Genome wide association study for plasma levels of natural anticoagulant inhibitors and protein C anticoagulant pathway: The MARTHA project

British Journal of Haematology

Volumn 157, Issue 2, 2012, Pages 230-239

  Oudot Mellakh, Tiphaine ^a   Cohen, William ^a,b   Germain, Marine ^a   Saut, Noémie ^a,b   Kallel, Choumous ^a,b   Zelenika, Diana ^c   Lathrop, Mark ^c   Trégouët, David Alexandre ^a   Morange, Pierre Emmanuel ^a,b  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c CENTRE NATIONAL DE GÉNOTYPAGE   (France)

Author keywords

Antithrombin Protein C; Genome wide association study; Protein S; Venous thrombosis

Indexed keywords

ANTITHROMBIN; GLYCINE; PROTEIN C; PROTEIN S; SERINE; SNAKE VENOM;

ADULT; AMINO ACID SUBSTITUTION; ARTICLE; CAUCASIAN; CHROMOSOME 1Q; CHROMOSOME 20Q; CONTROLLED STUDY; EDEM2 GENE; EIF2S2 GENE; ENZYME LINKED IMMUNOSORBENT ASSAY; FAM83C GENE; FEMALE; GDF5 GENE; GENE; GENE LOCUS; GENE MAPPING; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; GSS GENE; HUMAN; ITCH GENE; LOC729547 GENE; MAJOR CLINICAL STUDY; MALE; MMP24 GENE; MYH7B GENE; PRIORITY JOURNAL; PROCR GENE; SINGLE NUCLEOTIDE POLYMORPHISM; VEIN THROMBOSIS;

ADULT; ANTIGENS, CD; ANTITHROMBIN PROTEINS; BLOOD COAGULATION; CROTALID VENOMS; FEMALE; GENETIC LOCI; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN C; PROTEIN S; RECEPTORS, CELL SURFACE; RETROSPECTIVE STUDIES; RISK FACTORS; VENOUS THROMBOSIS;

EID: 84859215724     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2011.09025.x     Document Type: Article

References (38)

1. Almasy, L., Soria, J.M., Souto, J.C., Coll, I., Bacq, D., Faure, A., Mateo, J., Borrell, M., Munoz, X., Sala, N., Stone, W.H., Lathrop, M., Fontcuberta, J. & Blangero, J. (2003) A quantitative trait locus influencing free plasma protein S levels on human chromosome 1q: results from the Genetic Analysis of Idiopathic Thrombophilia (GAIT) project. Arteriosclerosis, Thrombosis, and Vascular Biology, 23, 508-511.
2. Antoni, G., Oudot-Mellakh, T., Dimitromanolakis, A., Germain, M., Cohen, W., Wells, P., Lathrop, M., Gagnon, F., Morange, P.E. & Tregouet, D.A. (2011) Combined analysis of three genome-wide association studies on vWF and FVIII plasma levels. BMC Medical Genetics, 12, 102.
3. Barrett, J.C., Fry, B., Maller, J. & Daly, M.J. (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics, 21, 263-265.
4. Buil, A., Soria, J.M., Souto, J.C., Almasy, L., Lathrop, M., Blangero, J. & Fontcuberta, J. (2004) Protein C levels are regulated by a quantitative trait locus on chromosome 16: results from the Genetic Analysis of Idiopathic Thrombophilia (GAIT) Project. Arteriosclerosis, Thrombosis, and Vascular Biology, 24, 1321-1325.
5. Castoldi, E. & Rosing, J. (2010) APC resistance: biological basis and acquired influences. Journal of Thrombosis and Haemostasis, 8, 445-453.
6. Egeberg, O. (1965) Inherited antithrombin deficiency causing Thrombophilia. Thromb Diath Haemorrh, 13, 516-530.
7. Germain, M., Saut, N., Greliche, N., Dina, C., Lambert, J.C., Perret, C., Cohen, W., Oudot-Mellakh, T., Antoni, G., Alessi, M.C., Zelenika, D., Cambien, F., Tiret, L., Bertrand, M., Dupuy, A.M., Letenneur, L., Lathrop, M., Emmerich, J., Amouyel, P., Tregouet, D.A. & Morange, P.E. (2011) Genetics of venous thrombosis: insights from a new genome wide association study. PLoS ONE, 6, e25581.
8. Griffin, J.H., Evatt, B., Zimmerman, T.S., Kleiss, A.J. & Wideman, C. (1981) Deficiency of protein C in congenital thrombotic disease. Journal of Clinical Investigation, 68, 1370-1373.
9. Houlihan, L.M., Davies, G., Tenesa, A., Harris, S.E., Luciano, M., Gow, A.J., McGhee, K.A., Liewald, D.C., Porteous, D.J., Starr, J.M., Lowe, G.D., Visscher, P.M. & Deary, I.J. (2010) Common variants of large effect in F12, KNG1, and HRG are associated with activated partial thromboplastin time. American Journal of Human Genetics, 86, 626-631.
10. Ireland, H.A., Cooper, J.A., Drenos, F., Acharya, J., Mitchell, J.P., Bauer, K.A., Morrissey, J.H., Esnouf, M.P. & Humphries, S.E. (2009) FVII, FVIIa, and downstream markers of extrinsic pathway activation differ by EPCR Ser219Gly variant in healthy men. Arteriosclerosis, Thrombosis, and Vascular Biology, 29, 1968-1974.
11. Johnson, A.D., Handsaker, R.E., Pulit, S.L., Nizzari, M.M., O'Donnell, C.J. & de Bakker, P.I. (2008) SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics, 24, 2938-2939.
12. Morange, P.E. & Tregouet, D.A. (2010) Deciphering the molecular basis of venous thromboembolism: where are we and where should we go? British Journal of Haematology, 148, 495-506.
13. Morange, P.E. & Tregouet, D.A. (2011) Lessons from genome-wide association studies in venous thrombosis. Journal of Thrombosis and Haemostasis, 9(Suppl 1), 258-264.
14. Morange, P.E., Oudot-Mellakh, T., Cohen, W., Germain, M., Saut, N., Antoni, G., Alessi, M.C., Bertrand, M., Dupuy, A.M., Letenneur, L., Lathrop, M., Lopez, L.M., Lambert, J.C., Emmerich, J., Amouyel, P. & Tregouet, D.A. (2011) KNG1 Ile581Thr and susceptibility to venous thrombosis. Blood, 117, 3692-3694.
15. Peng, B., Yu, R.K., Dehoff, K.L. & Amos, C.I. (2007) Normalizing a large number of quantitative traits using empirical normal quantile transformation. BMC Proceedings, 1(Suppl 1), S156.
16. Pintao, M.C., Roshani, S., de Visser, M.C., Tieken, C., Tanck, M.W., Wichers, I.M., Meijers, J.C., Rosendaal, F.R., Middeldorp, S. & Reitsma, P.H. (2011) High levels of protein C are determined by PROCR haplotype 3. Journal of Thrombosis and Haemostasis, 9, 969-976.
17. Pomp, E.R., Doggen, C.J., Vos, H.L., Reitsma, P.H. & Rosendaal, F.R. (2009) Polymorphisms in the protein C gene as risk factor for venous thrombosis. Thrombosis and Haemostasis, 101, 62-67.
18. Price, A.L., Patterson, N.J., Plenge, R.M., Weinblatt, M.E., Shadick, N.A. & Reich, D. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics, 38, 904-909.
19. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A., Bender, D., Maller, J., Sklar, P., de Bakker, P.I., Daly, M.J. & Sham, P.C. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81, 559-575.
20. Qu, D., Wang, Y., Song, Y., Esmon, N.L. & Esmon, C.T. (2006) The Ser219->Gly dimorphism of the endothelial protein C receptor contributes to the higher soluble protein levels observed in individuals with the A3 haplotype. Journal of Thrombosis and Haemostasis, 4, 229-235.
21. Reiner, A.P., Carty, C.L., Jenny, N.S., Nievergelt, C., Cushman, M., Stearns-Kurosawa, D.J., Kurosawa, S., Kuller, L.H. & Lange, L.A. (2008) PROC, PROCR and PROS1 polymorphisms, plasma anticoagulant phenotypes, and risk of cardiovascular disease and mortality in older adults: the Cardiovascular Health Study. Journal of Thrombosis and Haemostasis, 6, 1625-1632.
22. Robert, A., Eschwege, V., Hameg, H., Drouet, L. & Aillaud, M.F. (1996) Anticoagulant response to Agkistrodon contortrix venom (ACV test): a new global test to screen for defects in the anticoagulant protein C pathway. Thrombosis and Haemostasis, 75, 562-566.
23. Robert, A., Aillaud, M.F., Eschwege, V., Verdy, E., Barthet, M.C., Morange, P.E. & Juhan-Vague, I. (1999) Screening for identified and unidentified protein C pathway defects by the Agkistrodon contortrix venom test in consecutive patients. American Journal of Clinical Pathology, 112, 233-237.
24. Saposnik, B., Reny, J.L., Gaussem, P., Emmerich, J., Aiach, M. & Gandrille, S. (2004) A haplotype of the EPCR gene is associated with increased plasma levels of sEPCR and is a candidate risk factor for thrombosis. Blood, 103, 1311-1318.
25. Saposnik, B., Lesteven, E., Lokajczyk, A., Esmon, C.T., Aiach, M. & Gandrille, S. (2008) Alternative mRNA is favored by the A3 haplotype of the EPCR gene PROCR and generates a novel soluble form of EPCR in plasma. Blood, 111, 3442-3451.
26. Schwarz, H.P., Fischer, M., Hopmeier, P., Batard, M.A. & Griffin, J.H. (1984) Plasma protein S deficiency in familial thrombotic disease. Blood, 64, 1297-1300.
27. Simioni, P., Morboeuf, O., Tognin, G., Gavasso, S., Tormene, D., Woodhams, B. & Pagnan, A. (2006) Soluble endothelial protein C receptor (sEPCR) levels and venous thromboembolism in carriers of two dysfunctional protein C variants. Thrombosis Research, 117, 523-528.
28. Smith, N.L., Chen, M.H., Dehghan, A., Strachan, D.P., Basu, S., Soranzo, N., Hayward, C., Rudan, I., Sabater-Lleal, M., Bis, J.C., de Maat, M.P., Rumley, A., Kong, X., Yang, Q., Williams, F.M., Vitart, V., Campbell, H., Malarstig, A., Wiggins, K.L., Van Duijn, C.M., McArdle, W.L., Pankow, J.S., Johnson, A.D., Silveira, A., McKnight, B., Uitterlinden, A.G., Aleksic, N., Meigs, J.B., Peters, A., Koenig, W., Cushman, M., Kathiresan, S., Rotter, J.I., Bovill, E.G., Hofman, A., Boerwinkle, E., Tofler, G.H., Peden, J.F., Psaty, B.M., Leebeek, F., Folsom, A.R., Larson, M.G., Spector, T.D., Wright, A.F., Wilson, J.F., Hamsten, A., Lumley, T., Witteman, J.C., Tang, W. & O'Donnell, C.J. (2010) Novel associations of multiple genetic loci with plasma levels of factor VII, factor VIII, and von Willebrand factor: the CHARGE (Cohorts for Heart and Aging Research in Genome Epidemiology) Consortium. Circulation, 121, 1382-1392.
29. Soria, J.M. & Fontcuberta, J. (2005) New approaches and future prospects for evaluating genetic risk of thrombosis. Haematologica, 90, 1212-1222.
30. Tang, W., Basu, S., Kong, X., Pankow, J.S., Aleksic, N., Tan, A., Cushman, M., Boerwinkle, E. & Folsom, A.R. (2010) Genome-wide association study identifies novel loci for plasma levels of protein C: the ARIC study. Blood, 116, 5032-5036.
31. Tregouet, D.A. & Garelle, V. (2007) A new JAVA interface implementation of THESIAS: testing haplotype effects in association studies. Bioinformatics, 23, 1038-1039.
32. Tregouet, D.A., Heath, S., Saut, N., Biron-Andreani, C., Schved, J.F., Pernod, G., Galan, P., Drouet, L., Zelenika, D., Juhan-Vague, I., Alessi, M.C., Tiret, L., Lathrop, M., Emmerich, J. & Morange, P.E. (2009) Common susceptibility alleles are unlikely to contribute as strongly as the FV and ABO loci to VTE risk: results from a GWAS approach. Blood, 113, 5298-5303.
33. Uitte de Willige, S., Van Marion, V., Rosendaal, F.R., Vos, H.L., de Visser, M.C. & Bertina, R.M. (2004) Haplotypes of the EPCR gene, plasma sEPCR levels and the risk of deep venous thrombosis. Journal of Thrombosis and Haemostasis, 2, 1305-1310.
34. Van Walderveen, M.C., Berry, L.R., Atkinson, H.M. & Chan, A.K. (2010) Covalent antithrombin-heparin effect on thrombin-thrombomodulin and activated protein C reaction with factor V/Va. Thrombosis and Haemostasis, 103, 910-919.
35. Walker, F.J. (1981) Regulation of activated protein C by protein S. The role of phospholipid in factor Va inactivation. Journal of Biological Chemistry, 256, 11128-11131.
36. Walker, F.J., Chavin, S.I. & Fay, P.J. (1987) Inactivation of factor VIII by activated protein C and protein S. Archives of Biochemistry and Biophysics, 252, 322-328.
37. Yang, J., Benyamin, B., McEvoy, B.P., Gordon, S., Henders, A.K., Nyholt, D.R., Madden, P.A., Heath, A.C., Martin, N.G., Montgomery, G.W., Goddard, M.E. & Visscher, P.M. (2010) Common SNPs explain a large proportion of the heritability for human height. Nature Genetics, 42, 565-569.
38. Yang, J., Lee, S.H., Goddard, M.E. & Visscher, P.M. (2011) GCTA: a tool for genome-wide complex trait analysis. American Journal of Human Genetics, 88, 76-82.