMP-2, cleavage of matrix proteins, and adherens junctions during a snake venom metalloproteinase- induced endothelial cell apoptosis. Exp Cell Res. 2003; 288(1): 143-57. DOI: 10.1016/s0014-4827(03)00183-6
59- Gutiérrez JM, Rucavado A, Escalante T, Díaz C. Hemorrhage induced by snake venom metalloproteinases: biochemical and biophysical mechanisms involved in microvessel damage. Toxicon. 2005; 45(8): 997-1011. DOI: 10.1016/j.toxicon.2005.02.029
60- Gutiérrez JM, Núñez J, Escalante T, Rucavado A. Blood flow is required for rapid endothelial cell damage induced by a snake venom hemorrhagic metalloproteinase. Microvasc Res. 2005; 71(1): 55-63. DOI: 10.1016/j.mvr.2005.10.007
61- Kini RM. The intriguing world of prothrombin activators from snake venom. Toxicon. 2005; 45(8); 1133-45. DOI: 10.1016/j.toxicon.2005.02.019
62- Salmanizadeh H, Babaie M, Zolfagharian H. In vivo evaluation of homeostatic effects of Echis carinatus snake venom in Iran. J Venom Anim Toxins incl Trop Dis. 2013; 19(3): 21-9. DOI: 10.1186/1678-9199-19-3
63- Patra A, Kalita B, Chanda A, Mukherjee AK. Proteomics and antivenomics of Echis carinatus carinatus venom: Correlation with pharmacological properties and pathophysiology of envenomation. Sci Rep. 2017; 7(1): 17119. DOI: 10.1038/s41598-017-17227-y
64- Rao VS, Kini RM. Pseutarin C, a prothrombin activator from Pseudonaja textilis venom: its structural and functional similarity to mammalian coagulation factor Xa-Va complex. Thromb Haemost. 2002; 88(4): 611-9. Link
65- Rao VS, Swarup S, Kini RM. The nonenzymatic subunit of pseutarin C, a prothrombin activator from eastern brown snake (Pseudonaja textilis) venom, shows structural similarity to mammalian coagulation factor V. Blood. 2003; 102(4): 1347-54. DOI: 10.1182/blood-2002-12-3839
66- Joseph JS, Chung MC, Jeyaseelan K, Kini RM. Amino acid sequence of trocarin, a prothrombin activator from Tropidechis carinatus venom: its structural similarity to coagulation factor Xa. Blood. 1999; 94(2): 621-31. Link
67- Zolfagharian H, Mohajeri M, Babaie M. Honey bee venom (Apis mellifera) contains anticoagulation factors and increases the blood-clotting time. J Pharmacopuncture. 2015; 18(4): 7-11. DOI: 10.3831/KPI.2015.18.031
68- Babaie M, Zolfagharian H, Zolfaghari M, Jamili S. Biochemical, hematological effects and complications of Pseudosynanceia melanostigma envenoming. J Pharmacopuncture. 2019; 22(3): 140-46. DOI: 10.3831/KPI.2015.18.031
69- Babaie M, Ghaempanah A. Evaluation of hemolytic activity and biochemical properties of Apis mellifera bee venom on NIH laboratory mice. J Neyshabur Univ Med Sci. 2020; 8(3): 23-34. Link
70- Babaie M, Ghaempanah A, Mehrabi Z, Mollaei A. Partial purification and characterization of antimicrobial effects from snake (Echis carinatus), scorpion (Mesosobuthus epues) and bee (Apis mellifera) venoms. Iran J Med Microbiol. 2020; 14(5): 460-77. DOI: 10.30699/ijmm.14.5.460
71- Borojeni SK, Zolfagharian H, Babaie M, Javadi I. Cytotoxic effect of bee (A. mellifera) venom on cancer cell lines. J Pharmacopuncture. 2020; 23(4): 212-19. DOI: 10.3831/KPI.2020.23.4.212
Type of Study: Review |
Subject:
Biochemistry
Received: 2020/03/29 | Accepted: 2020/06/22 | ePublished ahead of print: 2021/05/10 | ePublished: 2021/06/20
Received: 2020/03/29 | Accepted: 2020/06/22 | ePublished ahead of print: 2021/05/10 | ePublished: 2021/06/20
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