Integrating spatial and single-cell transcriptomes reveals the role of COL1A2(+) MMP1(+/-) cancer-associated fibroblasts in ER-positive breast cancer

Abstract Cancer-associated fibroblasts (CAFs) are highly heterogeneous cells and important components of the breast tumor microenvironment (TME). However, their role and clinical value in ER-positive breast cancer have not been fully clarified. Our study aims to comprehensively characterize the hete...

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Main Authors: Zhi-Hao Yu, Huan-Ling Xu, Shuo Wang, Ying-Xi Li, Gui-Xin Wang, Yao Tian, Zhao-Hui Chen, Wen-Bin Song, Long He, Xin Wang, Xu-Chen Cao, Yue Yu
Format: Article
Language:English
Published: BMC 2025-03-01
Series:Cancer Cell International
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Online Access:https://doi.org/10.1186/s12935-025-03705-1
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author Zhi-Hao Yu
Huan-Ling Xu
Shuo Wang
Ying-Xi Li
Gui-Xin Wang
Yao Tian
Zhao-Hui Chen
Wen-Bin Song
Long He
Xin Wang
Xu-Chen Cao
Yue Yu
author_facet Zhi-Hao Yu
Huan-Ling Xu
Shuo Wang
Ying-Xi Li
Gui-Xin Wang
Yao Tian
Zhao-Hui Chen
Wen-Bin Song
Long He
Xin Wang
Xu-Chen Cao
Yue Yu
author_sort Zhi-Hao Yu
collection DOAJ
description Abstract Cancer-associated fibroblasts (CAFs) are highly heterogeneous cells and important components of the breast tumor microenvironment (TME). However, their role and clinical value in ER-positive breast cancer have not been fully clarified. Our study aims to comprehensively characterize the heterogeneity, potential biological functions, and molecular mechanisms of CAFs in ER-positive breast cancer within the tumor microenvironment using multi-omics data, to provide new strategies for the diagnosis and treatment of ER-positive breast cancer patients. In this study, we found that COL1A2(+) MMP1(+) and COL1A2(+) MMP1(-) CAFs were associated with unfavorable prognosis. The dynamic evolution and cell-cell communications of CAFs were analyzed, revealing that COL1A2(+) MMP1(+/-) CAFs show extensive crosstalk with tumor-associated macrophages (TAMs), contributing to an immunosuppressive TME. Moreover, the somatic mutation of TP53 may be a potential indicator for evaluating the infiltration of COL1A2(+) MMP1(+/-) CAFs. Finally, an MRI-based radiomic model was constructed to estimate the abundance of these CAFs. In conclusion, our findings provide a theoretical basis for targeting CAFs and offer a noninvasive approach to evaluate the infiltration level of COL1A2(+) MMP1(+/-) CAFs.
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spelling doaj-art-a9d8da3239574985b5112053cbf8c5f32025-08-20T03:05:49ZengBMCCancer Cell International1475-28672025-03-0125111610.1186/s12935-025-03705-1Integrating spatial and single-cell transcriptomes reveals the role of COL1A2(+) MMP1(+/-) cancer-associated fibroblasts in ER-positive breast cancerZhi-Hao Yu0Huan-Ling Xu1Shuo Wang2Ying-Xi Li3Gui-Xin Wang4Yao Tian5Zhao-Hui Chen6Wen-Bin Song7Long He8Xin Wang9Xu-Chen Cao10Yue Yu11The First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for CancerThe First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for CancerThe First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for CancerImmunology Department, Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), Tianjin Medical UniversityThe First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for CancerThe First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for CancerThe First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for CancerDepartment of General Surgery, Tianjin Key Laboratory of Precise Vascular Reconstruction and Organ Function Repair, Tianjin Medical University General Hospital, Tianjin General Surgery InstituteDepartment of General Surgery, Tianjin Key Laboratory of Precise Vascular Reconstruction and Organ Function Repair, Tianjin Medical University General Hospital, Tianjin General Surgery InstituteThe First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for CancerThe First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for CancerThe First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for CancerAbstract Cancer-associated fibroblasts (CAFs) are highly heterogeneous cells and important components of the breast tumor microenvironment (TME). However, their role and clinical value in ER-positive breast cancer have not been fully clarified. Our study aims to comprehensively characterize the heterogeneity, potential biological functions, and molecular mechanisms of CAFs in ER-positive breast cancer within the tumor microenvironment using multi-omics data, to provide new strategies for the diagnosis and treatment of ER-positive breast cancer patients. In this study, we found that COL1A2(+) MMP1(+) and COL1A2(+) MMP1(-) CAFs were associated with unfavorable prognosis. The dynamic evolution and cell-cell communications of CAFs were analyzed, revealing that COL1A2(+) MMP1(+/-) CAFs show extensive crosstalk with tumor-associated macrophages (TAMs), contributing to an immunosuppressive TME. Moreover, the somatic mutation of TP53 may be a potential indicator for evaluating the infiltration of COL1A2(+) MMP1(+/-) CAFs. Finally, an MRI-based radiomic model was constructed to estimate the abundance of these CAFs. In conclusion, our findings provide a theoretical basis for targeting CAFs and offer a noninvasive approach to evaluate the infiltration level of COL1A2(+) MMP1(+/-) CAFs.https://doi.org/10.1186/s12935-025-03705-1Cancer-associated fibroblastsRadiomicsER-positive breast cancerTumor microenvironmentSingle-cell RNA sequencing
spellingShingle Zhi-Hao Yu
Huan-Ling Xu
Shuo Wang
Ying-Xi Li
Gui-Xin Wang
Yao Tian
Zhao-Hui Chen
Wen-Bin Song
Long He
Xin Wang
Xu-Chen Cao
Yue Yu
Integrating spatial and single-cell transcriptomes reveals the role of COL1A2(+) MMP1(+/-) cancer-associated fibroblasts in ER-positive breast cancer
Cancer Cell International
Cancer-associated fibroblasts
Radiomics
ER-positive breast cancer
Tumor microenvironment
Single-cell RNA sequencing
title Integrating spatial and single-cell transcriptomes reveals the role of COL1A2(+) MMP1(+/-) cancer-associated fibroblasts in ER-positive breast cancer
title_full Integrating spatial and single-cell transcriptomes reveals the role of COL1A2(+) MMP1(+/-) cancer-associated fibroblasts in ER-positive breast cancer
title_fullStr Integrating spatial and single-cell transcriptomes reveals the role of COL1A2(+) MMP1(+/-) cancer-associated fibroblasts in ER-positive breast cancer
title_full_unstemmed Integrating spatial and single-cell transcriptomes reveals the role of COL1A2(+) MMP1(+/-) cancer-associated fibroblasts in ER-positive breast cancer
title_short Integrating spatial and single-cell transcriptomes reveals the role of COL1A2(+) MMP1(+/-) cancer-associated fibroblasts in ER-positive breast cancer
title_sort integrating spatial and single cell transcriptomes reveals the role of col1a2 mmp1 cancer associated fibroblasts in er positive breast cancer
topic Cancer-associated fibroblasts
Radiomics
ER-positive breast cancer
Tumor microenvironment
Single-cell RNA sequencing
url https://doi.org/10.1186/s12935-025-03705-1
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