Modulating the platelet-mediated innate foreign body response to affect in situ vascular tissue engineering outcomes

Abstract The success of implanted tissue-engineered vascular grafts (TEVGs) relies on the coordinated inflammation and wound healing processes that simultaneously degrade the scaffold and guide the formation of a neovessel. Dysregulated responses can lead to aberrant remodeling (e.g., stenosis), imp...

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Main Authors: Mackenzie E. Turner, Jingru Che, Joseph T. Leland, Delaney J. Villarreal, Sahana Rajesh, Sugath Suravarapu, Kan N. Hor, Matthew G. Wiet, Bryce A. Kerlin, Tai Yi, Cameron A. Best, James W. Reinhardt, Christopher K. Breuer
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:npj Regenerative Medicine
Online Access:https://doi.org/10.1038/s41536-025-00419-w
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author Mackenzie E. Turner
Jingru Che
Joseph T. Leland
Delaney J. Villarreal
Sahana Rajesh
Sugath Suravarapu
Kan N. Hor
Matthew G. Wiet
Bryce A. Kerlin
Tai Yi
Cameron A. Best
James W. Reinhardt
Christopher K. Breuer
author_facet Mackenzie E. Turner
Jingru Che
Joseph T. Leland
Delaney J. Villarreal
Sahana Rajesh
Sugath Suravarapu
Kan N. Hor
Matthew G. Wiet
Bryce A. Kerlin
Tai Yi
Cameron A. Best
James W. Reinhardt
Christopher K. Breuer
author_sort Mackenzie E. Turner
collection DOAJ
description Abstract The success of implanted tissue-engineered vascular grafts (TEVGs) relies on the coordinated inflammation and wound healing processes that simultaneously degrade the scaffold and guide the formation of a neovessel. Dysregulated responses can lead to aberrant remodeling (e.g., stenosis), impacting the long-term outcome and functionality of the TEVG. We developed a TEVG that, despite demonstrating growth capacity in the clinic, exhibited an unexpectedly high incidence of stenosis, or narrowing of the graft lumen. This study identified platelet-mediated immune signaling via the lysosomal trafficking regulator (Lyst) as a key driver of stenosis. Lyst mutations significantly impaired platelet dense granule exocytosis yet preserved alpha granule secretion and adhesion to the biomaterial. Uncontrolled platelet aggregation, potentiated by dense granule signaling, results in the formation of a mural thrombus that remodels into occlusive neotissue. Importantly, inhibiting sustained platelet aggregation using the P2Y12 antagonist, prasugrel, is a successful strategy for optimizing neotissue formation and improving overall TEVG performance.
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spelling doaj-art-351bb342eb0b4f23a0bddab4881706e22025-08-20T04:01:53ZengNature Portfolionpj Regenerative Medicine2057-39952025-07-0110111210.1038/s41536-025-00419-wModulating the platelet-mediated innate foreign body response to affect in situ vascular tissue engineering outcomesMackenzie E. Turner0Jingru Che1Joseph T. Leland2Delaney J. Villarreal3Sahana Rajesh4Sugath Suravarapu5Kan N. Hor6Matthew G. Wiet7Bryce A. Kerlin8Tai Yi9Cameron A. Best10James W. Reinhardt11Christopher K. Breuer12Center for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalCenter for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalCenter for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalCenter for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalCenter for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalCenter for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalDepartment of Pediatrics, The Ohio State University College of MedicineCenter for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalCenter for Clinical and Translational Research, Research Institute at Nationwide Children’s HospitalCenter for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalCenter for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalCenter for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalCenter for Regenerative Medicine, Research Institute at Nationwide Children’s HospitalAbstract The success of implanted tissue-engineered vascular grafts (TEVGs) relies on the coordinated inflammation and wound healing processes that simultaneously degrade the scaffold and guide the formation of a neovessel. Dysregulated responses can lead to aberrant remodeling (e.g., stenosis), impacting the long-term outcome and functionality of the TEVG. We developed a TEVG that, despite demonstrating growth capacity in the clinic, exhibited an unexpectedly high incidence of stenosis, or narrowing of the graft lumen. This study identified platelet-mediated immune signaling via the lysosomal trafficking regulator (Lyst) as a key driver of stenosis. Lyst mutations significantly impaired platelet dense granule exocytosis yet preserved alpha granule secretion and adhesion to the biomaterial. Uncontrolled platelet aggregation, potentiated by dense granule signaling, results in the formation of a mural thrombus that remodels into occlusive neotissue. Importantly, inhibiting sustained platelet aggregation using the P2Y12 antagonist, prasugrel, is a successful strategy for optimizing neotissue formation and improving overall TEVG performance.https://doi.org/10.1038/s41536-025-00419-w
spellingShingle Mackenzie E. Turner
Jingru Che
Joseph T. Leland
Delaney J. Villarreal
Sahana Rajesh
Sugath Suravarapu
Kan N. Hor
Matthew G. Wiet
Bryce A. Kerlin
Tai Yi
Cameron A. Best
James W. Reinhardt
Christopher K. Breuer
Modulating the platelet-mediated innate foreign body response to affect in situ vascular tissue engineering outcomes
npj Regenerative Medicine
title Modulating the platelet-mediated innate foreign body response to affect in situ vascular tissue engineering outcomes
title_full Modulating the platelet-mediated innate foreign body response to affect in situ vascular tissue engineering outcomes
title_fullStr Modulating the platelet-mediated innate foreign body response to affect in situ vascular tissue engineering outcomes
title_full_unstemmed Modulating the platelet-mediated innate foreign body response to affect in situ vascular tissue engineering outcomes
title_short Modulating the platelet-mediated innate foreign body response to affect in situ vascular tissue engineering outcomes
title_sort modulating the platelet mediated innate foreign body response to affect in situ vascular tissue engineering outcomes
url https://doi.org/10.1038/s41536-025-00419-w
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