Probing rare von Willebrand disease–causing mutations in the D4 and C-domains of von Willebrand factor

Background: von Willebrand disease (VWD) is characterized by absence or reduction of plasma von Willebrand factor (VWF) levels or reduced protein function. While the spectrum of causative VWD mutations is vast, there has been limited characterization of variants occurring within the D4-C6 domains of...

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Main Authors: Golzar Mobayen, Sammy El-Mansi, Alain Chion, Thomas D. Nightingale, Thomas A.J. McKinnon
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:Research and Practice in Thrombosis and Haemostasis
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Online Access:http://www.sciencedirect.com/science/article/pii/S2475037925002468
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author Golzar Mobayen
Sammy El-Mansi
Alain Chion
Thomas D. Nightingale
Thomas A.J. McKinnon
author_facet Golzar Mobayen
Sammy El-Mansi
Alain Chion
Thomas D. Nightingale
Thomas A.J. McKinnon
author_sort Golzar Mobayen
collection DOAJ
description Background: von Willebrand disease (VWD) is characterized by absence or reduction of plasma von Willebrand factor (VWF) levels or reduced protein function. While the spectrum of causative VWD mutations is vast, there has been limited characterization of variants occurring within the D4-C6 domains of VWF that comprise the C-terminal portion of the molecule. Objectives: In this study, we investigated the impact of 9 putative low-frequency VWD-causing variants on VWF function. Methods: Variants were generated by site-directed mutagenesis and expressed in human embryonic kidney (HEK)293(T) cells and analyzed for expression, intracellular storage, and multimeric profile. The ability of Arg2379Cys to form dimers was assessed using an A2-CK fragment of VWF. Results: Arg2379Cys, Ser2497Pro, and Cys2639Tyr had significantly reduced secretion from HEK293T cells, while the other mutations all failed to be secreted. While cotransfection with wild-type VWF appeared to rescue expression, cotransfection with a deletion A1 construct demonstrated that only the Gly2044Asp, Glu2343Val, Ser2497Pro, and Cys2693Tyr variants could be rescued. All the variants failed to form appreciable pseudo–Weibel-Palade bodies in HEK293 cells and showed abnormal multimers in cell lysates. The Arg2379Cys variant could be overexpressed by only formed monomers and some dimers. Analysis with a VWF-A2CK protein demonstrated that in the homozygous state Arg2379Cys behaves likes a type 2A variant, while it is likely to be a type 1 variant in the heterozygous state. Conclusion: These data show that variants within the C-terminal region of VWF can dramatically impact proper VWF expression and can different impacts on VWF depending on homozygosity or heterozygosity.
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spelling doaj-art-96fccff27a11442d9b08aa0c8ac03ab82025-08-20T03:04:58ZengElsevierResearch and Practice in Thrombosis and Haemostasis2475-03792025-05-019410292210.1016/j.rpth.2025.102922Probing rare von Willebrand disease–causing mutations in the D4 and C-domains of von Willebrand factorGolzar Mobayen0Sammy El-Mansi1Alain Chion2Thomas D. Nightingale3Thomas A.J. McKinnon4Department of Immunology and Inflammation, Centre for Haematology, Imperial College Academic Health Science Centre, Hammersmith Hospital, London, UK; Correspondence Golzar Mobayen and Thomas A. J. McKinnon, Department of Immunology and Inflammation, Centre for Haematology, Imperial College Academic Health Science Centre, Hammersmith Hospital, London W12 0NN, UK.Department of Medicine, Centre for Microvascular Research, William Harvey Research Institute, Queen Mary University of London, London, UKIrish Centre for Vascular Biology, School of Pharmacy and Biomolecular Sciences, Royal College of Surgeons in Ireland, Dublin, IrelandDepartment of Medicine, Centre for Microvascular Research, William Harvey Research Institute, Queen Mary University of London, London, UKDepartment of Immunology and Inflammation, Centre for Haematology, Imperial College Academic Health Science Centre, Hammersmith Hospital, London, UK; Correspondence Golzar Mobayen and Thomas A. J. McKinnon, Department of Immunology and Inflammation, Centre for Haematology, Imperial College Academic Health Science Centre, Hammersmith Hospital, London W12 0NN, UK.Background: von Willebrand disease (VWD) is characterized by absence or reduction of plasma von Willebrand factor (VWF) levels or reduced protein function. While the spectrum of causative VWD mutations is vast, there has been limited characterization of variants occurring within the D4-C6 domains of VWF that comprise the C-terminal portion of the molecule. Objectives: In this study, we investigated the impact of 9 putative low-frequency VWD-causing variants on VWF function. Methods: Variants were generated by site-directed mutagenesis and expressed in human embryonic kidney (HEK)293(T) cells and analyzed for expression, intracellular storage, and multimeric profile. The ability of Arg2379Cys to form dimers was assessed using an A2-CK fragment of VWF. Results: Arg2379Cys, Ser2497Pro, and Cys2639Tyr had significantly reduced secretion from HEK293T cells, while the other mutations all failed to be secreted. While cotransfection with wild-type VWF appeared to rescue expression, cotransfection with a deletion A1 construct demonstrated that only the Gly2044Asp, Glu2343Val, Ser2497Pro, and Cys2693Tyr variants could be rescued. All the variants failed to form appreciable pseudo–Weibel-Palade bodies in HEK293 cells and showed abnormal multimers in cell lysates. The Arg2379Cys variant could be overexpressed by only formed monomers and some dimers. Analysis with a VWF-A2CK protein demonstrated that in the homozygous state Arg2379Cys behaves likes a type 2A variant, while it is likely to be a type 1 variant in the heterozygous state. Conclusion: These data show that variants within the C-terminal region of VWF can dramatically impact proper VWF expression and can different impacts on VWF depending on homozygosity or heterozygosity.http://www.sciencedirect.com/science/article/pii/S2475037925002468von Willebrand factorvon Willebrand diseasevariant analysisbleedingmutations
spellingShingle Golzar Mobayen
Sammy El-Mansi
Alain Chion
Thomas D. Nightingale
Thomas A.J. McKinnon
Probing rare von Willebrand disease–causing mutations in the D4 and C-domains of von Willebrand factor
Research and Practice in Thrombosis and Haemostasis
von Willebrand factor
von Willebrand disease
variant analysis
bleeding
mutations
title Probing rare von Willebrand disease–causing mutations in the D4 and C-domains of von Willebrand factor
title_full Probing rare von Willebrand disease–causing mutations in the D4 and C-domains of von Willebrand factor
title_fullStr Probing rare von Willebrand disease–causing mutations in the D4 and C-domains of von Willebrand factor
title_full_unstemmed Probing rare von Willebrand disease–causing mutations in the D4 and C-domains of von Willebrand factor
title_short Probing rare von Willebrand disease–causing mutations in the D4 and C-domains of von Willebrand factor
title_sort probing rare von willebrand disease causing mutations in the d4 and c domains of von willebrand factor
topic von Willebrand factor
von Willebrand disease
variant analysis
bleeding
mutations
url http://www.sciencedirect.com/science/article/pii/S2475037925002468
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