Single‐Cell Analysis Clarifies Pathological Heterogeneity in Tenosynovial Giant Cell Tumor and Identifies Biomarkers for Predicting Disease Recurrence

Abstract Diffuse‐type tenosynovial giant cell tumor (D‐TGCT) and localized‐type tenosynovial giant cell tumor (L‐TGCT) share common genomic aberrations and histopathological features, but the former has a more aggressive nature and a higher recurrence rate, leading to worse prognoses for patients. I...

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Main Authors: Yubin Xie, Chen Chen, Fei Wu, Yiman Peng, Jing Su, Yang Zhao, Hongjie Huang, Zhong Alan Li, Yin Pei, Wencui Li, Yi He, Tianchen Xue, Chenxi Cao, Sui Peng, Xin Zhang, Weidong Song
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202415835
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author Yubin Xie
Chen Chen
Fei Wu
Yiman Peng
Jing Su
Yang Zhao
Hongjie Huang
Zhong Alan Li
Yin Pei
Wencui Li
Yi He
Tianchen Xue
Chenxi Cao
Sui Peng
Xin Zhang
Weidong Song
author_facet Yubin Xie
Chen Chen
Fei Wu
Yiman Peng
Jing Su
Yang Zhao
Hongjie Huang
Zhong Alan Li
Yin Pei
Wencui Li
Yi He
Tianchen Xue
Chenxi Cao
Sui Peng
Xin Zhang
Weidong Song
author_sort Yubin Xie
collection DOAJ
description Abstract Diffuse‐type tenosynovial giant cell tumor (D‐TGCT) and localized‐type tenosynovial giant cell tumor (L‐TGCT) share common genomic aberrations and histopathological features, but the former has a more aggressive nature and a higher recurrence rate, leading to worse prognoses for patients. In this study, single‐cell RNA sequencing (scRNA‐seq) on human D‐TGCT and L‐TGCT lesions is conducted to discover transcriptional differences. A unique cluster of tumor cells in D‐TGCT is identified that regulated differentiation of CD34+ fibroblasts into MMP3+ fibroblasts or APOE+ fibroblasts via COL6A3 − (ITGAV + ITGB8) interaction. The APOE+ fibroblasts further activated IL‐1B+CCL20+ macrophages through the CXCL12/CXCR4 axis. IL‐1B+CCL20+ macrophages and MMP3+ fibroblasts participated in local aggression of D‐TGCT. Two effective biomarkers, ROR1 and PRKD1 are also identified and validated, to predict disease recurrence. This study not only clarified the underlying mechanisms of aggressive behavior in D‐TGCT but also provided a theoretical basis and potential targets for intervention into and treatment of this disease.
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spelling doaj-art-18e80bc6b86544a3bc1dd379985c262f2025-08-20T03:36:45ZengWileyAdvanced Science2198-38442025-07-011226n/an/a10.1002/advs.202415835Single‐Cell Analysis Clarifies Pathological Heterogeneity in Tenosynovial Giant Cell Tumor and Identifies Biomarkers for Predicting Disease RecurrenceYubin Xie0Chen Chen1Fei Wu2Yiman Peng3Jing Su4Yang Zhao5Hongjie Huang6Zhong Alan Li7Yin Pei8Wencui Li9Yi He10Tianchen Xue11Chenxi Cao12Sui Peng13Xin Zhang14Weidong Song15Institute of Precision Medicine The First Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 518000 P. R. ChinaInstitute of Precision Medicine The First Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 518000 P. R. ChinaDepartment of Sports Medicine Peking University Third Hospital 49 North Garden Road, Haidian District Beijing 100191 P. R. ChinaDepartment of Sports Medicine Peking University Third Hospital 49 North Garden Road, Haidian District Beijing 100191 P. R. ChinaDepartment of Pathology School of Basic Medical Sciences Peking University Third Hospital Peking University Health Science Center Beijing 100191 P. R. ChinaDepartment of Laboratory Medicine Peking University Third Hospital 49 North Garden Road, Haidian District Beijing 100191 P. R. ChinaDepartment of Sports Medicine Peking University Third Hospital 49 North Garden Road, Haidian District Beijing 100191 P. R. ChinaDepartment of Biomedical Engineering The Chinese University of Hong Kong Hong Kong SAR 999077 ChinaDepartment of Sports Medicine Peking University Third Hospital 49 North Garden Road, Haidian District Beijing 100191 P. R. ChinaHand and Foot Surgery Department The First Affiliated Hospital of Shenzhen University Shenzhen Second People's Hospital Shenzhen Guangdong 518035 P. R. ChinaEmergency Trauma Center Fifth Affiliated Hospital of Guangzhou Medical University Guangzhou Guangdong 510700 P. R. ChinaDepartment of Pathology The First Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 518000 P. R. ChinaDepartment of Sports Medicine Peking University Third Hospital 49 North Garden Road, Haidian District Beijing 100191 P. R. ChinaInstitute of Precision Medicine The First Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 518000 P. R. ChinaDepartment of Sports Medicine Peking University Third Hospital 49 North Garden Road, Haidian District Beijing 100191 P. R. ChinaTrauma Orthopedics Foot and Ankle Surgery Sun Yat‐Sen Memorial Hospital Sun Yat‐Sen University 107 Yanjiangxi Road Guangzhou Guangdong 510120 P. R. ChinaAbstract Diffuse‐type tenosynovial giant cell tumor (D‐TGCT) and localized‐type tenosynovial giant cell tumor (L‐TGCT) share common genomic aberrations and histopathological features, but the former has a more aggressive nature and a higher recurrence rate, leading to worse prognoses for patients. In this study, single‐cell RNA sequencing (scRNA‐seq) on human D‐TGCT and L‐TGCT lesions is conducted to discover transcriptional differences. A unique cluster of tumor cells in D‐TGCT is identified that regulated differentiation of CD34+ fibroblasts into MMP3+ fibroblasts or APOE+ fibroblasts via COL6A3 − (ITGAV + ITGB8) interaction. The APOE+ fibroblasts further activated IL‐1B+CCL20+ macrophages through the CXCL12/CXCR4 axis. IL‐1B+CCL20+ macrophages and MMP3+ fibroblasts participated in local aggression of D‐TGCT. Two effective biomarkers, ROR1 and PRKD1 are also identified and validated, to predict disease recurrence. This study not only clarified the underlying mechanisms of aggressive behavior in D‐TGCT but also provided a theoretical basis and potential targets for intervention into and treatment of this disease.https://doi.org/10.1002/advs.202415835local aggressionrecurrencesingle‐cell RNA sequencingtenosynovial giant cell tumors
spellingShingle Yubin Xie
Chen Chen
Fei Wu
Yiman Peng
Jing Su
Yang Zhao
Hongjie Huang
Zhong Alan Li
Yin Pei
Wencui Li
Yi He
Tianchen Xue
Chenxi Cao
Sui Peng
Xin Zhang
Weidong Song
Single‐Cell Analysis Clarifies Pathological Heterogeneity in Tenosynovial Giant Cell Tumor and Identifies Biomarkers for Predicting Disease Recurrence
Advanced Science
local aggression
recurrence
single‐cell RNA sequencing
tenosynovial giant cell tumors
title Single‐Cell Analysis Clarifies Pathological Heterogeneity in Tenosynovial Giant Cell Tumor and Identifies Biomarkers for Predicting Disease Recurrence
title_full Single‐Cell Analysis Clarifies Pathological Heterogeneity in Tenosynovial Giant Cell Tumor and Identifies Biomarkers for Predicting Disease Recurrence
title_fullStr Single‐Cell Analysis Clarifies Pathological Heterogeneity in Tenosynovial Giant Cell Tumor and Identifies Biomarkers for Predicting Disease Recurrence
title_full_unstemmed Single‐Cell Analysis Clarifies Pathological Heterogeneity in Tenosynovial Giant Cell Tumor and Identifies Biomarkers for Predicting Disease Recurrence
title_short Single‐Cell Analysis Clarifies Pathological Heterogeneity in Tenosynovial Giant Cell Tumor and Identifies Biomarkers for Predicting Disease Recurrence
title_sort single cell analysis clarifies pathological heterogeneity in tenosynovial giant cell tumor and identifies biomarkers for predicting disease recurrence
topic local aggression
recurrence
single‐cell RNA sequencing
tenosynovial giant cell tumors
url https://doi.org/10.1002/advs.202415835
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