SARS-CoV-2 ORF7a activates the endothelium to release von Willebrand factor that promotes thrombosis

Background: Patients with severe and critical COVID-19 frequently exhibit thromboembolic complications, a significant cause of mortality and morbidity. Increased plasma levels of von Willebrand factor (VWF) following SARS-CoV-2 infection have been extensively reported, which links to thrombosis and...

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Main Authors: Quan Zhang, Xiaohu Huang, Hangnoh Lee, Jin-Gu Lee, Szumam Liu, Shiwani Limbu, Malay K. Basu, Joyce van de Leemput, Felice D’Agnillo, Zhe Han, X. Long Zheng
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/S2475037925002717
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author Quan Zhang
Xiaohu Huang
Hangnoh Lee
Jin-Gu Lee
Szumam Liu
Shiwani Limbu
Malay K. Basu
Joyce van de Leemput
Felice D’Agnillo
Zhe Han
X. Long Zheng
author_facet Quan Zhang
Xiaohu Huang
Hangnoh Lee
Jin-Gu Lee
Szumam Liu
Shiwani Limbu
Malay K. Basu
Joyce van de Leemput
Felice D’Agnillo
Zhe Han
X. Long Zheng
author_sort Quan Zhang
collection DOAJ
description Background: Patients with severe and critical COVID-19 frequently exhibit thromboembolic complications, a significant cause of mortality and morbidity. Increased plasma levels of von Willebrand factor (VWF) following SARS-CoV-2 infection have been extensively reported, which links to thrombosis and increased mortality. However, the mechanism underlying SARS-CoV-2–associated thrombotic complications is not fully understood. Objectives: To determine the mechanism of SARS-CoV-2–associated thrombosis. Methods: Drosophila genetic screening and molecular, cellular, and biochemical approaches were used. Results: Genetic screening identified a SARS-CoV-2 accessory protein, Orf7a, as a crucial factor promoting agglutination of hemolymph, the circulatory fluid of flies, which is functionally comparable to the blood and lymph of vertebrates. Further studies using cultured murine splenic vascular endothelial cells and human umbilical cord endothelial cells demonstrated that overexpression of ORF7a in these cells significantly activated and stimulated the release of VWF, leading to an increased rate and final coverage of Adamts-13-/- murine platelets on activated endothelial surfaces under arterial shear. Moreover, a soluble recombinant ORF7a could also activate human endothelial cells and trigger the release of VWF from Weibel–Palade bodies. Conclusion: We demonstrate for the first time that SARS-CoV-2 ORF7a may be one of the pathogenic factors contributing to COVID-19–associated thrombosis by activating the vascular endothelium to release ultralarge VWF, which promotes platelet adhesion and agglutination, and thrombus formation. Thus, a strategy specifically targeting VWF-platelet interaction, such as recombinant a disintegrin and metalloprotease with thrombospondin type 1 repeats, 13 (ADAMTS-13) and/or caplacizumab, may be efficacious in reducing COVID-19–associated thrombosis and mortality.
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spelling doaj-art-25512a7cc53b4e4e843fd3dc248f70f92025-08-20T03:04:58ZengElsevierResearch and Practice in Thrombosis and Haemostasis2475-03792025-05-019410294710.1016/j.rpth.2025.102947SARS-CoV-2 ORF7a activates the endothelium to release von Willebrand factor that promotes thrombosisQuan Zhang0Xiaohu Huang1Hangnoh Lee2Jin-Gu Lee3Szumam Liu4Shiwani Limbu5Malay K. Basu6Joyce van de Leemput7Felice D’Agnillo8Zhe Han9X. Long Zheng10Departments of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, USA; Department of Pulmonary and Critical Care Medicine, The Second Xiangya Hospital, Central South University, Changsha, ChinaDepartment of Medicine, Center for Precision Disease Modeling, University of Maryland School of Medicine, Baltimore, Maryland, USA; Division of Endocrinology, Diabetes and Nutrition, Department of Medicine, University of Maryland School of Medicine, Baltimore, Maryland, USADepartment of Medicine, Center for Precision Disease Modeling, University of Maryland School of Medicine, Baltimore, Maryland, USA; Division of Endocrinology, Diabetes and Nutrition, Department of Medicine, University of Maryland School of Medicine, Baltimore, Maryland, USADepartment of Medicine, Center for Precision Disease Modeling, University of Maryland School of Medicine, Baltimore, Maryland, USA; Division of Endocrinology, Diabetes and Nutrition, Department of Medicine, University of Maryland School of Medicine, Baltimore, Maryland, USADepartments of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, USADepartments of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, USADepartments of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, USADepartment of Medicine, Center for Precision Disease Modeling, University of Maryland School of Medicine, Baltimore, Maryland, USA; Division of Endocrinology, Diabetes and Nutrition, Department of Medicine, University of Maryland School of Medicine, Baltimore, Maryland, USALaboratory of Biochemistry and Vascular Biology, Center for Biologics Evaluation and Research, Food and Drug Administration, Silver Spring, Maryland, USADepartment of Medicine, Center for Precision Disease Modeling, University of Maryland School of Medicine, Baltimore, Maryland, USA; Division of Endocrinology, Diabetes and Nutrition, Department of Medicine, University of Maryland School of Medicine, Baltimore, Maryland, USA; Correspondence Zhe Han, Department of Medicine, Center for Precision Disease Modeling, University of Maryland School of Medicine, 670 W Baltimore Street, 4052, HSFIII, Baltimore, MD 21201, USA.Departments of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, USA; Institute of Reproductive and Developmental Sciences, University of Kansas Medical Center, Kansas City, Kansas, USA; X. Long Zheng, Departments of Pathology and Laboratory Medicine, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS 66216, USA.Background: Patients with severe and critical COVID-19 frequently exhibit thromboembolic complications, a significant cause of mortality and morbidity. Increased plasma levels of von Willebrand factor (VWF) following SARS-CoV-2 infection have been extensively reported, which links to thrombosis and increased mortality. However, the mechanism underlying SARS-CoV-2–associated thrombotic complications is not fully understood. Objectives: To determine the mechanism of SARS-CoV-2–associated thrombosis. Methods: Drosophila genetic screening and molecular, cellular, and biochemical approaches were used. Results: Genetic screening identified a SARS-CoV-2 accessory protein, Orf7a, as a crucial factor promoting agglutination of hemolymph, the circulatory fluid of flies, which is functionally comparable to the blood and lymph of vertebrates. Further studies using cultured murine splenic vascular endothelial cells and human umbilical cord endothelial cells demonstrated that overexpression of ORF7a in these cells significantly activated and stimulated the release of VWF, leading to an increased rate and final coverage of Adamts-13-/- murine platelets on activated endothelial surfaces under arterial shear. Moreover, a soluble recombinant ORF7a could also activate human endothelial cells and trigger the release of VWF from Weibel–Palade bodies. Conclusion: We demonstrate for the first time that SARS-CoV-2 ORF7a may be one of the pathogenic factors contributing to COVID-19–associated thrombosis by activating the vascular endothelium to release ultralarge VWF, which promotes platelet adhesion and agglutination, and thrombus formation. Thus, a strategy specifically targeting VWF-platelet interaction, such as recombinant a disintegrin and metalloprotease with thrombospondin type 1 repeats, 13 (ADAMTS-13) and/or caplacizumab, may be efficacious in reducing COVID-19–associated thrombosis and mortality.http://www.sciencedirect.com/science/article/pii/S2475037925002717ADAMTS-13coagulationendotheliumHmlOrf7aSARS-CoV-2
spellingShingle Quan Zhang
Xiaohu Huang
Hangnoh Lee
Jin-Gu Lee
Szumam Liu
Shiwani Limbu
Malay K. Basu
Joyce van de Leemput
Felice D’Agnillo
Zhe Han
X. Long Zheng
SARS-CoV-2 ORF7a activates the endothelium to release von Willebrand factor that promotes thrombosis
Research and Practice in Thrombosis and Haemostasis
ADAMTS-13
coagulation
endothelium
Hml
Orf7a
SARS-CoV-2
title SARS-CoV-2 ORF7a activates the endothelium to release von Willebrand factor that promotes thrombosis
title_full SARS-CoV-2 ORF7a activates the endothelium to release von Willebrand factor that promotes thrombosis
title_fullStr SARS-CoV-2 ORF7a activates the endothelium to release von Willebrand factor that promotes thrombosis
title_full_unstemmed SARS-CoV-2 ORF7a activates the endothelium to release von Willebrand factor that promotes thrombosis
title_short SARS-CoV-2 ORF7a activates the endothelium to release von Willebrand factor that promotes thrombosis
title_sort sars cov 2 orf7a activates the endothelium to release von willebrand factor that promotes thrombosis
topic ADAMTS-13
coagulation
endothelium
Hml
Orf7a
SARS-CoV-2
url http://www.sciencedirect.com/science/article/pii/S2475037925002717
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