Meta-analysis of 65,734 individuals identifies TSPAN15 and SLC44A2 as two susceptibility loci for venous thromboembolism

American Journal of Human Genetics

Volumn 96, Issue 4, 2015, Pages 532-542

  Germain, Marine ^a,b,c   Chasman, Daniel I ^d   De Haan, Hugoline ^e   Tang, Weihong ^f   Lindström, Sara ^g   Weng, Lu Chen ^f   De Andrade, Mariza ^h   De Visser, Marieke C H ^e   Wiggins, Kerri L ⁱ   Suchon, Pierre ^a,j,k   Saut, Noémie ^a,j,k   Smadja, David M ^a,l,m   Le Gal, Grégoire ^n,o   Van Hylckama Vlieg, Astrid ^e   Di Narzo, Antonio ^p   Hao, Ke ^p   Nelson, Christopher P ^q,r   Rocanin Arjo, Ares ^a,b,c   Folkersen, Lasse ^s   Monajemi, Ramin ^e   Rose, Lynda M ^t   Brody, Jennifer A ^u   Slagboom, Eline ^e   Aïssi, Dylan ^a,b,c   Gagnon, France ^v   Deleuze, Jean Francois ^w   Deloukas, Panos ^x,y   Tzourio, Christophe ^z   Dartigues, Jean Francois ^z   Berr, Claudine ^a   Taylor, Kent D ^aa   Civelek, Mete ^ab   Eriksson, Per ^ac   Psaty, Bruce M ^u,ad   Houwing Duitermaat, Jeanine ^e   Goodall, Alison H ^q,r   Cambien, François ^a,b,c   Kraft, Peter ^g   Amouyel, Philippe ^ae,af   Samani, Nilesh J ^q,r   Basu, Saonli ^f   Ridker, Paul M ^d   Rosendaal, Frits R ^e   Kabrhel, Christopher ^d   Folsom, Aaron R ^f   Heit, John ^h   Reitsma, Pieter H ^e   Trégouët, David Alexandre ^a,b,c   Smith, Nicholas L ^i,ad,ag   Morange, Pierre Emmanuel ^a,j,k   more..

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c Institute of Cardiometabolism and Nutrition (ICAN)   (France)

^d HARVARD MEDICAL SCHOOL   (United States)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF MINNESOTA   (United States)

^g HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^h MAYO CLINIC   (United States)

ⁱ UNIVERSITY OF WASHINGTON   (United States)

^j TIMONE HOSPITAL   (France)

^k AIX MARSEILLE UNIVERSITY   (France)

^l UNIVERSITÉ PARIS DESCARTES   (France)

^m HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

ⁿ UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

^o OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^p MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^q UNIVERSITY OF LEICESTER   (United Kingdom)

^r Queen Mary University of London and Barts NIHR BRC NHS Trust National Institute for Health and Care Research   (United Kingdom)

^s University of Leicester ^*  (Denmark)

^t BRIGHAM AND WOMEN S HOSPITAL   (United States)

^u UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^v UNIVERSITY OF TORONTO   (Canada)

^w CENTRE NATIONAL DE GÉNOTYPAGE   (France)

^x QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^y KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^z UNIVERSITÉ DE BORDEAUX   (France)

^aa HARBOR UCLA MEDICAL CENTER   (United States)

^ab UNIVERSITY OF CALIFORNIA   (United States)

^ac KAROLINSKA INSTITUTE   (Sweden)

^ad CENTER FOR HEALTH STUDIES   (United States)

^ae UNIV LILLE   (France)

^af LILLE UNIVERSITY HOSPITAL   (France)

^ag Seattle Epidemiologic Research and Information Center   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; GENE; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HUMAN; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SLC44A2 GENE; TRANSFUSION RELATED ACUTE LUNG INJURY; TSPAN15 GENE; VENOUS THROMBOEMBOLISM; GENETIC PREDISPOSITION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; META ANALYSIS; ODDS RATIO;

CARRIER PROTEIN; MEMBRANE PROTEIN; SLC44A2 PROTEIN, HUMAN; TETRASPANIN; TSPAN15 PROTEIN, HUMAN;

GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; ODDS RATIO; TETRASPANINS; VENOUS THROMBOEMBOLISM;

EID: 84926245873     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2015.01.019     Document Type: Article

References (57)

1. I.A. Naess, S.C. Christiansen, P. Romundstad, S.C. Cannegieter, F.R. Rosendaal, and J. Hammerstrøm Incidence and mortality of venous thrombosis: a population-based study J. Thromb. Haemost. 5 2007 692 699
2. R. Virchow Gesammelte Abhandlungen zur Wissenschaftlichen Medizin 1856 Meidinger Frankfurt
3. J.A. Heit, M.A. Phelps, S.A. Ward, J.P. Slusser, T.M. Petterson, and M. De Andrade Familial segregation of venous thromboembolism J. Thromb. Haemost. 2 2004 731 736
4. B. Zöller, X. Li, J. Sundquist, and K. Sundquist Age- and gender-specific familial risks for venous thromboembolism: a nationwide epidemiological study based on hospitalizations in Sweden Circulation 124 2011 1012 1020
5. W. Tang, M. Teichert, D.I. Chasman, J.A. Heit, P.-E. Morange, G. Li, N. Pankratz, F.W. Leebeek, G. Paré, and M. de Andrade A genome-wide association study for venous thromboembolism: the extended cohorts for heart and aging research in genomic epidemiology (CHARGE) consortium Genet. Epidemiol. 37 2013 512 521
6. M. Germain, N. Saut, T. Oudot-Mellakh, L. Letenneur, A.-M. Dupuy, M. Bertrand, M.C. Alessi, J.C. Lambert, D. Zelenika, and J. Emmerich Caution in interpreting results from imputation analysis when linkage disequilibrium extends over a large distance: a case study on venous thrombosis PLoS ONE 7 2012 e38538
7. P.E. Morange, and D.A. Trégouët Current knowledge on the genetics of incident venous thrombosis J. Thromb. Haemost. 11 1 2013 111 121
8. The ARIC investigators The Atherosclerosis Risk in Communities (ARIC) Study: design and objectives. The ARIC investigators Am. J. Epidemiol. 129 1989 687 702
9. L.P. Fried, N.O. Borhani, P. Enright, C.D. Furberg, J.M. Gardin, R.A. Kronmal, L.H. Kuller, T.A. Manolio, M.B. Mittelmark, and A. Newman The Cardiovascular Health Study: design and rationale Ann. Epidemiol. 1 1991 263 276
10. G.S. Tell, L.P. Fried, B. Hermanson, T.A. Manolio, A.B. Newman, and N.O. Borhani Recruitment of adults 65 years and older as participants in the Cardiovascular Health Study Ann. Epidemiol. 3 1993 358 366
11. D.-A. Trégouët, S. Heath, N. Saut, C. Biron-Andreani, J.-F. Schved, G. Pernod, P. Galan, L. Drouet, D. Zelenika, and I. Juhan-Vague 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 2009 5298 5303
12. M.C.H. de Visser, R. van Minkelen, V. van Marion, M. den Heijer, J. Eikenboom, H.L. Vos, P.E. Slagboom, J.J. Houwing-Duistermaat, F.R. Rosendaal, and R.M. Bertina Genome-wide linkage scan in affected sibling pairs identifies novel susceptibility region for venous thromboembolism: Genetics In Familial Thrombosis study J. Thromb. Haemost. 11 2013 1474 1484
13. B.M. Psaty, S.R. Heckbert, T.D. Koepsell, D.S. Siscovick, T.E. Raghunathan, N.S. Weiss, F.R. Rosendaal, R.N. Lemaitre, N.L. Smith, and P.W. Wahl The risk of myocardial infarction associated with antihypertensive drug therapies JAMA 274 1995 620 625
14. M. Germain, N. Saut, N. Greliche, C. Dina, J.-C. Lambert, C. Perret, W. Cohen, T. Oudot-Mellakh, G. Antoni, and M.C. Alessi Genetics of venous thrombosis: insights from a new genome wide association study PLoS ONE 6 2011 e25581
15. J.A. Heit, S.M. Armasu, Y.W. Asmann, J.M. Cunningham, M.E. Matsumoto, T.M. Petterson, and M. De Andrade A genome-wide association study of venous thromboembolism identifies risk variants in chromosomes 1q24.2 and 9q J. Thromb. Haemost. 10 2012 1521 1531
16. J.W. Blom, C.J.M. Doggen, S. Osanto, and F.R. Rosendaal Malignancies, prothrombotic mutations, and the risk of venous thrombosis JAMA 293 2005 715 722
17. S.E. Hankinson, G.A. Colditz, D.J. Hunter, J.E. Manson, W.C. Willett, M.J. Stampfer, C. Longcope, and F.E. Speizer Reproductive factors and family history of breast cancer in relation to plasma estrogen and prolactin levels in postmenopausal women in the Nurses' Health Study (United States) Cancer Causes Control 6 1995 217 224
18. S.S. Tworoger, P. Sluss, and S.E. Hankinson Association between plasma prolactin concentrations and risk of breast cancer among predominately premenopausal women Cancer Res. 66 2006 2476 2482
19. P.M. Ridker, D.I. Chasman, R.Y.L. Zee, A. Parker, L. Rose, N.R. Cook, J.E. Buring Women's Genome Health Study Working Group Rationale, design, and methodology of the Women's Genome Health Study: a genome-wide association study of more than 25,000 initially healthy american women Clin. Chem. 54 2008 249 255
20. E. Oger, K. Lacut, G. Le Gal, F. Couturaud, D. Guénet, J.-H. Abalain, A.M. Roguedas, D. Mottier EDITH COLLABORATIVE STUDY GROUP Hyperhomocysteinemia and low B vitamin levels are independently associated with venous thromboembolism: results from the EDITH study: a hospital-based case-control study J. Thromb. Haemost. 4 2006 793 799
21. E.O. Johnson, D.B. Hancock, J.L. Levy, N.C. Gaddis, N.L. Saccone, L.J. Bierut, and G.P. Page Imputation across genotyping arrays for genome-wide association studies: assessment of bias and a correction strategy Hum. Genet. 132 2013 509 522
22. C.J. Willer, Y. Li, and G.R. Abecasis METAL: fast and efficient meta-analysis of genomewide association scans Bioinformatics 26 2010 2190 2191
23. M.-X. Li, J.M.Y. Yeung, S.S. Cherny, and P.C. Sham Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets Hum. Genet. 131 2012 747 756
24. O.A. Panagiotou, J.P.A. Ioannidis Genome-Wide Significance Project What should the genome-wide significance threshold be? Empirical replication of borderline genetic associations Int. J. Epidemiol. 41 2012 273 286
25. A.D. Skol, L.J. Scott, G.R. Abecasis, and M. Boehnke Joint analysis is more efficient than replication-based analysis for two-stage genome-wide association studies Nat. Genet. 38 2006 209 213
26. N.L. Smith, M.H. Chen, A. Dehghan, D.P. Strachan, S. Basu, N. Soranzo, C. Hayward, I. Rudan, M. Sabater-Lleal, J.C. Bis Wellcome Trust Case Control Consortium 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 2010 1382 1392
27. Y. Li, I.D. Bezemer, C.M. Rowland, C.H. Tong, A.R. Arellano, J.J. Catanese, J.J. Devlin, P.H. Reitsma, L.A. Bare, and F.R. Rosendaal Genetic variants associated with deep vein thrombosis: the F11 locus J. Thromb. Haemost. 7 2009 1802 1808
28. A. Rocanin-Arjo, W. Cohen, L. Carcaillon, C. Frère, N. Saut, L. Letenneur, M. Alhenc-Gelas, A.M. Dupuy, M. Bertrand, M.C. Alessi CardioGenics Consortium A meta-analysis of genome-wide association studies identifies ORM1 as a novel gene controlling thrombin generation potential Blood 123 2014 777 785
29. T. Oudot-Mellakh, W. Cohen, M. Germain, N. Saut, C. Kallel, D. Zelenika, M. Lathrop, D.A. Trégouët, and P.E. Morange Genome wide association study for plasma levels of natural anticoagulant inhibitors and protein C anticoagulant pathway: the MARTHA project Br. J. Haematol. 157 2012 230 239
30. M. Sabater-Lleal, J. Huang, D. Chasman, S. Naitza, A. Dehghan, A.D. Johnson, A. Teumer, A.P. Reiner, L. Folkersen, S. Basu VTE Consortium STROKE Consortium Wellcome Trust Case Control Consortium 2 (WTCCC2) C4D Consortium CARDIoGRAM Consortium Multiethnic meta-analysis of genome-wide association studies in >100 000 subjects identifies 23 fibrinogen-associated loci but no strong evidence of a causal association between circulating fibrinogen and cardiovascular disease Circulation 128 2013 1310 1324
31. N.L. Smith, J.E. Huffman, D.P. Strachan, J. Huang, A. Dehghan, S. Trompet, L.M. Lopez, S.Y. Shin, J. Baumert, and V. Vitart Genetic predictors of fibrin D-dimer levels in healthy adults Circulation 123 2011 1864 1872
32. W. Tang, C. Schwienbacher, L.M. Lopez, Y. Ben-Shlomo, T. Oudot-Mellakh, A.D. Johnson, N.J. Samani, S. Basu, M. Gögele, and G. Davies Genetic associations for activated partial thromboplastin time and prothrombin time, their gene expression profiles, and risk of coronary artery disease Am. J. Hum. Genet. 91 2012 152 162
33. W. Tang, S. Basu, X. Kong, J.S. Pankow, N. Aleksic, A. Tan, M. Cushman, E. Boerwinkle, and A.R. Folsom Genome-wide association study identifies novel loci for plasma levels of protein C: the ARIC study Blood 116 2010 5032 5036
34. W.J. Gauderman Sample size requirements for matched case-control studies of gene-environment interaction Stat. Med. 21 2002 35 50
35. B.P. Fairfax, S. Makino, J. Radhakrishnan, K. Plant, S. Leslie, A. Dilthey, P. Ellis, C. Langford, F.O. Vannberg, and J.C. Knight Genetics of gene expression in primary immune cells identifies cell type-specific master regulators and roles of HLA alleles Nat. Genet. 44 2012 502 510
36. A. Erbilgin, M. Civelek, C.E. Romanoski, C. Pan, R. Hagopian, J.A. Berliner, and A.J. Lusis Identification of CAD candidate genes in GWAS loci and their expression in vascular cells J. Lipid Res. 54 2013 1894 1905
37. GTEx Consortium The Genotype-Tissue Expression (GTEx) project Nat. Genet. 45 2013 580 585
38. L. Folkersen, F. van't Hooft, E. Chernogubova, H.E. Agardh, G.K. Hansson, U. Hedin, J. Liska, A.C. Syvänen, G. Paulsson-Berne, A. Franco-Cereceda BiKE and ASAP study groups Association of genetic risk variants with expression of proximal genes identifies novel susceptibility genes for cardiovascular disease Circ Cardiovasc Genet 3 2010 365 373
39. B. Kabakchiev, and M.S. Silverberg Expression quantitative trait loci analysis identifies associations between genotype and gene expression in human intestine Gastroenterology 144 2013 1488 1496, e1-e3
40. E.E. Schadt, C. Molony, E. Chudin, K. Hao, X. Yang, P.Y. Lum, A. Kasarskis, B. Zhang, S. Wang, and C. Suver Mapping the genetic architecture of gene expression in human liver PLoS Biol. 6 2008 e107
41. S. Garnier, V. Truong, J. Brocheton, T. Zeller, M. Rovital, P.S. Wild, A. Ziegler, T. Munzel, L. Tiret, S. Blankenberg Cardiogenics Consortium Genome-wide haplotype analysis of cis expression quantitative trait loci in monocytes PLoS Genet. 9 2013 e1003240
42. B.P. Fairfax, P. Humburg, S. Makino, V. Naranbhai, D. Wong, E. Lau, L. Jostins, K. Plant, R. Andrews, C. McGee, and J.C. Knight Innate immune activity conditions the effect of regulatory variants upon monocyte gene expression Science 343 2014 1246949
43. K.J. Dick, C.P. Nelson, L. Tsaprouni, J.K. Sandling, D. Aïssi, S. Wahl, E. Meduri, P.-E. Morange, F. Gagnon, and H. Grallert DNA methylation and body-mass index: a genome-wide analysis Lancet 383 2014 1990 1998
44. H.J. Westra, M.J. Peters, T. Esko, H. Yaghootkar, C. Schurmann, J. Kettunen, M.W. Christiansen, B.P. Fairfax, K. Schramm, and J.E. Powell Systematic identification of trans eQTLs as putative drivers of known disease associations Nat. Genet. 45 2013 1238 1243
45. A.D. Johnson, R.E. Handsaker, S.L. Pulit, M.M. Nizzari, C.J. O'Donnell, and P.I. de Bakker SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap Bioinformatics 24 2008 2938 2939
46. L.D. Ward, and M. Kellis HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants Nucleic Acids Res. 40 2012 D930 D934
47. M. Barenboim, and T. Manke ChroMoS: an integrated web tool for SNP classification, prioritization and functional interpretation Bioinformatics 29 2013 2197 2198
48. A.P. Boyle, E.L. Hong, M. Hariharan, Y. Cheng, M.A. Schaub, M. Kasowski, K.J. Karczewski, J. Park, B.C. Hitz, and S. Weng Annotation of functional variation in personal genomes using RegulomeDB Genome Res. 22 2012 1790 1797
49. F. Berditchevski Complexes of tetraspanins with integrins: more than meets the eye J. Cell Sci. 114 2001 4143 4151
50. L.-M. Lau, J.L. Wee, M.D. Wright, G.W. Moseley, P.M. Hogarth, L.K. Ashman, and D.E. Jackson The tetraspanin superfamily member CD151 regulates outside-in integrin alphaIIbbeta3 signaling and platelet function Blood 104 2004 2368 2375
51. M.W. Goschnick, L.-M. Lau, J.L. Wee, Y.S. Liu, P.M. Hogarth, L.M. Robb, M.J. Hickey, M.D. Wright, and D.E. Jackson Impaired "outside-in" integrin alphaIIbbeta3 signaling and thrombus stability in TSSC6-deficient mice Blood 108 2006 1911 1918
52. R.L. Bailey, J.M. Herbert, K. Khan, V.L. Heath, R. Bicknell, and M.G. Tomlinson The emerging role of tetraspanin microdomains on endothelial cells Biochem. Soc. Trans. 39 2011 1667 1673
53. M. Poeter, I. Brandherm, J. Rossaint, G. Rosso, V. Shahin, B.V. Skryabin, A. Zarbock, V. Gerke, and U. Rescher Annexin A8 controls leukocyte recruitment to activated endothelial cells via cell surface delivery of CD63 Nat. Commun. 5 2014 3738
54. E. Traiffort, S. O'Regan, and M. Ruat The choline transporter-like family SLC44: properties and roles in human diseases Mol. Aspects Med. 34 2013 646 654
55. A. Greinacher, J. Wesche, E. Hammer, B. Fürll, U. Völker, A. Reil, and J. Bux Characterization of the human neutrophil alloantigen-3a Nat. Med. 16 2010 45 48
56. B.R. Curtis, N.J. Cox, M.J. Sullivan, A. Konkashbaev, K. Bowens, K. Hansen, and R.H. Aster The neutrophil alloantigen HNA-3a (5b) is located on choline transporter-like protein 2 and appears to be encoded by an R>Q154 amino acid substitution Blood 115 2010 2073 2076
57. B. Bayat, Y. Tjahjono, A. Sydykov, S. Werth, S. Hippenstiel, N. Weissmann, U.J. Sachs, and S. Santoso Anti-human neutrophil antigen-3a induced transfusion-related acute lung injury in mice by direct disturbance of lung endothelial cells Arterioscler. Thromb. Vasc. Biol. 33 2013 2538 2548