Elevated prothrombin promotes venous, but not arterial, thrombosis in mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 8, 2013, Pages 1829-1836

  Aleman, Maria M ^a   Walton, Bethany L ^a   Byrnes, James R ^a   Wang, Jian Guo ^a   Heisler, Matthew J ^a   Machlus, Kellie R ^a   Cooley, Brian C ^b   Wolberg, Alisa S ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Arterial; Fibrin; Hyperprothrombinemia; Platelet; Prothrombin; Thrombosis; Venous

Indexed keywords

FERRIC CHLORIDE; PROTHROMBIN; THROMBIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY THROMBOSIS; ARTICLE; BLOOD CLOTTING; BLOOD VESSEL INJURY; CAROTID ARTERY; CONTROLLED STUDY; EX VIVO STUDY; FEMORAL VEIN; FIBRIN DEPOSITION; IN VIVO STUDY; INFERIOR CAVA VEIN; MOUSE; NONHUMAN; PRIORITY JOURNAL; THROMBOGENICITY; VEIN THROMBOSIS;

ARTERIAL; FIBRIN; HYPERPROTHROMBINEMIA; PLATELET; PROTHROMBIN; THROMBOSIS; VENOUS;

ANIMALS; BLOOD COAGULATION; BLOOD PLATELETS; CAROTID ARTERIES; CHLORIDES; DISEASE MODELS, ANIMAL; FEMORAL VEIN; FERRIC COMPOUNDS; FIBRIN; HUMANS; MICE; NOXAE; PROTHROMBIN; RISK FACTORS; THROMBOPHILIA; VENA CAVA, INFERIOR; VENOUS THROMBOSIS;

EID: 84881026510     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.301607     Document Type: Article

References (46)

1. Lijfering WM, Flinterman LE, Vandenbroucke JP, Rosendaal FR, Cannegieter SC. Relationship between venous and arterial thrombosis: a review of the literature from a causal perspective. Semin Thromb Hemost. 2011;37: 885-896.
2. Turpie AG, Esmon C. Venous and arterial thrombosis-pathogenesis and the rationale for anticoagulation. Thromb Haemost. 2011;105: 586-596.
3. Brighton TA, Eikelboom JW, Mann K, Mister R, Gallus A, Ockelford P, Gibbs H, Hague W, Xavier D, Diaz R, Kirby A, Simes J; ASPIRE Investigators. Low-dose aspirin for preventing recurrent venous thromboembolism. N Engl J Med. 2012;367: 1979-1987.
4. Poort SR, Rosendaal FR, Reitsma PH, Bertina RM. A common genetic variation in the 3'-untranslated region of the prothrombin gene is associated with elevated plasma prothrombin levels and an increase in venous thrombosis. Blood. 1996;88: 3698-3703.
5. Makris M, Preston FE, Beauchamp NJ, Cooper PC, Daly ME, Hampton KK, Bayliss P, Peake IR, Miller GJ. Co-inheritance of the 20210A allele of the prothrombin gene increases the risk of thrombosis in subjects with familial thrombophilia. Thromb Haemost. 1997;78: 1426-1429.
6. Kyrle PA, Mannhalter C, Béguin S, Stümpflen A, Hirschl M, Weltermann A, Stain M, Brenner B, Speiser W, Pabinger I, Lechner K, Eichinger S. Clinical studies and thrombin generation in patients homozygous or heterozygous for the G20210A mutation in the prothrombin gene. Arterioscler Thromb Vasc Biol. 1998;18: 1287-1291.
7. Rosendaal FR, Doggen CJ, Zivelin A, Arruda VR, Aiach M, Siscovick DS, Hillarp A, Watzke HH, Bernardi F, Cumming AM, Preston FE, Reitsma PH. Geographic distribution of the 20210 G to A prothrombin variant. Thromb Haemost. 1998;79: 706-708.
8. Kim RJ, Becker RC. Association between factor V Leiden, prothrombin G20210A, and methylenetetrahydrofolate reductase C677T mutations and events of the arterial circulatory system: a meta-analysis of published studies. Am Heart J. 2003;146: 948-957.
9. Ye Z, Liu EH, Higgins JP, Keavney BD, Lowe GD, Collins R, Danesh J. Seven haemostatic gene polymorphisms in coronary disease: meta-analysis of 66,155 cases and 91,307 controls. Lancet. 2006;367: 651-658.
10. Arruda VR, Annichino-Bizzacchi JM, Gonçalves MS, Costa FF. Prevalence of the prothrombin gene variant (nt20210A) in venous thrombosis and arterial disease. Thromb Haemost. 1997;78: 1430-1433.
11. Watzke HH, Schüttrumpf J, Graf S, Huber K, Panzer S. Increased prevalence of a polymorphism in the gene coding for human prothrombin in patients with coronary heart disease. Thromb Res. 1997;87: 521-526.
12. De Stefano V, Chiusolo P, Paciaroni K, Casorelli I, Rossi E, Molinari M, Servidei S, Tonali PA, Leone G. Prothrombin G20210A mutant genotype is a risk factor for cerebrovascular ischemic disease in young patients. Blood. 1998;91: 3562-3565.
13. Rosendaal FR, Siscovick DS, Schwartz SM, Psaty BM, Raghunathan TE, Vos HL. A common prothrombin variant (20210 G to A) increases the risk of myocardial infarction in young women. Blood. 1997;90: 1747-1750.
14. Doggen CJ, Cats VM, Bertina RM, Rosendaal FR. Interaction of coagulation defects and cardiovascular risk factors: increased risk of myocardial infarction associated with factor V Leiden or prothrombin 20210A. Circulation. 1998;97: 1037-1041.
15. Martinelli I, Franchi F, Akwan S, Bettini P, Merati G, Mannucci PM. The transition G to A at position 20210 in the 3'-untranslated region of the prothrombin gene is not associated with cerebral ischemia. Blood. 1997;90:3806.
16. Lalouschek W, Aull S, Series W, Zeiler K, Mannhalter C. The prothrombin G20210A mutation and factor V Leiden mutation in patients with cerebrovascular disease. Blood. 1998;92: 704-705.
17. Coulet F, Godard V, Verdy E, Soubrier F. Lack of association of the prothrombin gene variant G20210A with myocardial infarction in Caucasian males. Thromb Haemost. 2000;83: 796-797.
18. Ferraresi P, Marchetti G, Legnani C, Cavallari E, Castoldi E, Mascoli F, Ardissino D, Palareti G, Bernardi F. The heterozygous 20210 G/A prothrombin genotype is associated with early venous thrombosis in inherited thrombophilias and is not increased in frequency in artery disease. Arterioscler Thromb Vasc Biol. 1997;17: 2418-2422.
19. Wolberg AS, Monroe DM, Roberts HR, Hoffman M. Elevated prothrombin results in clots with an altered fiber structure: a possible mechanism of the increased thrombotic risk. Blood. 2003;101: 3008-3013.
20. Allen GA, Wolberg AS, Oliver JA, Hoffman M, Roberts HR, Monroe DM. Impact of procoagulant concentration on rate, peak and total thrombin generation in a model system. J Thromb Haemost. 2004;2: 402-413.
21. Butenas S, van't Veer C, Mann KG. "Normal" thrombin generation. Blood. 1999;94: 2169-2178.
22. Castoldi E, Simioni P, Tormene D, Thomassen MC, Spiezia L, Gavasso S, Rosing J. Differential effects of high prothrombin levels on thrombin generation depending on the cause of the hyperprothrombinemia. J Thromb Haemost. 2007;5: 971-979.
23. Binetti BM, Rotunno C, Tripodi A, Asti D, Semeraro F, Semeraro N, Colucci M. Hyperprothrombinaemia-induced APC resistance: differential influence on fibrin formation and fibrinolysis. Thromb Haemost. 2006;95: 606-611.
24. Colucci M, Binetti BM, Tripodi A, Chantarangkul V, Semeraro N. Hyperprothrombinemia associated with prothrombin G20210A mutation inhibits plasma fibrinolysis through a TAFI-mediated mechanism. Blood. 2004;103: 2157-2161.
25. Degen SJ, Schaefer LA, Jamison CS, Grant SG, Fitzgibbon JJ, Pai JA, Chapman VM, Elliott RW. Characterization of the cDNA coding for mouse prothrombin and localization of the gene on mouse chromosome 2. DNA Cell Biol. 1990;9: 487-498.
26. Mosesson MW, Hernandez I, Raife TJ, Medved L, Yakovlev S, Simpson- Haidaris PJ, Uitte DE Willige S, Bertina RM. Plasma fibrinogen gamma' chain content in the thrombotic microangiopathy syndrome. J Thromb Haemost. 2007;5: 62-69.
27. Pretorius E, Oberholzer HM, Smit E. Ultrastructure of activated mouse platelets: a qualitative scanning electron microscopy study. Microsc Res Tech. 2008;71: 413-417.
28. Weiler-Guettler H, Christie PD, Beeler DL, Healy AM, Hancock WW, Rayburn H, Edelberg JM, Rosenberg RD. A targeted point mutation in thrombomodulin generates viable mice with a prethrombotic state. J Clin Invest. 1998;101: 1983-1991.
29. Kumada T, Dittman WA, Majerus PW. A role for thrombomodulin in the pathogenesis of thrombin-induced thromboembolism in mice. Blood. 1988;71: 728-733.
30. Cooley BC. In vivo fluorescence imaging of large-vessel thrombosis in mice. Arterioscler Thromb Vasc Biol. 2011;31: 1351-1356.
31. Cooley BC, Herrera AJ. Cross-modulatory effects of clopidogrel and heparin on platelet and fibrin incorporation in thrombosis. Blood Coagul Fibrinolysis. March 13, 2013. doi: 10.1097/MBC.0b013e3283602a03. http://journals. lww.com/bloodcoagulation/Abstract/publishahead/Cross- modulatory- effects-of-clopidogrel-and.99394.aspx. Accessed June 4, 2013.
32. Day SM, Reeve JL, Pedersen B, Farris DM, Myers DD, Im M, Wakefield TW, Mackman N, Fay WP. Macrovascular thrombosis is driven by tissue factor derived primarily from the blood vessel wall. Blood. 2005;105: 192-198.
33. Woollard KJ, Sturgeon S, Chin-Dusting JP, Salem HH, Jackson SP. Erythrocyte hemolysis and hemoglobin oxidation promote ferric chlorideinduced vascular injury. J Biol Chem. 2009;284: 13110-13118.
34. Eckly A, Hechler B, Freund M, Zerr M, Cazenave JP, Lanza F, Mangin PH, Gachet C. Mechanisms underlying FeCl3-induced arterial thrombosis. J Thromb Haemost. 2011;9: 779-789.
35. Owens AP 3rd, Lu Y, Whinna HC, Gachet C, Fay WP, Mackman N. Towards a standardization of the murine ferric chloride-induced carotid arterial thrombosis model. J Thromb Haemost. 2011;9: 1862-1863.
36. Siller-Matula JM, Bayer G, Bergmeister H, Quehenberger P, Petzelbauer P, Friedl P, Mesteri I, Jilma B. An experimental model to study isolated effects of thrombin in vivo. Thromb Res. 2010;126: 454-461.
37. Siller-Matula JM, Schwameis M, Blann A, Mannhalter C, Jilma B. Thrombin as a multi-functional enzyme. Focus on in vitro and in vivo effects. Thromb Haemost. 2011;106: 1020-1033.
38. Cooley BC. Murine models of thrombosis. Thromb Res. 2012;129(Suppl 2):S62-S64.
39. Borissoff JI, Otten JJ, Heeneman S, et al. Genetic and pharmacological modifications of thrombin formation in apolipoprotein e-deficient mice determine atherosclerosis severity and atherothrombosis onset in a neutrophil- dependent manner. PLoS One. 2013;8:e55784.
40. Wolberg AS. Thrombin generation and fibrin clot structure. Blood Rev. 2007;21: 131-142.
41. Machlus KR, Lin FC, Wolberg AS. Procoagulant activity induced by vascular injury determines contribution of elevated factor VIII to thrombosis and thrombus stability in mice. Blood. 2011;118: 3960-3968.
42. Marchi R, Walton BL, McGary CS, Lin FC, Ma AD, Pawlinski R, Mackman N, Campbell RA, Di Paola J, Wolberg AS. Dysregulated coagulation associated with hypofibrinogenaemia and plasma hypercoagulability: implications for identifying coagulopathic mechanisms in humans. Thromb Haemost. 2012;108: 516-526.
43. Golder M, Mewburn J, Lillicrap D. In vitro and in vivo evaluation of the effect of elevated factor VIII on the thrombogenic process. Thromb Haemost. 2013;109: 53-60.
44. Machlus KR, Colby EA, Wu JR, Koch GG, Key NS, Wolberg AS. Effects of tissue factor, thrombomodulin and elevated clotting factor levels on thrombin generation in the calibrated automated thrombogram. Thromb Haemost. 2009;102: 936-944.
45. Monroe DM, Hoffman M. What does it take to make the perfect clot? Arterioscler Thromb Vasc Biol. 2006;26: 41-48.
46. Corral J, Zuazu-Jausoro I, Rivera J, González-Conejero R, Ferrer F, Vicente V. Clinical and analytical relevance of the combination of prothrombin 20210A/A and factor V Leiden: results from a large family. Br J Haematol. 1999;105: 560-563.