Genome‐Wide Search for Nonadditive Allele Effects Identifies PSKH2 as Involved in the Variability of Factor V Activity

Background Factor V (FV) is a key molecular player in the coagulation cascade. FV plasma levels have been associated with several human diseases, including thrombosis, bleeding, and diabetic complications. So far, 2 genes have been robustly found through genome‐wide association analyses to contribut...

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Main Authors: Blandine Gendre, Angel Martinez‐Perez, Marcus E. Kleber, Astrid van Hylckama Vlieg, Anne Boland, Robert Olaso, Marine Germain, Gaëlle Munsch, Angela Patricia Moissl, Pierre Suchon, Juan Carlos Souto, José Manuel Soria, Jean‐François Deleuze, Winfried März, Frits R. Rosendaal, Maria Sabater‐Lleal, Pierre‐Emmanuel Morange, David‐Alexandre Trégouët
Format: Article
Language:English
Published: Wiley 2024-11-01
Series:Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
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Online Access:https://www.ahajournals.org/doi/10.1161/JAHA.124.034943
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author Blandine Gendre
Angel Martinez‐Perez
Marcus E. Kleber
Astrid van Hylckama Vlieg
Anne Boland
Robert Olaso
Marine Germain
Gaëlle Munsch
Angela Patricia Moissl
Pierre Suchon
Juan Carlos Souto
José Manuel Soria
Jean‐François Deleuze
Winfried März
Frits R. Rosendaal
Maria Sabater‐Lleal
Pierre‐Emmanuel Morange
David‐Alexandre Trégouët
author_facet Blandine Gendre
Angel Martinez‐Perez
Marcus E. Kleber
Astrid van Hylckama Vlieg
Anne Boland
Robert Olaso
Marine Germain
Gaëlle Munsch
Angela Patricia Moissl
Pierre Suchon
Juan Carlos Souto
José Manuel Soria
Jean‐François Deleuze
Winfried März
Frits R. Rosendaal
Maria Sabater‐Lleal
Pierre‐Emmanuel Morange
David‐Alexandre Trégouët
author_sort Blandine Gendre
collection DOAJ
description Background Factor V (FV) is a key molecular player in the coagulation cascade. FV plasma levels have been associated with several human diseases, including thrombosis, bleeding, and diabetic complications. So far, 2 genes have been robustly found through genome‐wide association analyses to contribute to the inter‐individual variability of plasma FV levels: structural F5 gene and PLXDC2. Methods and Results The authors used the underestimated Brown‐Forsythe methodology implemented in the QuickTest software to search for non‐additive genetic effects that could contribute to the inter‐individual variability of FV plasma activity. QUICKTEST was applied to 4 independent genome‐wide association studies studies (LURIC [Ludwigshafen RIsk and Cardiovascular Health Study], MARTHA [Marseille Thrombosis Association], MEGA [Multiple Environmental and Genetic Assessment], and RETROVE [Riesgo de Enfermedad Tromboembolica Venosa]) totaling 4505 participants of European ancestry with measured FV plasma levels. Results obtained in the 4 cohorts were meta‐analyzed using a fixed‐effect model. Additional analyses involved exploring haplotype and gene×gene interactions in downstream investigations. A genome‐wide significant signal at the PSKH2 locus on chr8q21.3 with lead variant rs75463553 with no evidence for heterogeneity across cohorts was observed (P=0.518). Although rs75463553 did not show an association with mean FV levels (P=0.49), it demonstrated a robust significant (P=3.38x10−9) association with the variance of FV plasma levels. Further analyses confirmed the reported association of PSKH2 with neutrophil biology and revealed that rs75463553 likely interacts with two loci, GRIN2A and POM121L12, known for their involvement in smoking biology. Conclusions This comprehensive approach identifies the role of PSKH2 as a novel molecular player in the genetic regulation of FV, shedding light on the contribution of neutrophils to FV biology.
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spelling doaj-art-becf52ad5d8646cd8abf1c175a980a042025-08-20T02:07:28ZengWileyJournal of the American Heart Association: Cardiovascular and Cerebrovascular Disease2047-99802024-11-01132110.1161/JAHA.124.034943Genome‐Wide Search for Nonadditive Allele Effects Identifies PSKH2 as Involved in the Variability of Factor V ActivityBlandine Gendre0Angel Martinez‐Perez1Marcus E. Kleber2Astrid van Hylckama Vlieg3Anne Boland4Robert Olaso5Marine Germain6Gaëlle Munsch7Angela Patricia Moissl8Pierre Suchon9Juan Carlos Souto10José Manuel Soria11Jean‐François Deleuze12Winfried März13Frits R. Rosendaal14Maria Sabater‐Lleal15Pierre‐Emmanuel Morange16David‐Alexandre Trégouët17INSERM, Bordeaux Population Health Research Center, UMR 1219, ELEANOR, University of Bordeaux Bordeaux FranceUnit of Genomics of Complex Diseases, Institut de Recerca Sant Pau (IR SANT PAU) Barcelona SpainDepartment of Medicine V, Medical Faculty Mannheim University of Heidelberg Mannheim GermanyDepartment of Clinical Epidemiology Leiden University Medical Center Leiden NetherlandsCEA, Centre National de Recherche en Génomique Humaine (CNRGH), Université Paris‐Saclay Evry FranceCEA, Centre National de Recherche en Génomique Humaine (CNRGH), Université Paris‐Saclay Evry FranceINSERM, Bordeaux Population Health Research Center, UMR 1219, ELEANOR, University of Bordeaux Bordeaux FranceINSERM, Bordeaux Population Health Research Center, UMR 1219, ELEANOR, University of Bordeaux Bordeaux FranceDepartment of Medicine V, Medical Faculty Mannheim University of Heidelberg Mannheim GermanyCardiovascular and Nutrition Research Center (C2VN), INSERM, INRAE, Aix‐Marseille University Marseille FranceCentre for Biomedical Network Research on Rare Diseases (CIBERER), Instituto de Salud Carlos III Madrid SpainUnit of Genomics of Complex Diseases, Institut de Recerca Sant Pau (IR SANT PAU) Barcelona SpainCEA, Centre National de Recherche en Génomique Humaine (CNRGH), Université Paris‐Saclay Evry FranceDepartment of Medicine V, Medical Faculty Mannheim University of Heidelberg Mannheim GermanyDepartment of Clinical Epidemiology Leiden University Medical Center Leiden NetherlandsUnit of Genomics of Complex Diseases, Institut de Recerca Sant Pau (IR SANT PAU) Barcelona SpainCardiovascular and Nutrition Research Center (C2VN), INSERM, INRAE, Aix‐Marseille University Marseille FranceINSERM, Bordeaux Population Health Research Center, UMR 1219, ELEANOR, University of Bordeaux Bordeaux FranceBackground Factor V (FV) is a key molecular player in the coagulation cascade. FV plasma levels have been associated with several human diseases, including thrombosis, bleeding, and diabetic complications. So far, 2 genes have been robustly found through genome‐wide association analyses to contribute to the inter‐individual variability of plasma FV levels: structural F5 gene and PLXDC2. Methods and Results The authors used the underestimated Brown‐Forsythe methodology implemented in the QuickTest software to search for non‐additive genetic effects that could contribute to the inter‐individual variability of FV plasma activity. QUICKTEST was applied to 4 independent genome‐wide association studies studies (LURIC [Ludwigshafen RIsk and Cardiovascular Health Study], MARTHA [Marseille Thrombosis Association], MEGA [Multiple Environmental and Genetic Assessment], and RETROVE [Riesgo de Enfermedad Tromboembolica Venosa]) totaling 4505 participants of European ancestry with measured FV plasma levels. Results obtained in the 4 cohorts were meta‐analyzed using a fixed‐effect model. Additional analyses involved exploring haplotype and gene×gene interactions in downstream investigations. A genome‐wide significant signal at the PSKH2 locus on chr8q21.3 with lead variant rs75463553 with no evidence for heterogeneity across cohorts was observed (P=0.518). Although rs75463553 did not show an association with mean FV levels (P=0.49), it demonstrated a robust significant (P=3.38x10−9) association with the variance of FV plasma levels. Further analyses confirmed the reported association of PSKH2 with neutrophil biology and revealed that rs75463553 likely interacts with two loci, GRIN2A and POM121L12, known for their involvement in smoking biology. Conclusions This comprehensive approach identifies the role of PSKH2 as a novel molecular player in the genetic regulation of FV, shedding light on the contribution of neutrophils to FV biology.https://www.ahajournals.org/doi/10.1161/JAHA.124.034943Brown‐Forsythe testcoagulationfactor V plasma levelsnon‐additive genetic effectsparent‐of‐origin effects
spellingShingle Blandine Gendre
Angel Martinez‐Perez
Marcus E. Kleber
Astrid van Hylckama Vlieg
Anne Boland
Robert Olaso
Marine Germain
Gaëlle Munsch
Angela Patricia Moissl
Pierre Suchon
Juan Carlos Souto
José Manuel Soria
Jean‐François Deleuze
Winfried März
Frits R. Rosendaal
Maria Sabater‐Lleal
Pierre‐Emmanuel Morange
David‐Alexandre Trégouët
Genome‐Wide Search for Nonadditive Allele Effects Identifies PSKH2 as Involved in the Variability of Factor V Activity
Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
Brown‐Forsythe test
coagulation
factor V plasma levels
non‐additive genetic effects
parent‐of‐origin effects
title Genome‐Wide Search for Nonadditive Allele Effects Identifies PSKH2 as Involved in the Variability of Factor V Activity
title_full Genome‐Wide Search for Nonadditive Allele Effects Identifies PSKH2 as Involved in the Variability of Factor V Activity
title_fullStr Genome‐Wide Search for Nonadditive Allele Effects Identifies PSKH2 as Involved in the Variability of Factor V Activity
title_full_unstemmed Genome‐Wide Search for Nonadditive Allele Effects Identifies PSKH2 as Involved in the Variability of Factor V Activity
title_short Genome‐Wide Search for Nonadditive Allele Effects Identifies PSKH2 as Involved in the Variability of Factor V Activity
title_sort genome wide search for nonadditive allele effects identifies pskh2 as involved in the variability of factor v activity
topic Brown‐Forsythe test
coagulation
factor V plasma levels
non‐additive genetic effects
parent‐of‐origin effects
url https://www.ahajournals.org/doi/10.1161/JAHA.124.034943
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