Addressing the pathophysiology of venous thrombosis and chronic kidney disease in sickle cell trait using a mouse model

Abstract: Sickle cell trait (SCT) is present in participants who possess a single copy of the βS-globin gene mutation. Although most affected individuals are asymptomatic, SCT is a well-established risk factor for venous thrombosis and renal complications, including chronic and end-stage kidney dise...

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Main Authors: Fatima Trebak, Mohammad O. Sako, Steven P. Grover, Karnsasin Seanoon, Izabela Pawlinski, Chatphatai Moonla, Michael W. Henderson, Vimal K. Derebail, Dougald M. Monroe, Patrick Ellsworth, Rafal Pawlinski, Malgorzata Kasztan, Nigel S. Key
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Blood Advances
Online Access:http://www.sciencedirect.com/science/article/pii/S2473952925001582
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author Fatima Trebak
Mohammad O. Sako
Steven P. Grover
Karnsasin Seanoon
Izabela Pawlinski
Chatphatai Moonla
Michael W. Henderson
Vimal K. Derebail
Dougald M. Monroe
Patrick Ellsworth
Rafal Pawlinski
Malgorzata Kasztan
Nigel S. Key
author_facet Fatima Trebak
Mohammad O. Sako
Steven P. Grover
Karnsasin Seanoon
Izabela Pawlinski
Chatphatai Moonla
Michael W. Henderson
Vimal K. Derebail
Dougald M. Monroe
Patrick Ellsworth
Rafal Pawlinski
Malgorzata Kasztan
Nigel S. Key
author_sort Fatima Trebak
collection DOAJ
description Abstract: Sickle cell trait (SCT) is present in participants who possess a single copy of the βS-globin gene mutation. Although most affected individuals are asymptomatic, SCT is a well-established risk factor for venous thrombosis and renal complications, including chronic and end-stage kidney disease. After prolonged hypoxia, SCT red blood cells (RBCs) can undergo sickling, and hypoxia-mediated RBC sickling can be enhanced by cellular dehydration, hyperosmolarity, and/or acidosis. Some or all of these conditions may be encountered in the nidus of venous thrombi and in the medulla of the kidney. We sought to determine whether Townes sickle trait (AS) mice develop kidney dysfunction and manifest enhanced venous thrombosis. We demonstrated that the harsh environment within the inner medulla induces RBC sickling in vitro and in vivo and is associated with kidney-related pathologies, including impaired urinary concentration, albuminuria, and declining renal function, closely mimicking those seen in human SCT. In the inferior vena cava model of venous thrombosis, extreme and prolonged hypoxia in the core of RBC-rich venous thrombi resulted in irreversible RBC sickling and larger clots in Townes AS mice than AA controls (littermates expressing hemoglobin A only). Our results support the use of Townes AS mice in future studies investigating mechanisms of venous thrombosis and chronic kidney disease in SCT.
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spelling doaj-art-85e0052b540d4636bdf0afa481d203922025-08-20T02:34:53ZengElsevierBlood Advances2473-95292025-06-019112709272110.1182/bloodadvances.2024015674Addressing the pathophysiology of venous thrombosis and chronic kidney disease in sickle cell trait using a mouse modelFatima Trebak0Mohammad O. Sako1Steven P. Grover2Karnsasin Seanoon3Izabela Pawlinski4Chatphatai Moonla5Michael W. Henderson6Vimal K. Derebail7Dougald M. Monroe8Patrick Ellsworth9Rafal Pawlinski10Malgorzata Kasztan11Nigel S. Key12Division of Hematology and Blood Research Center, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NCDivision of Hematology-Oncology, Department of Pediatrics, University of Alabama at Birmingham, Birmingham, ALDivision of Hematology and Blood Research Center, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NCDivision of Hematology and Blood Research Center, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NCDivision of Hematology and Blood Research Center, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NCDivision of Hematology and Blood Research Center, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NCDivision of Hematology and Blood Research Center, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NCDivision of Nephrology and Hypertension, Department of Medicine, UNC Kidney Center, University of North Carolina at Chapel Hill, Chapel Hill, NCDivision of Hematology and Blood Research Center, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NCDivision of Hematology and Blood Research Center, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NCDivision of Hematology and Blood Research Center, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NCDivision of Hematology-Oncology, Department of Pediatrics, University of Alabama at Birmingham, Birmingham, AL; Correspondence: Malgorzata Kasztan, Division of Hematology/Oncology, Department of Pediatrics, University of Alabama at Birmingham, 1918 University Blvd, MCLM 535, Birmingham, AL 35233;Division of Hematology and Blood Research Center, Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC; Nigel S. Key, Department of Medicine, University of North Carolina at Chapel Hill, 116 Manning Dr, 8008B Mary Ellen Jones, CB #7035, Chapel Hill, NC 27599;Abstract: Sickle cell trait (SCT) is present in participants who possess a single copy of the βS-globin gene mutation. Although most affected individuals are asymptomatic, SCT is a well-established risk factor for venous thrombosis and renal complications, including chronic and end-stage kidney disease. After prolonged hypoxia, SCT red blood cells (RBCs) can undergo sickling, and hypoxia-mediated RBC sickling can be enhanced by cellular dehydration, hyperosmolarity, and/or acidosis. Some or all of these conditions may be encountered in the nidus of venous thrombi and in the medulla of the kidney. We sought to determine whether Townes sickle trait (AS) mice develop kidney dysfunction and manifest enhanced venous thrombosis. We demonstrated that the harsh environment within the inner medulla induces RBC sickling in vitro and in vivo and is associated with kidney-related pathologies, including impaired urinary concentration, albuminuria, and declining renal function, closely mimicking those seen in human SCT. In the inferior vena cava model of venous thrombosis, extreme and prolonged hypoxia in the core of RBC-rich venous thrombi resulted in irreversible RBC sickling and larger clots in Townes AS mice than AA controls (littermates expressing hemoglobin A only). Our results support the use of Townes AS mice in future studies investigating mechanisms of venous thrombosis and chronic kidney disease in SCT.http://www.sciencedirect.com/science/article/pii/S2473952925001582
spellingShingle Fatima Trebak
Mohammad O. Sako
Steven P. Grover
Karnsasin Seanoon
Izabela Pawlinski
Chatphatai Moonla
Michael W. Henderson
Vimal K. Derebail
Dougald M. Monroe
Patrick Ellsworth
Rafal Pawlinski
Malgorzata Kasztan
Nigel S. Key
Addressing the pathophysiology of venous thrombosis and chronic kidney disease in sickle cell trait using a mouse model
Blood Advances
title Addressing the pathophysiology of venous thrombosis and chronic kidney disease in sickle cell trait using a mouse model
title_full Addressing the pathophysiology of venous thrombosis and chronic kidney disease in sickle cell trait using a mouse model
title_fullStr Addressing the pathophysiology of venous thrombosis and chronic kidney disease in sickle cell trait using a mouse model
title_full_unstemmed Addressing the pathophysiology of venous thrombosis and chronic kidney disease in sickle cell trait using a mouse model
title_short Addressing the pathophysiology of venous thrombosis and chronic kidney disease in sickle cell trait using a mouse model
title_sort addressing the pathophysiology of venous thrombosis and chronic kidney disease in sickle cell trait using a mouse model
url http://www.sciencedirect.com/science/article/pii/S2473952925001582
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