Soluble immune checkpoint landscape in sickle cell disease links systemic inflammation, autoimmunity, and pain

BackgroundSickle cell disease (SCD) is a chronic condition characterized by inflammation, immune dysregulation, and debilitating pain.AimThis study investigates soluble immune checkpoints (sICPs) and their associations with inflammatory mediators, immune cell profiles, autoantibodies, and clinical o...

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Main Authors: Wei Li, Andrew Q. Pucka, Lina Houran, Xiaoqing Huang, Candice Debats, Brandon A. Reyes, Andrew R. W. O’Brien, Qigui Yu, Ying Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-07-01
Series:Frontiers in Hematology
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Online Access:https://www.frontiersin.org/articles/10.3389/frhem.2025.1580009/full
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author Wei Li
Andrew Q. Pucka
Lina Houran
Xiaoqing Huang
Candice Debats
Brandon A. Reyes
Andrew R. W. O’Brien
Qigui Yu
Ying Wang
Ying Wang
author_facet Wei Li
Andrew Q. Pucka
Lina Houran
Xiaoqing Huang
Candice Debats
Brandon A. Reyes
Andrew R. W. O’Brien
Qigui Yu
Ying Wang
Ying Wang
author_sort Wei Li
collection DOAJ
description BackgroundSickle cell disease (SCD) is a chronic condition characterized by inflammation, immune dysregulation, and debilitating pain.AimThis study investigates soluble immune checkpoints (sICPs) and their associations with inflammatory mediators, immune cell profiles, autoantibodies, and clinical outcomes in SCD.MethodPeripheral blood samples from 50 SCD patients and 40 demographic-matched healthy controls (HCs) were analyzed for 37 sICPs, 80 inflammatory mediators, and 18 autoantibodies using multiplex assays, alongside immune cell profiles via flow cytometry. Pain and quality of life (QoL) were assessed through patient-reported outcome measures (PROMs).ResultsTwenty-three sICPs, including arginase-1, BTLA, CD27, CD28, CD47, CD80, CD96, CD134, CD137, CD152, GITR, HVEM, IDO, LAG-3, MICA, MICB, Nectin-2, PD-1, Siglec-7, Siglec-9, TIM-3, TIMD-4, and VISTA, were significantly elevated in SCD patients compared to HCs. These sICPs correlated with multiple proinflammatory mediators (e.g., IL-18), autoantibodies (e.g., MPO), and immune cell activation markers (e.g., CD38/HLA-DR on CD8 T cells). Notably, CD28, CD152, HVEM, and VISTA were strongly associated with systemic inflammation and immune cell activation, while BTLA, LAG-3, PD-1, and CD80 correlated with pain and anxiety scores and QoL.ConclusionThis study highlights complex interactions between sICPs, immune activation, inflammation, and clinical outcomes in SCD, underscoring their potential as biomarkers or therapeutic targets to alleviate inflammation and improve QoL in this challenging clinical population.
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spelling doaj-art-ce34aa8c360e43b596cb3dc3b38ba0a62025-08-20T03:17:55ZengFrontiers Media S.A.Frontiers in Hematology2813-39352025-07-01410.3389/frhem.2025.15800091580009Soluble immune checkpoint landscape in sickle cell disease links systemic inflammation, autoimmunity, and painWei Li0Andrew Q. Pucka1Lina Houran2Xiaoqing Huang3Candice Debats4Brandon A. Reyes5Andrew R. W. O’Brien6Qigui Yu7Ying Wang8Ying Wang9Department of Microbiology and Immunology, Indiana University School of Medicine, Indianapolis, IN, United StatesDepartment of Anesthesia, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, United StatesDepartment of Anesthesia, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, United StatesDepartment of Biostatistics and Health Data Science, Indiana University School of Medicine, Indianapolis, IN, United StatesDepartment of Anesthesia, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, United StatesDepartment of Anesthesia, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, United StatesDivision of Hematology/Oncology, Department of Medicine, Indiana University School of Medicine, Indianapolis, IN, United StatesDepartment of Microbiology and Immunology, Indiana University School of Medicine, Indianapolis, IN, United StatesDepartment of Anesthesia, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, United StatesDivision of Hematology/Oncology, Department of Medicine, Indiana University School of Medicine, Indianapolis, IN, United StatesBackgroundSickle cell disease (SCD) is a chronic condition characterized by inflammation, immune dysregulation, and debilitating pain.AimThis study investigates soluble immune checkpoints (sICPs) and their associations with inflammatory mediators, immune cell profiles, autoantibodies, and clinical outcomes in SCD.MethodPeripheral blood samples from 50 SCD patients and 40 demographic-matched healthy controls (HCs) were analyzed for 37 sICPs, 80 inflammatory mediators, and 18 autoantibodies using multiplex assays, alongside immune cell profiles via flow cytometry. Pain and quality of life (QoL) were assessed through patient-reported outcome measures (PROMs).ResultsTwenty-three sICPs, including arginase-1, BTLA, CD27, CD28, CD47, CD80, CD96, CD134, CD137, CD152, GITR, HVEM, IDO, LAG-3, MICA, MICB, Nectin-2, PD-1, Siglec-7, Siglec-9, TIM-3, TIMD-4, and VISTA, were significantly elevated in SCD patients compared to HCs. These sICPs correlated with multiple proinflammatory mediators (e.g., IL-18), autoantibodies (e.g., MPO), and immune cell activation markers (e.g., CD38/HLA-DR on CD8 T cells). Notably, CD28, CD152, HVEM, and VISTA were strongly associated with systemic inflammation and immune cell activation, while BTLA, LAG-3, PD-1, and CD80 correlated with pain and anxiety scores and QoL.ConclusionThis study highlights complex interactions between sICPs, immune activation, inflammation, and clinical outcomes in SCD, underscoring their potential as biomarkers or therapeutic targets to alleviate inflammation and improve QoL in this challenging clinical population.https://www.frontiersin.org/articles/10.3389/frhem.2025.1580009/fullsickle cell diseasesoluble immune checkpointsinflammationautoantibodiessteady-state conditionvaso-occlusive crisis
spellingShingle Wei Li
Andrew Q. Pucka
Lina Houran
Xiaoqing Huang
Candice Debats
Brandon A. Reyes
Andrew R. W. O’Brien
Qigui Yu
Ying Wang
Ying Wang
Soluble immune checkpoint landscape in sickle cell disease links systemic inflammation, autoimmunity, and pain
Frontiers in Hematology
sickle cell disease
soluble immune checkpoints
inflammation
autoantibodies
steady-state condition
vaso-occlusive crisis
title Soluble immune checkpoint landscape in sickle cell disease links systemic inflammation, autoimmunity, and pain
title_full Soluble immune checkpoint landscape in sickle cell disease links systemic inflammation, autoimmunity, and pain
title_fullStr Soluble immune checkpoint landscape in sickle cell disease links systemic inflammation, autoimmunity, and pain
title_full_unstemmed Soluble immune checkpoint landscape in sickle cell disease links systemic inflammation, autoimmunity, and pain
title_short Soluble immune checkpoint landscape in sickle cell disease links systemic inflammation, autoimmunity, and pain
title_sort soluble immune checkpoint landscape in sickle cell disease links systemic inflammation autoimmunity and pain
topic sickle cell disease
soluble immune checkpoints
inflammation
autoantibodies
steady-state condition
vaso-occlusive crisis
url https://www.frontiersin.org/articles/10.3389/frhem.2025.1580009/full
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