Exacerbated venous thromboembolism in mice carrying a protein S K196E mutation

Blood - Tập 126 - Trang 2247-2253 - 2015
Fumiaki Banno1, Toshiyuki Kita1, José A. Fernández2, Hiroji Yanamoto3, Yuko Tashima1, Koichi Kokame1, John H. Griffin2, Toshiyuki Miyata1,4
1Department of Molecular Pathogenesis, National Cerebral and Cardiovascular Center, Suita, Japan
2Department of Molecular and Experimental Medicine, The Scripps Research Institute, La Jolla, CA
3Laboratory of Neurology and Neurosurgery
4Department of Cerebrovascular Medicine, National Cerebral and Cardiovascular Center, Suita, Japan

Tóm tắt

Key Points

A protein S-K196E mutation reduced its activated protein C cofactor activity in recombinant murine protein S-K196E and in K196E mutant mice. Mice carrying a protein S-K196E mutation or heterozygous protein S deficiency were more vulnerable to venous thrombosis than wild-type mice.


Tài liệu tham khảo

Dahlbäck, 2007, The tale of protein S and C4b-binding protein, a story of affection., Thromb Haemost, 98, 90 Griffin, 2012, Protein C anticoagulant and cytoprotective pathways., Int J Hematol, 95, 333, 10.1007/s12185-012-1059-0 Saller, 2009, Generation and phenotypic analysis of protein S-deficient mice., Blood, 114, 2307, 10.1182/blood-2009-03-209031 García de Frutos, 2007, Molecular basis of protein S deficiency., Thromb Haemost, 98, 543 Gómez, 1994, Homozygous protein S deficiency due to a one base pair deletion that leads to a stop codon in exon III of the protein S gene., Thromb Haemost, 71, 723, 10.1055/s-0038-1642512 Hayashi, 1994, Protein S Tokushima: abnormal molecule with a substitution of Glu for Lys-155 in the second epidermal growth factor-like domain of protein S., Blood, 83, 683, 10.1182/blood.V83.3.683.683 Yamazaki, 1993, A phenotypically neutral dimorphism of protein S: the substitution of Lys155 by Glu in the second EGF domain predicted by an A to G base exchange in the gene., Thromb Res, 70, 395, 10.1016/0049-3848(93)90081-X Kinoshita, 2005, Protein S and protein C gene mutations in Japanese deep vein thrombosis patients., Clin Biochem, 38, 908, 10.1016/j.clinbiochem.2005.05.006 Kimura, 2006, Protein S-K196E mutation as a genetic risk factor for deep vein thrombosis in Japanese patients., Blood, 107, 1737, 10.1182/blood-2005-09-3892 Ikejiri, 2010, The association of protein S Tokushima-K196E with a risk of deep vein thrombosis., Int J Hematol, 92, 302, 10.1007/s12185-010-0671-0 Yin, 2014, Dysfunction of protein C anticoagulant system, main genetic risk factor for venous thromboembolism in northeast Asians., J Thromb Thrombolysis, 37, 56, 10.1007/s11239-013-1005-x Kimura, 2006, Plasma protein S activity correlates with protein S genotype but is not sensitive to identify K196E mutant carriers., J Thromb Haemost, 4, 2010, 10.1111/j.1538-7836.2006.02071.x Miyata, 2006, Genetic risk factors for deep vein thrombosis among Japanese: importance of protein S K196E mutation., Int J Hematol, 83, 217, 10.1532/IJH97.A20514 Miyata, 2012, More on: racial differences in venous thromboembolism., J Thromb Haemost, 10, 319, 10.1111/j.1538-7836.2011.04578.x Neki, 2011, Genetic analysis of patients with deep vein thrombosis during pregnancy and postpartum., Int J Hematol, 94, 150, 10.1007/s12185-011-0902-z Miyata, 2009, Prevalence of genetic mutations in protein S, protein C and antithrombin genes in Japanese patients with deep vein thrombosis., Thromb Res, 124, 14, 10.1016/j.thromres.2008.08.020 Neki, 2014, Nonsynonymous mutations in three anticoagulant genes in Japanese patients with adverse pregnancy outcomes., Thromb Res, 133, 914, 10.1016/j.thromres.2014.02.012 Pecheniuk, 2008, Failure to validate association of gene polymorphisms in EPCR, PAR-1, FSAP and protein S Tokushima with venous thromboembolism among Californians of European ancestry., Thromb Haemost, 99, 453, 10.1160/TH07-10-0607 Liu, 2013, Protein S K196E mutation, a genetic risk factor for venous thromboembolism, is limited to Japanese., Thromb Res, 132, 314, 10.1016/j.thromres.2013.05.008 Goldhaber, 2014, Race and venous thromboembolism: nature or nurture?, Circulation, 129, 1463, 10.1161/CIRCULATIONAHA.114.008799 Kujovich, 2011, Factor V Leiden thrombophilia., Genet Med, 13, 1, 10.1097/GIM.0b013e3181faa0f2 Dahlbäck, 2008, Advances in understanding pathogenic mechanisms of thrombophilic disorders., Blood, 112, 19, 10.1182/blood-2008-01-077909 Ridker, 1995, Mutation in the gene coding for coagulation factor V and the risk of myocardial infarction, stroke, and venous thrombosis in apparently healthy men., N Engl J Med, 332, 912, 10.1056/NEJM199504063321403 Cui, 2000, Spontaneous thrombosis in mice carrying the factor V Leiden mutation., Blood, 96, 4222, 10.1182/blood.V96.13.4222 Eitzman, 2005, Homozygosity for factor V Leiden leads to enhanced thrombosis and atherosclerosis in mice., Circulation, 111, 1822, 10.1161/01.CIR.0000160854.75779.E8 Kerlin, 2003, Survival advantage associated with heterozygous factor V Leiden mutation in patients with severe sepsis and in mouse endotoxemia., Blood, 102, 3085, 10.1182/blood-2003-06-1789 Wang, 2011, Low but sustained coagulation activation ameliorates glucose-induced podocyte apoptosis: protective effect of factor V Leiden in diabetic nephropathy., Blood, 117, 5231, 10.1182/blood-2010-10-314773 Burstyn-Cohen, 2009, Lack of protein S in mice causes embryonic lethal coagulopathy and vascular dysgenesis., J Clin Invest, 119, 2942, 10.1172/JCI39325 Okuda, 2004, Ndrg1-deficient mice exhibit a progressive demyelinating disorder of peripheral nerves., Mol Cell Biol, 24, 3949, 10.1128/MCB.24.9.3949-3956.2004 Banno, 2006, Complete deficiency in ADAMTS13 is prothrombotic, but it alone is not sufficient to cause thrombotic thrombocytopenic purpura., Blood, 107, 3161, 10.1182/blood-2005-07-2765 Yamamoto, 2011, NDRG4 protein-deficient mice exhibit spatial learning deficits and vulnerabilities to cerebral ischemia., J Biol Chem, 286, 26158, 10.1074/jbc.M111.256446 Eura, 2012, Derlin-1 deficiency is embryonic lethal, Derlin-3 deficiency appears normal, and Herp deficiency is intolerant to glucose load and ischemia in mice., PLoS One, 7, e34298, 10.1371/journal.pone.0034298 Fernández, 2009, Species-specific anticoagulant and mitogenic activities of murine protein S., Haematologica, 94, 1721, 10.3324/haematol.2009.009233 Diaz, 2013, The electrolytic inferior vena cava model (EIM) to study thrombogenesis and thrombus resolution with continuous blood flow in the mouse., Thromb Haemost, 109, 1158, 10.1160/TH12-09-0711 Tashima, 2015, Influence of ADAMTS13 deficiency on venous thrombosis in mice., Thromb Haemost, 114, 206, 10.1160/TH14-08-0656 Smith, 2010, Polyphosphate exerts differential effects on blood clotting, depending on polymer size., Blood, 116, 4353, 10.1182/blood-2010-01-266791 Müller, 2009, Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo., Cell, 139, 1143, 10.1016/j.cell.2009.11.001 Yanamoto, 2003, Evaluation of MCAO stroke models in normotensive rats: standardized neocortical infarction by the 3VO technique., Exp Neurol, 182, 261, 10.1016/S0014-4886(03)00116-X Yang, 2014, An integrated stroke model with a consistent penumbra for the assessment of neuroprotective interventions., Eur Neurol, 71, 4, 10.1159/000356048 Wojcik, 2011, Interleukin-6: a potential target for post-thrombotic syndrome., Ann Vasc Surg, 25, 229, 10.1016/j.avsg.2010.09.003 DeRoo, 2015, The role of galectin-3 and galectin-3-binding protein in venous thrombosis., Blood, 125, 1813, 10.1182/blood-2014-04-569939 Kita, 2012, Large infarct and high mortality by cerebral ischemia in mice carrying the factor V Leiden mutation., J Thromb Haemost, 10, 1453, 10.1111/j.1538-7836.2012.04776.x MacArthur, 2014, Guidelines for investigating causality of sequence variants in human disease., Nature, 508, 469, 10.1038/nature13127 Rodríguez de Córdoba, 1994, The gene coding for the beta-chain of C4b-binding protein (C4BPB) has become a pseudogene in the mouse., Genomics, 21, 501, 10.1006/geno.1994.1308 Maruyama, 2015, ELISA-based detection system for protein S K196E mutation, a genetic risk factor for venous thromboembolism., PLoS One, 10, e0133196, 10.1371/journal.pone.0133196 Liu Zhu, 2010, Protein S controls hypoxic/ischemic blood-brain barrier disruption through the TAM receptor Tyro3 and sphingosine 1-phosphate receptor., Blood, 115, 4963, 10.1182/blood-2010-01-262386 Zhong, 2010, Protein S protects neurons from excitotoxic injury by activating the TAM receptor Tyro3-phosphatidylinositol 3-kinase-Akt pathway through its sex hormone-binding globulin-like region., J Neurosci, 30, 15521, 10.1523/JNEUROSCI.4437-10.2010 Griffin, 2015, Activated protein C: biased for translation., Blood, 125, 2898, 10.1182/blood-2015-02-355974 Abrams, 2011, Framing postpartum hemorrhage as a consequence of human placental biology: an evolutionary and comparative perspective., Am Anthropol, 113, 417, 10.1111/j.1548-1433.2011.01351.x