IL‐33‐Induced TREM2+ Macrophages Promote Pathological New Bone Formation Through CREG1‐IGF2R Axis in Ankylosing Spondylitis

Abstract Pathological new bone formation is the main cause of disability in ankylosing spondylitis (AS), and so far, it lacks a targeted therapy. Macrophages are central orchestrators of inflammation progression and tissue remodeling, but their contribution to pathological new bone formation has lar...

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Main Authors: Wenjun Hao, Siwen Chen, Hua Chao, Zihao Li, Hao Yang, Dongying Chen, Sifang Li, Shuai Zhang, Jingyu Zhang, Jianru Wang, Zemin Li, Xiang Li, Zhongping Zhan, Tangming Guan, Yiwen Zhang, Wende Li, Hui Liu
Format: Article
Language:English
Published: Wiley 2025-05-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202500952
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author Wenjun Hao
Siwen Chen
Hua Chao
Zihao Li
Hao Yang
Dongying Chen
Sifang Li
Shuai Zhang
Jingyu Zhang
Jianru Wang
Zemin Li
Xiang Li
Zhongping Zhan
Tangming Guan
Yiwen Zhang
Wende Li
Hui Liu
author_facet Wenjun Hao
Siwen Chen
Hua Chao
Zihao Li
Hao Yang
Dongying Chen
Sifang Li
Shuai Zhang
Jingyu Zhang
Jianru Wang
Zemin Li
Xiang Li
Zhongping Zhan
Tangming Guan
Yiwen Zhang
Wende Li
Hui Liu
author_sort Wenjun Hao
collection DOAJ
description Abstract Pathological new bone formation is the main cause of disability in ankylosing spondylitis (AS), and so far, it lacks a targeted therapy. Macrophages are central orchestrators of inflammation progression and tissue remodeling, but their contribution to pathological new bone formation has largely not been explored. Here, it is identified that TREM2+ macrophages predominated within the sites of new bone formation and adjacent to osteogenic precursor cells. In vivo, both depletion of macrophages and knockout of Trem2 significantly reduced pathological new bone formation in a collagen antibody‐induced arthritis (CAIA) model. Specifically, TREM2+ macrophages promoted osteogenic differentiation of ligament‐derived progenitor cells (LDPCs) by secreting CREG1, a secretory glycoprotein involved in cell differentiation and normal physiology. CREG1‐IGF2R‐PI3K‐AKT signaling pathway is involved in TREM2+ macrophage‐mediated pathological new bone formation. In addition, it is found that IL‐33 promoted TREM2+ macrophage differentiation through phosphorylation of STAT6. Targeting the above signalings alleviated new bone formation in the CAIA model. The findings highlight the critical role of IL‐33‐induced TREM2+ macrophages in pathological new bone formation and provide potential therapeutic targets for halting spinal ankylosis in AS.
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publishDate 2025-05-01
publisher Wiley
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spelling doaj-art-5d299b3ce6fd45008dae50d5a19f2ecc2025-08-20T03:25:16ZengWileyAdvanced Science2198-38442025-05-011218n/an/a10.1002/advs.202500952IL‐33‐Induced TREM2+ Macrophages Promote Pathological New Bone Formation Through CREG1‐IGF2R Axis in Ankylosing SpondylitisWenjun Hao0Siwen Chen1Hua Chao2Zihao Li3Hao Yang4Dongying Chen5Sifang Li6Shuai Zhang7Jingyu Zhang8Jianru Wang9Zemin Li10Xiang Li11Zhongping Zhan12Tangming Guan13Yiwen Zhang14Wende Li15Hui Liu16Department of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaDepartment of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaDepartment of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaDepartment of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaPediatric Orthopaedics Beijing Jishuitan Hospital Capital Medical University Beijing 102200 ChinaDepartment of Rheumatology and Immunology The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaDepartment of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaDepartment of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaDepartment of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaDepartment of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaDepartment of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaDepartment of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaDepartment of Rheumatology and Immunology The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaGuangdong Laboratory Animals Monitoring Institute Guangdong Key Laboratory of Laboratory Animals Guangzhou 510000 ChinaInstitute of Human Virology Department of Pathogen Biology and Biosecurity Key Laboratory of Tropical Disease Control of Ministry of Education Zhongshan School of Medicine Sun Yat‐sen University Guangzhou 510080 ChinaGuangdong Laboratory Animals Monitoring Institute Guangdong Key Laboratory of Laboratory Animals Guangzhou 510000 ChinaDepartment of Spine Surgery The First Affiliated Hospital Sun Yat‐sen University Guangzhou 510080 ChinaAbstract Pathological new bone formation is the main cause of disability in ankylosing spondylitis (AS), and so far, it lacks a targeted therapy. Macrophages are central orchestrators of inflammation progression and tissue remodeling, but their contribution to pathological new bone formation has largely not been explored. Here, it is identified that TREM2+ macrophages predominated within the sites of new bone formation and adjacent to osteogenic precursor cells. In vivo, both depletion of macrophages and knockout of Trem2 significantly reduced pathological new bone formation in a collagen antibody‐induced arthritis (CAIA) model. Specifically, TREM2+ macrophages promoted osteogenic differentiation of ligament‐derived progenitor cells (LDPCs) by secreting CREG1, a secretory glycoprotein involved in cell differentiation and normal physiology. CREG1‐IGF2R‐PI3K‐AKT signaling pathway is involved in TREM2+ macrophage‐mediated pathological new bone formation. In addition, it is found that IL‐33 promoted TREM2+ macrophage differentiation through phosphorylation of STAT6. Targeting the above signalings alleviated new bone formation in the CAIA model. The findings highlight the critical role of IL‐33‐induced TREM2+ macrophages in pathological new bone formation and provide potential therapeutic targets for halting spinal ankylosis in AS.https://doi.org/10.1002/advs.202500952ankylosing spondylitisCREG1IL33pathological new bone formationTREM2+ macrophages
spellingShingle Wenjun Hao
Siwen Chen
Hua Chao
Zihao Li
Hao Yang
Dongying Chen
Sifang Li
Shuai Zhang
Jingyu Zhang
Jianru Wang
Zemin Li
Xiang Li
Zhongping Zhan
Tangming Guan
Yiwen Zhang
Wende Li
Hui Liu
IL‐33‐Induced TREM2+ Macrophages Promote Pathological New Bone Formation Through CREG1‐IGF2R Axis in Ankylosing Spondylitis
Advanced Science
ankylosing spondylitis
CREG1
IL33
pathological new bone formation
TREM2+ macrophages
title IL‐33‐Induced TREM2+ Macrophages Promote Pathological New Bone Formation Through CREG1‐IGF2R Axis in Ankylosing Spondylitis
title_full IL‐33‐Induced TREM2+ Macrophages Promote Pathological New Bone Formation Through CREG1‐IGF2R Axis in Ankylosing Spondylitis
title_fullStr IL‐33‐Induced TREM2+ Macrophages Promote Pathological New Bone Formation Through CREG1‐IGF2R Axis in Ankylosing Spondylitis
title_full_unstemmed IL‐33‐Induced TREM2+ Macrophages Promote Pathological New Bone Formation Through CREG1‐IGF2R Axis in Ankylosing Spondylitis
title_short IL‐33‐Induced TREM2+ Macrophages Promote Pathological New Bone Formation Through CREG1‐IGF2R Axis in Ankylosing Spondylitis
title_sort il 33 induced trem2 macrophages promote pathological new bone formation through creg1 igf2r axis in ankylosing spondylitis
topic ankylosing spondylitis
CREG1
IL33
pathological new bone formation
TREM2+ macrophages
url https://doi.org/10.1002/advs.202500952
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