Endothelial Cell Senescence in Marfan Syndrome: Pathogenesis and Therapeutic Potential of TGF‐β Pathway Inhibition

Background Marfan syndrome (MFS) is a heritable connective tissue disorder caused by mutations in the Fibrillin‐1 gene, which encodes the extracellular matrix protein fibrillin‐1. Patients with MFS are predisposed to aortic aneurysms and dissections, significantly contributing to mortality. Emerging...

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Main Authors: Yuhao Chen, Yuankang Zhu, Xiaoli Ren, Lu Ding, Yubin Xu, Miqi Zhou, Runze Dong, Peifeng Jin, Xiufang Chen, Xiaofang Fan, Ming Li, Yongsheng Gong, Yongyu Wang
Format: Article
Language:English
Published: Wiley 2025-05-01
Series:Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
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Online Access:https://www.ahajournals.org/doi/10.1161/JAHA.124.037826
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author Yuhao Chen
Yuankang Zhu
Xiaoli Ren
Lu Ding
Yubin Xu
Miqi Zhou
Runze Dong
Peifeng Jin
Xiufang Chen
Xiaofang Fan
Ming Li
Yongsheng Gong
Yongyu Wang
author_facet Yuhao Chen
Yuankang Zhu
Xiaoli Ren
Lu Ding
Yubin Xu
Miqi Zhou
Runze Dong
Peifeng Jin
Xiufang Chen
Xiaofang Fan
Ming Li
Yongsheng Gong
Yongyu Wang
author_sort Yuhao Chen
collection DOAJ
description Background Marfan syndrome (MFS) is a heritable connective tissue disorder caused by mutations in the Fibrillin‐1 gene, which encodes the extracellular matrix protein fibrillin‐1. Patients with MFS are predisposed to aortic aneurysms and dissections, significantly contributing to mortality. Emerging evidence suggests that endothelial cell (EC) senescence plays a critical role in the pathogenesis of aortic aneurysms in MFS. This study aims to elucidate the role of EC senescence in the development of aortic aneurysms in MFS using a vascular model derived from human induced pluripotent stem cells. Methods and Results We generated human induced pluripotent stem cells lines from 2 patients with MFS carrying specific Fibrillin‐1 mutations and differentiated these into ECs. These MFS–hiPSC‐derived ECs were characterized using immunofluorescence, reverse transcription‐quantitative polymerase chain reaction, and Western blotting. Functional assays including cell proliferation, scratch wound, tube formation, NO content detection, and senescence‐associated β‐galactosidase staining were conducted. RNA sequencing was performed to elucidate underlying signaling pathways, and pharmacological inhibition of the transforming growth factor‐beta pathway was assessed for its therapeutic potential. MFS–hiPSC‐derived ECs recapitulated the pathological features observed in Marfan aortas, particularly pronounced cellular senescence, decreased cell proliferation, and abnormal transforming growth factor‐beta and NF‐κB signaling. These senescent ECs exhibited diminished proliferative and migratory capacities, reduced NO signaling, increased production of inflammatory cytokines, and attenuated responses to inflammatory stimuli. Importantly, senescence and dysfunction in MFS‐hiPSCderived ECs were ameliorated by transforming growth factor‐beta signaling pathway inhibitor, SB‐431542, suggesting a potential therapeutic strategy. Conclusions This study highlights the pivotal role of endothelial cell senescence in the pathogenesis of aortic aneurysms in MFS. Our human induced pluripotent stem cells–based disease model provides new insights into the disease mechanisms and underscores the potential of targeting the transforming growth factor‐beta pathway to mitigate endothelial dysfunction and senescence, offering a promising therapeutic avenue for MFS.
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spelling doaj-art-cea7ece8649746f38edab18fef7fe2eb2025-08-20T02:26:28ZengWileyJournal of the American Heart Association: Cardiovascular and Cerebrovascular Disease2047-99802025-05-0114910.1161/JAHA.124.037826Endothelial Cell Senescence in Marfan Syndrome: Pathogenesis and Therapeutic Potential of TGF‐β Pathway InhibitionYuhao Chen0Yuankang Zhu1Xiaoli Ren2Lu Ding3Yubin Xu4Miqi Zhou5Runze Dong6Peifeng Jin7Xiufang Chen8Xiaofang Fan9Ming Li10Yongsheng Gong11Yongyu Wang12Department of Cell Biology, Institute of Hypoxia Medicine, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaDepartment of Gerontology Xinhua Hospital, Shanghai Jiao Tong University School of Medicine Shanghai ChinaDepartment of Cell Biology, Institute of Hypoxia Medicine, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaDepartment of Cell Biology, Institute of Hypoxia Medicine, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaDepartment of Cell Biology, Institute of Hypoxia Medicine, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaDepartment of Cell Biology, Institute of Hypoxia Medicine, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaDepartment of Cell Biology, Institute of Hypoxia Medicine, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaDepartment of Cardiac Surgery The First Affiliated Hospital of Wenzhou Medical University Zhejiang ChinaDepartment of Biochemistry and Molecular Biology, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaDepartment of Cell Biology, Institute of Hypoxia Medicine, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaCardiac Regeneration Research Institute, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaDepartment of Cell Biology, Institute of Hypoxia Medicine, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaDepartment of Cell Biology, Institute of Hypoxia Medicine, School of Basic Medical Sciences Wenzhou Medical University Zhejiang ChinaBackground Marfan syndrome (MFS) is a heritable connective tissue disorder caused by mutations in the Fibrillin‐1 gene, which encodes the extracellular matrix protein fibrillin‐1. Patients with MFS are predisposed to aortic aneurysms and dissections, significantly contributing to mortality. Emerging evidence suggests that endothelial cell (EC) senescence plays a critical role in the pathogenesis of aortic aneurysms in MFS. This study aims to elucidate the role of EC senescence in the development of aortic aneurysms in MFS using a vascular model derived from human induced pluripotent stem cells. Methods and Results We generated human induced pluripotent stem cells lines from 2 patients with MFS carrying specific Fibrillin‐1 mutations and differentiated these into ECs. These MFS–hiPSC‐derived ECs were characterized using immunofluorescence, reverse transcription‐quantitative polymerase chain reaction, and Western blotting. Functional assays including cell proliferation, scratch wound, tube formation, NO content detection, and senescence‐associated β‐galactosidase staining were conducted. RNA sequencing was performed to elucidate underlying signaling pathways, and pharmacological inhibition of the transforming growth factor‐beta pathway was assessed for its therapeutic potential. MFS–hiPSC‐derived ECs recapitulated the pathological features observed in Marfan aortas, particularly pronounced cellular senescence, decreased cell proliferation, and abnormal transforming growth factor‐beta and NF‐κB signaling. These senescent ECs exhibited diminished proliferative and migratory capacities, reduced NO signaling, increased production of inflammatory cytokines, and attenuated responses to inflammatory stimuli. Importantly, senescence and dysfunction in MFS‐hiPSCderived ECs were ameliorated by transforming growth factor‐beta signaling pathway inhibitor, SB‐431542, suggesting a potential therapeutic strategy. Conclusions This study highlights the pivotal role of endothelial cell senescence in the pathogenesis of aortic aneurysms in MFS. Our human induced pluripotent stem cells–based disease model provides new insights into the disease mechanisms and underscores the potential of targeting the transforming growth factor‐beta pathway to mitigate endothelial dysfunction and senescence, offering a promising therapeutic avenue for MFS.https://www.ahajournals.org/doi/10.1161/JAHA.124.037826endothelial cell senescencefibrillin‐1induced pluripotent stem cellsMarfan syndromeTGF‐β
spellingShingle Yuhao Chen
Yuankang Zhu
Xiaoli Ren
Lu Ding
Yubin Xu
Miqi Zhou
Runze Dong
Peifeng Jin
Xiufang Chen
Xiaofang Fan
Ming Li
Yongsheng Gong
Yongyu Wang
Endothelial Cell Senescence in Marfan Syndrome: Pathogenesis and Therapeutic Potential of TGF‐β Pathway Inhibition
Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
endothelial cell senescence
fibrillin‐1
induced pluripotent stem cells
Marfan syndrome
TGF‐β
title Endothelial Cell Senescence in Marfan Syndrome: Pathogenesis and Therapeutic Potential of TGF‐β Pathway Inhibition
title_full Endothelial Cell Senescence in Marfan Syndrome: Pathogenesis and Therapeutic Potential of TGF‐β Pathway Inhibition
title_fullStr Endothelial Cell Senescence in Marfan Syndrome: Pathogenesis and Therapeutic Potential of TGF‐β Pathway Inhibition
title_full_unstemmed Endothelial Cell Senescence in Marfan Syndrome: Pathogenesis and Therapeutic Potential of TGF‐β Pathway Inhibition
title_short Endothelial Cell Senescence in Marfan Syndrome: Pathogenesis and Therapeutic Potential of TGF‐β Pathway Inhibition
title_sort endothelial cell senescence in marfan syndrome pathogenesis and therapeutic potential of tgf β pathway inhibition
topic endothelial cell senescence
fibrillin‐1
induced pluripotent stem cells
Marfan syndrome
TGF‐β
url https://www.ahajournals.org/doi/10.1161/JAHA.124.037826
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