Thrombospondin-1 mitigates osteoarthritis progression by inhibiting mechanical stress-induced chondrocyte ferroptosis via the integrin/YAP pathway

IntroductionOsteoarthritis in weight-bearing joints significantly impacts the quality of life in middle-aged and elderly individuals. Abnormal mechanical stress can induce chondrocytes ferroptosis, thereby accelerating the progression of osteoarthritis. In this study, we investigated the therapeutic...

Full description

Saved in:
Bibliographic Details
Main Authors: Shaoyi Wang, Xiaocong Zhou, Fujian Zhang, Haoxin Zhai, Yuanqiang Zhang, Yongyuan Guo
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1577234/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849328594890784768
author Shaoyi Wang
Shaoyi Wang
Xiaocong Zhou
Fujian Zhang
Haoxin Zhai
Yuanqiang Zhang
Yuanqiang Zhang
Yongyuan Guo
author_facet Shaoyi Wang
Shaoyi Wang
Xiaocong Zhou
Fujian Zhang
Haoxin Zhai
Yuanqiang Zhang
Yuanqiang Zhang
Yongyuan Guo
author_sort Shaoyi Wang
collection DOAJ
description IntroductionOsteoarthritis in weight-bearing joints significantly impacts the quality of life in middle-aged and elderly individuals. Abnormal mechanical stress can induce chondrocytes ferroptosis, thereby accelerating the progression of osteoarthritis. In this study, we investigated the therapeutic effects of targeting chondrocyte ferroptosis to delay the progression of osteoarthritis and identified a potential therapeutic target.MethodsThrough transcriptomic sequencing analysis, we identified a potential association between thrombospondin-1 (THBS1) and mechanical stress-induced chondrocyte ferroptosis. In this study we used via adeno-associated virus-mediated THBS1 overexpression, cell pressurization model and GPX4-conditional knockout (Col2a1-CreERT: GPX4flox/flox) mice to verify the regulatory effect of THBS1 on chondrocytes ferroptosis. Additionally, protein interaction network analysis, immunofluorescence co-localization, and co-immunoprecipitation were conducted to investigate the mechanism by which THBS1 modulates chondrocytes ferroptosis.ResultsThe expression of THBS1 protein was reduced in load-bearing cartilage tissue in humans. THBS1 suppressed chondrocytes ferroptosis induced by excessive mechanical stress. Immunofluorescence co-localization and CO-IP experiments indicated that integrin αV/β1 serves as the membrane receptor through which THBS1 regulates chondrocyte ferroptosis under mechanical stress. Upon activation, integrin αV/β1 modulated YAP1 nuclear translocation, thereby affecting GPX4 activity. Intra-articular injection of THBS1 synthetic peptides effectively reduced cartilage damage in mouse OA models, protecting articular cartilage and slowing the progression of osteoarthritis.DiscussionOur results indicate THBS1 regulates mechanical stress-induced chondrocyte ferroptosis through the Integrin/YAP pathway. Furthermore, THBS1 effectively slows the progression of osteoarthritis and protects articular cartilage.
format Article
id doaj-art-623a571d74b84b58aee5349e00feb760
institution Kabale University
issn 1664-3224
language English
publishDate 2025-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj-art-623a571d74b84b58aee5349e00feb7602025-08-20T03:47:33ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-05-011610.3389/fimmu.2025.15772341577234Thrombospondin-1 mitigates osteoarthritis progression by inhibiting mechanical stress-induced chondrocyte ferroptosis via the integrin/YAP pathwayShaoyi Wang0Shaoyi Wang1Xiaocong Zhou2Fujian Zhang3Haoxin Zhai4Yuanqiang Zhang5Yuanqiang Zhang6Yongyuan Guo7Department of Orthopedics, Qilu Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, ChinaQilu Hospital of Shandong University Spine and Spinal Cord Disease Research Center - International Chinese Musculoskeletal Research Society (ICMRS) Collaborating Center for Orthopedic Translational Research, Shandong University, Jinan, Shandong, ChinaHealth Management Centre, The First Affiliated Hospital of Shandong First Medical University, Jinan, Shandong, ChinaDepartment of Orthopedics, Qilu Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, ChinaDepartment of Orthopedics, Qilu Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, ChinaDepartment of Orthopedics, Qilu Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, ChinaQilu Hospital of Shandong University Spine and Spinal Cord Disease Research Center - International Chinese Musculoskeletal Research Society (ICMRS) Collaborating Center for Orthopedic Translational Research, Shandong University, Jinan, Shandong, ChinaDepartment of Orthopedics, Qilu Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, ChinaIntroductionOsteoarthritis in weight-bearing joints significantly impacts the quality of life in middle-aged and elderly individuals. Abnormal mechanical stress can induce chondrocytes ferroptosis, thereby accelerating the progression of osteoarthritis. In this study, we investigated the therapeutic effects of targeting chondrocyte ferroptosis to delay the progression of osteoarthritis and identified a potential therapeutic target.MethodsThrough transcriptomic sequencing analysis, we identified a potential association between thrombospondin-1 (THBS1) and mechanical stress-induced chondrocyte ferroptosis. In this study we used via adeno-associated virus-mediated THBS1 overexpression, cell pressurization model and GPX4-conditional knockout (Col2a1-CreERT: GPX4flox/flox) mice to verify the regulatory effect of THBS1 on chondrocytes ferroptosis. Additionally, protein interaction network analysis, immunofluorescence co-localization, and co-immunoprecipitation were conducted to investigate the mechanism by which THBS1 modulates chondrocytes ferroptosis.ResultsThe expression of THBS1 protein was reduced in load-bearing cartilage tissue in humans. THBS1 suppressed chondrocytes ferroptosis induced by excessive mechanical stress. Immunofluorescence co-localization and CO-IP experiments indicated that integrin αV/β1 serves as the membrane receptor through which THBS1 regulates chondrocyte ferroptosis under mechanical stress. Upon activation, integrin αV/β1 modulated YAP1 nuclear translocation, thereby affecting GPX4 activity. Intra-articular injection of THBS1 synthetic peptides effectively reduced cartilage damage in mouse OA models, protecting articular cartilage and slowing the progression of osteoarthritis.DiscussionOur results indicate THBS1 regulates mechanical stress-induced chondrocyte ferroptosis through the Integrin/YAP pathway. Furthermore, THBS1 effectively slows the progression of osteoarthritis and protects articular cartilage.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1577234/fullosteoarthritisferroptosismechanical stressTHBS1chondrocytes
spellingShingle Shaoyi Wang
Shaoyi Wang
Xiaocong Zhou
Fujian Zhang
Haoxin Zhai
Yuanqiang Zhang
Yuanqiang Zhang
Yongyuan Guo
Thrombospondin-1 mitigates osteoarthritis progression by inhibiting mechanical stress-induced chondrocyte ferroptosis via the integrin/YAP pathway
Frontiers in Immunology
osteoarthritis
ferroptosis
mechanical stress
THBS1
chondrocytes
title Thrombospondin-1 mitigates osteoarthritis progression by inhibiting mechanical stress-induced chondrocyte ferroptosis via the integrin/YAP pathway
title_full Thrombospondin-1 mitigates osteoarthritis progression by inhibiting mechanical stress-induced chondrocyte ferroptosis via the integrin/YAP pathway
title_fullStr Thrombospondin-1 mitigates osteoarthritis progression by inhibiting mechanical stress-induced chondrocyte ferroptosis via the integrin/YAP pathway
title_full_unstemmed Thrombospondin-1 mitigates osteoarthritis progression by inhibiting mechanical stress-induced chondrocyte ferroptosis via the integrin/YAP pathway
title_short Thrombospondin-1 mitigates osteoarthritis progression by inhibiting mechanical stress-induced chondrocyte ferroptosis via the integrin/YAP pathway
title_sort thrombospondin 1 mitigates osteoarthritis progression by inhibiting mechanical stress induced chondrocyte ferroptosis via the integrin yap pathway
topic osteoarthritis
ferroptosis
mechanical stress
THBS1
chondrocytes
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1577234/full
work_keys_str_mv AT shaoyiwang thrombospondin1mitigatesosteoarthritisprogressionbyinhibitingmechanicalstressinducedchondrocyteferroptosisviatheintegrinyappathway
AT shaoyiwang thrombospondin1mitigatesosteoarthritisprogressionbyinhibitingmechanicalstressinducedchondrocyteferroptosisviatheintegrinyappathway
AT xiaocongzhou thrombospondin1mitigatesosteoarthritisprogressionbyinhibitingmechanicalstressinducedchondrocyteferroptosisviatheintegrinyappathway
AT fujianzhang thrombospondin1mitigatesosteoarthritisprogressionbyinhibitingmechanicalstressinducedchondrocyteferroptosisviatheintegrinyappathway
AT haoxinzhai thrombospondin1mitigatesosteoarthritisprogressionbyinhibitingmechanicalstressinducedchondrocyteferroptosisviatheintegrinyappathway
AT yuanqiangzhang thrombospondin1mitigatesosteoarthritisprogressionbyinhibitingmechanicalstressinducedchondrocyteferroptosisviatheintegrinyappathway
AT yuanqiangzhang thrombospondin1mitigatesosteoarthritisprogressionbyinhibitingmechanicalstressinducedchondrocyteferroptosisviatheintegrinyappathway
AT yongyuanguo thrombospondin1mitigatesosteoarthritisprogressionbyinhibitingmechanicalstressinducedchondrocyteferroptosisviatheintegrinyappathway