Antithrombin, Protein C, and Protein S: Genome and Transcriptome-Wide Association Studies Identify 7 Novel Loci Regulating Plasma Levels.


Journal

Arteriosclerosis, thrombosis, and vascular biology
ISSN: 1524-4636
Titre abrégé: Arterioscler Thromb Vasc Biol
Pays: United States
ID NLM: 9505803

Informations de publication

Date de publication:
07 2023
Historique:
pmc-release: 01 07 2024
medline: 23 6 2023
pubmed: 2 5 2023
entrez: 2 5 2023
Statut: ppublish

Résumé

Antithrombin, PC (protein C), and PS (protein S) are circulating natural anticoagulant proteins that regulate hemostasis and of which partial deficiencies are causes of venous thromboembolism. Previous genetic association studies involving antithrombin, PC, and PS were limited by modest sample sizes or by being restricted to candidate genes. In the setting of the Cohorts for Heart and Aging Research in Genomic Epidemiology consortium, we meta-analyzed across ancestries the results from 10 genome-wide association studies of plasma levels of antithrombin, PC, PS free, and PS total. Study participants were of European and African ancestries, and genotype data were imputed to TOPMed, a dense multiancestry reference panel. Each of the 10 studies conducted a genome-wide association studies for each phenotype and summary results were meta-analyzed, stratified by ancestry. Analysis of antithrombin included 25 243 European ancestry and 2688 African ancestry participants, PC analysis included 16 597 European ancestry and 2688 African ancestry participants, PSF and PST analysis included 4113 and 6409 European ancestry participants. We also conducted transcriptome-wide association analyses and multiphenotype analysis to discover additional associations. Novel genome-wide association studies and transcriptome-wide association analyses findings were validated by in vitro functional experiments. Mendelian randomization was performed to assess the causal relationship between these proteins and cardiovascular outcomes. Genome-wide association studies meta-analyses identified 4 newly associated loci: 3 with antithrombin levels ( The use of larger sample sizes, diverse populations, and a denser imputation reference panel allowed the detection of 7 novel genomic loci associated with plasma antithrombin, PC, and PS levels.

Sections du résumé

BACKGROUND
Antithrombin, PC (protein C), and PS (protein S) are circulating natural anticoagulant proteins that regulate hemostasis and of which partial deficiencies are causes of venous thromboembolism. Previous genetic association studies involving antithrombin, PC, and PS were limited by modest sample sizes or by being restricted to candidate genes. In the setting of the Cohorts for Heart and Aging Research in Genomic Epidemiology consortium, we meta-analyzed across ancestries the results from 10 genome-wide association studies of plasma levels of antithrombin, PC, PS free, and PS total.
METHODS
Study participants were of European and African ancestries, and genotype data were imputed to TOPMed, a dense multiancestry reference panel. Each of the 10 studies conducted a genome-wide association studies for each phenotype and summary results were meta-analyzed, stratified by ancestry. Analysis of antithrombin included 25 243 European ancestry and 2688 African ancestry participants, PC analysis included 16 597 European ancestry and 2688 African ancestry participants, PSF and PST analysis included 4113 and 6409 European ancestry participants. We also conducted transcriptome-wide association analyses and multiphenotype analysis to discover additional associations. Novel genome-wide association studies and transcriptome-wide association analyses findings were validated by in vitro functional experiments. Mendelian randomization was performed to assess the causal relationship between these proteins and cardiovascular outcomes.
RESULTS
Genome-wide association studies meta-analyses identified 4 newly associated loci: 3 with antithrombin levels (
CONCLUSIONS
The use of larger sample sizes, diverse populations, and a denser imputation reference panel allowed the detection of 7 novel genomic loci associated with plasma antithrombin, PC, and PS levels.

Identifiants

pubmed: 37128921
doi: 10.1161/ATVBAHA.122.318213
pmc: PMC10330350
mid: NIHMS1893756
doi:

Substances chimiques

Protein C 0
Protein S 0
Antithrombins 0
Anticoagulants 0
Antithrombin III 9000-94-6

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

e254-e269

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL139553
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL105756
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL126974
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL141291
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL141399
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL134894
Pays : United States

Commentaires et corrections

Type : CommentIn

Références

Nat Med. 2019 Aug;25(8):1274-1279
pubmed: 31285632
Nat Genet. 2015 Oct;47(10):1121-1130
pubmed: 26343387
Nat Genet. 2015 Sep;47(9):1091-8
pubmed: 26258848
Genet Epidemiol. 2018 Mar;42(2):134-145
pubmed: 29226385
PLoS One. 2011;6(7):e21851
pubmed: 21765920
PLoS Genet. 2019 Dec 23;15(12):e1008500
pubmed: 31869403
Circulation. 2000 Apr 4;101(13):1546-51
pubmed: 10747348
Nat Genet. 2013 Jan;45(1):25-33
pubmed: 23202125
Haematologica. 2005 Nov;90(11):1557-61
pubmed: 16266904
Nat Protoc. 2014 May;9(5):1192-212
pubmed: 24762786
BMC Med Genet. 2011 Aug 02;12:102
pubmed: 21810271
PLoS One. 2019 Apr 30;14(4):e0215911
pubmed: 31039173
Blood. 2014 Jan 30;123(5):777-85
pubmed: 24357727
Genet Epidemiol. 2016 May;40(4):304-14
pubmed: 27061298
Nat Genet. 2019 Apr;51(4):675-682
pubmed: 30926970
Am J Epidemiol. 1989 Apr;129(4):687-702
pubmed: 2646917
J Transl Med. 2015 Nov 05;13:348
pubmed: 26541195
Br Med J (Clin Res Ed). 1984 Nov 3;289(6453):1192
pubmed: 6437481
Nat Commun. 2022 Mar 9;13(1):1222
pubmed: 35264566
Circ Cardiovasc Genet. 2009 Feb;2(1):73-80
pubmed: 20031568
Hum Genet. 2007 Mar;121(1):23-34
pubmed: 17048007
J Gen Physiol. 1988 Dec;92(6):713-29
pubmed: 3216188
Nat Commun. 2018 May 8;9(1):1825
pubmed: 29739930
Ann Epidemiol. 1991 Feb;1(3):263-76
pubmed: 1669507
Blood. 2019 Dec 5;134(23):2082-2091
pubmed: 31064749
Hum Genet. 2014 Aug;133(8):985-95
pubmed: 24643644
J Pharm Pharmacol. 1987 Jun;39(6):416-20
pubmed: 2886597
Genet Epidemiol. 2014 Dec;38(8):709-13
pubmed: 25376901
Cardiology. 2009;114(3):174-8
pubmed: 19571538
Acta Diabetol. 2016 Apr;53(2):237-42
pubmed: 25976242
J Clin Invest. 1981 Nov;68(5):1370-3
pubmed: 6895379
Int J Epidemiol. 2017 Dec 1;46(6):1985-1998
pubmed: 29040600
J Mol Biol. 1984 Apr 5;174(2):319-41
pubmed: 6716481
Thromb Haemost. 2017 Jan 26;117(2):262-268
pubmed: 27882376
Circ Res. 2006 Dec 8;99(12):1419-25
pubmed: 17082477
J Thromb Haemost. 2022 Jun;20(6):1331-1349
pubmed: 35285134
PLoS One. 2011;6(12):e29168
pubmed: 22216198
Proc Natl Acad Sci U S A. 2013 Jan 8;110(2):588-93
pubmed: 23267103
Clin Respir J. 2019 Aug;13(8):530-537
pubmed: 31295762
Nat Genet. 2012 Mar 18;44(4):369-75, S1-3
pubmed: 22426310
Genet Epidemiol. 2017 Feb;41(2):145-151
pubmed: 27990689
Thromb Haemost. 2009 Oct;102(4):615-9
pubmed: 19806245
J Am Heart Assoc. 2022 Feb 15;11(4):e023018
pubmed: 35112923
Hum Mol Genet. 2017 Feb 1;26(3):637-649
pubmed: 28053049
Thromb Res. 2018 Sep;169:57-63
pubmed: 30015229
PLoS Genet. 2014 May 15;10(5):e1004383
pubmed: 24830394
Arch Intern Med. 1994 Jun 27;154(12):1333-9
pubmed: 8002685
Hum Genet. 1993 Mar;91(2):196
pubmed: 8462980
Eur J Immunogenet. 2000 Aug;27(4):231-40
pubmed: 10998088
EMBO J. 2002 Aug 15;21(16):4259-67
pubmed: 12169628
Blood. 2010 Dec 2;116(23):5032-6
pubmed: 20802025
Thromb Haemost. 1994 Apr;71(4):441-5
pubmed: 8052960
Haematologica. 2009 Apr;94(4):589-92
pubmed: 19229049
FEBS Lett. 1985 Sep 23;189(2):221-4
pubmed: 3840099
Am Fam Physician. 2017 Mar 1;95(5):295-302
pubmed: 28290648
J Thromb Haemost. 2010 Jun;8(6):1193-200
pubmed: 20230415
Am J Clin Nutr. 2011 Aug;94(2):495-500
pubmed: 21653798
Circulation. 2022 Oct 18;146(16):1225-1242
pubmed: 36154123
J Thromb Haemost. 2014 Jun;12(6):879-86
pubmed: 24628832
Endocr J. 2014;61(7):683-9
pubmed: 24785259
Am J Hum Genet. 2018 Nov 1;103(5):691-706
pubmed: 30388399
Am J Hum Genet. 2000 Dec;67(6):1452-9
pubmed: 11038326
Int J Epidemiol. 2015 Apr;44(2):512-25
pubmed: 26050253
N Engl J Med. 1983 Aug 11;309(6):340-4
pubmed: 6688122
Am J Hum Genet. 2011 Jan 7;88(1):76-82
pubmed: 21167468
Clin Chem. 1995 Feb;41(2):264-70
pubmed: 7874780
Int J Inflam. 2013;2013:980327
pubmed: 23710416
Thromb Haemost. 2022 Jun;122(6):1027-1039
pubmed: 35272364
JAMA. 1995 Aug 23-30;274(8):620-5
pubmed: 7637142
Thromb Haemost. 1999 Sep;82(3):1088-92
pubmed: 10494768
Nat Genet. 2013 Jun;45(6):580-5
pubmed: 23715323
Hum Genet. 1992 Aug;89(6):683-4
pubmed: 1511988
Nat Commun. 2021 Feb 3;12(1):764
pubmed: 33536417
Biomed Res Int. 2015;2015:678924
pubmed: 25969834
Blood. 2019 Nov 7;134(19):1645-1657
pubmed: 31420334
Circulation. 2010 Mar 30;121(12):1382-92
pubmed: 20231535
Clin Sci (Lond). 2019 Mar 15;133(5):723-737
pubmed: 30877150
Hum Genet. 2000 Nov;107(5):458-65
pubmed: 11140943
EMBO J. 1987 Aug;6(8):2289-96
pubmed: 2822385
J Thromb Haemost. 2016 Jan;14(1):83-8
pubmed: 26565658
Hum Genet. 1992 Dec;90(4):457-9
pubmed: 1483705
Br J Haematol. 2012 Apr;157(2):230-9
pubmed: 22443383
Eur Heart J. 2010 May;31(10):1237-47
pubmed: 20200015
Bioinformatics. 2010 Sep 1;26(17):2190-1
pubmed: 20616382
Genes (Basel). 2022 Mar 10;13(3):
pubmed: 35328045
Hepatology. 2012 Mar;55(3):781-9
pubmed: 22105854
Proc Natl Acad Sci U S A. 2017 Apr 4;114(14):E2862-E2871
pubmed: 28330995
Nat Genet. 2019 Nov;51(11):1574-1579
pubmed: 31676865
Nat Commun. 2019 Sep 24;10(1):4330
pubmed: 31551420
J Diabetes Investig. 2018 Sep;9(5):1189-1195
pubmed: 29356453
Nat Genet. 2020 Jul;52(7):680-691
pubmed: 32541925
Blood. 1984 Dec;64(6):1297-300
pubmed: 6238642
Nat Genet. 2019 Jan;51(1):187-195
pubmed: 30478440
Ann Intern Med. 2011 Sep 6;155(5):316-22
pubmed: 21893624
Int J Cardiol. 2018 Dec 1;272:298-305
pubmed: 30025651
Nature. 2015 Oct 1;526(7571):68-74
pubmed: 26432245
J Cardiol. 2014 Nov;64(5):339-46
pubmed: 24674750
PLoS Genet. 2019 Jan 22;15(1):e1007889
pubmed: 30668570
Arterioscler Thromb Vasc Biol. 2002 Jun 1;22(6):1018-22
pubmed: 12067914
Br J Haematol. 1987 Apr;65(4):457-62
pubmed: 3472589
Hum Mol Genet. 2016 Oct 1;25(19):4350-4368
pubmed: 27577874
Diabetologia. 2021 Jul;64(7):1613-1625
pubmed: 33842983
Br J Haematol. 2018 Feb;180(3):335-345
pubmed: 29082522
Arterioscler Thromb Vasc Biol. 2017 Mar;37(3):589-597
pubmed: 28082259
Br J Haematol. 2013 Mar;160(6):838-41
pubmed: 23150947
PLoS One. 2013 May 21;8(5):e64998
pubmed: 23705025
Nat Genet. 2018 Apr;50(4):524-537
pubmed: 29531354
Circulation. 1966 Nov;34(5):856-64
pubmed: 5332331
Genome Biol. 2021 Jan 26;22(1):49
pubmed: 33499903
Genome Med. 2016 Jan 06;8(1):2
pubmed: 26739746
Nat Hum Behav. 2018 Jan;2(1):6-10
pubmed: 30980045
Nat Genet. 2021 Dec;53(12):1712-1721
pubmed: 34857953

Auteurs

Yuekai Ji (Y)

Cardiovascular Division, Department of Medicine, University of Minnesota, MN (Y.J.).

Gerard Temprano-Sagrera (G)

Unit of genomics of Complex Disease, Institut d'Investigació Biomèdica Sant Pau (IIB SANT PAU), Barcelona, Spain (G.T.-S., N.-Q.L., A.M.-P., J.C.S., J.M.S., M.S.-L.).

Lori A Holle (LA)

Department of Pathology and Laboratory Medicine and UNC Blood Research Center, University of North Carolina at Chapel Hill (L.A.H., K.K., D.A.D., A.S.W.).

Allison Bebo (A)

Human Genetics Center, Department of Epidemiology, Human Genetics, and Environmental Sciences, School of Public Health, The University of Texas Health Science Center at Houston (A.B., M.R.B., A.C.M., P.S.d.V.).

Jennifer A Brody (JA)

Department of Medicine, University of Washington (J.A.B., K.L.W.).

Ngoc-Quynh Le (NQ)

Unit of genomics of Complex Disease, Institut d'Investigació Biomèdica Sant Pau (IIB SANT PAU), Barcelona, Spain (G.T.-S., N.-Q.L., A.M.-P., J.C.S., J.M.S., M.S.-L.).

Kadri Kangro (K)

Department of Pathology and Laboratory Medicine and UNC Blood Research Center, University of North Carolina at Chapel Hill (L.A.H., K.K., D.A.D., A.S.W.).

Michael R Brown (MR)

Human Genetics Center, Department of Epidemiology, Human Genetics, and Environmental Sciences, School of Public Health, The University of Texas Health Science Center at Houston (A.B., M.R.B., A.C.M., P.S.d.V.).

Angel Martinez-Perez (A)

Unit of genomics of Complex Disease, Institut d'Investigació Biomèdica Sant Pau (IIB SANT PAU), Barcelona, Spain (G.T.-S., N.-Q.L., A.M.-P., J.C.S., J.M.S., M.S.-L.).

Colleen M Sitlani (CM)

Cardiovascular Health Research Unit, Department of Medicine, University of Washington, Seattle (C.M.S.).

Pierre Suchon (P)

C2VN, INSERM, INRAE, Aix Marseille Univ, France (P.S., P.-E.M.).
Laboratory of Haematology, La Timone Hospital, France (P.S., P.-E.M.).

Marcus E Kleber (ME)

SYNLAB MVZ für Humangenetik Mannheim, Germany (M.E.K.).
Vth Department of Medicine, Medical Faculty Mannheim, Heidelberg University, Germany (M.E.K., G.E.D., A.P.M., W.M.).

David B Emmert (DB)

Institute for Biomedicine (affiliated to the University of Lübeck), Eurac Research, Italy (D.B.E., M.G., C.F., A.A.H.).

Ayse Bilge Ozel (A)

Department of Human Genetics, University of Michigan, C.S. Mott Children's Hospital, Ann Arbor (A.B.O.).

Dre'Von A Dobson (DA)

Department of Pathology and Laboratory Medicine and UNC Blood Research Center, University of North Carolina at Chapel Hill (L.A.H., K.K., D.A.D., A.S.W.).

Weihong Tang (W)

Division of Epidemiology and Community Health, School of Public Health, University of Minnesota, MN (W.T., J.S.P.).

Dolors Llobet (D)

Unit of Thrombosis and Hemostasis, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain (D.L., J.C.S.).

Russell P Tracy (RP)

Department of Pathology and Laboratory Medicine, University of Vermont College of Medicine, Burlington (R.P.T.).

Jean-François Deleuze (JF)

Centre National de Recherche en Génomique Humaine, CEA, France (J.-F.D.).
Centre d'Etude du Polymorphisme Humain, Fondation Jean Dausset, France (J.-F.D.).
Laboratory of Excellence on Medical Genomics (GenMed), France (J.-F.D., D.-A.T.).

Graciela E Delgado (GE)

Vth Department of Medicine, Medical Faculty Mannheim, Heidelberg University, Germany (M.E.K., G.E.D., A.P.M., W.M.).

Martin Gögele (M)

Institute for Biomedicine (affiliated to the University of Lübeck), Eurac Research, Italy (D.B.E., M.G., C.F., A.A.H.).

Kerri L Wiggins (KL)

Department of Medicine, University of Washington (J.A.B., K.L.W.).

Juan Carlos Souto (JC)

Unit of genomics of Complex Disease, Institut d'Investigació Biomèdica Sant Pau (IIB SANT PAU), Barcelona, Spain (G.T.-S., N.-Q.L., A.M.-P., J.C.S., J.M.S., M.S.-L.).
Unit of Thrombosis and Hemostasis, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain (D.L., J.C.S.).

James S Pankow (JS)

Division of Epidemiology and Community Health, School of Public Health, University of Minnesota, MN (W.T., J.S.P.).

Kent D Taylor (KD)

The Institute for Translational Genomics and Population Sciences, Department of Pediatrics, The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center, CA (K.D.T.).

David-Alexandre Trégouët (DA)

Laboratory of Excellence on Medical Genomics (GenMed), France (J.-F.D., D.-A.T.).
INSERM UMR 1219, Bordeaux Population Health Research Center, France (D.-A.T.).

Angela P Moissl (AP)

Vth Department of Medicine, Medical Faculty Mannheim, Heidelberg University, Germany (M.E.K., G.E.D., A.P.M., W.M.).
Institute of Nutritional Sciences, Friedrich Schiller University Jena, Germany (A.P.M.).
Competence Cluster for Nutrition and Cardiovascular Health(nutriCARD) Halle-Jena-Leipzig, Germany (A.P.M.).

Christian Fuchsberger (C)

Institute for Biomedicine (affiliated to the University of Lübeck), Eurac Research, Italy (D.B.E., M.G., C.F., A.A.H.).

Frits R Rosendaal (FR)

Department of Clinical Epidemiology, Leiden University Medical Center, the Netherlands (F.R.R.).

Alanna C Morrison (AC)

Human Genetics Center, Department of Epidemiology, Human Genetics, and Environmental Sciences, School of Public Health, The University of Texas Health Science Center at Houston (A.B., M.R.B., A.C.M., P.S.d.V.).

Jose Manuel Soria (JM)

Unit of genomics of Complex Disease, Institut d'Investigació Biomèdica Sant Pau (IIB SANT PAU), Barcelona, Spain (G.T.-S., N.-Q.L., A.M.-P., J.C.S., J.M.S., M.S.-L.).

Mary Cushman (M)

Larner College of Medicine, University of Vermont, Burlington (M.C.).

Pierre-Emmanuel Morange (PE)

C2VN, INSERM, INRAE, Aix Marseille Univ, France (P.S., P.-E.M.).
Laboratory of Haematology, La Timone Hospital, France (P.S., P.-E.M.).

Winfried März (W)

Vth Department of Medicine, Medical Faculty Mannheim, Heidelberg University, Germany (M.E.K., G.E.D., A.P.M., W.M.).
Synlab Academy, Synlab Holding Deutschland GmbH, Germany (W.M.).

Andrew A Hicks (AA)

Institute for Biomedicine (affiliated to the University of Lübeck), Eurac Research, Italy (D.B.E., M.G., C.F., A.A.H.).

Karl C Desch (KC)

Department of Pediatrics, University of Michigan, C.S. Mott Children's Hospital, Ann Arbor (K.C.D.).

Andrew D Johnson (AD)

National Heart Lung and Blood Institute, Division of Intramural Research, Population Sciences Branch, The Framingham Heart Study, MA (A.D.J.).

Paul S de Vries (PS)

Human Genetics Center, Department of Epidemiology, Human Genetics, and Environmental Sciences, School of Public Health, The University of Texas Health Science Center at Houston (A.B., M.R.B., A.C.M., P.S.d.V.).

Alisa S Wolberg (AS)

Department of Pathology and Laboratory Medicine and UNC Blood Research Center, University of North Carolina at Chapel Hill (L.A.H., K.K., D.A.D., A.S.W.).

Nicholas L Smith (NL)

Department of Epidemiology, University of Washington, Seattle (N.L.S.).
Kaiser Permanente Washington Health Research Institute (N.L.S.).
Seattle Epidemiologic Research and Information Center, Department of Veterans Affairs Office of Research and Development, WA (N.L.S.).

Maria Sabater-Lleal (M)

Unit of genomics of Complex Disease, Institut d'Investigació Biomèdica Sant Pau (IIB SANT PAU), Barcelona, Spain (G.T.-S., N.-Q.L., A.M.-P., J.C.S., J.M.S., M.S.-L.).
Cardiovascular Medicine Unit, Department of Medicine, Karolinska Institutet, Center for Molecular Medicine, Stockholm, Sweden (M.S.-L.).

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