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Cancer-associated fibroblasts drive lung adenocarcinoma progression via THBS2-mediated epithelial-mesenchymal transition

Oncogene (2025)Cite this article

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Abstract

The role of cancer-associated fibroblasts (CAFs) in the initiation and invasion phases of human lung adenocarcinoma (LUAD) development is not fully understood. In this study, we utilized single-cell RNA sequencing, spatial transcriptomics, and a combination of in vivo and in vitro models to decode the dynamics of tumor-stroma interactions during human LUAD progression, focusing primarily on adenocarcinoma in situ (AIS), minimally invasive adenocarcinoma (MIA), and invasive adenocarcinoma (IAC). We identified a matrix CAF (mCAF) subtype characterized by high THBS2 expression, which was closely associated with poor clinical outcomes, tumor recurrence, and the invasive dynamics of LUAD. Spatial transcriptomics and multiplex immunohistochemistry analysis revealed that this CAF subpopulation was closely associated with tumor cells, with clear spatial colocalization. In vivo and in vitro experiments demonstrated that THBS2 secreted by these mCAFs directly binds to SDC4 on tumor cells, enhancing tumor epithelial-mesenchymal transition (EMT) programs. This study highlights THBS2+ mCAFs as key regulators of tumor-stroma interactions and identifies the THBS2-SDC4-EMT axis as a potential therapeutic target in LUAD.

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Fig. 1: Fibroblasts exhibit stronger interactions and associations with LUAD cells in multimodal data.
Fig. 2: CAF dynamics and functional heterogeneity in LUAD progression.
Fig. 3: Identification of critical genes linking CAFs to LUAD progression.
Fig. 4: THBS2 enhances oncogenic phenotypes and induces EMT in LUAD cells.
Fig. 5: THBS2 promotes tumor growth in vivo.
Fig. 6: THBS2 promotes malignant phenotype of LUAD through Binding to SDC4.
Fig. 7: THBS2-SDC4 axis promotes tumor progression through the activation of EMT signaling.

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Data availability

All scRNA-seq datasets used in this study are publicly available. The datasets can be accessed via the following links: GSE189357 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE189357) and GSE164789 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE164789). The bulk transcriptome data was download from the TCGA (https://portal.gdc.cancer.gov/) and Gene Expression Omnibus database, including GSE14814 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE14814), GSE50081 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE50081), GSE72094 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE72094), GSE31210 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE31210), GSE3141 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE3141, GSE26939 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE26939), GSE30219 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE30219), and GSE20913 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE20913). Additionally, the 10X Visium Spatial transcriptome data were collected from GSE189487 dataset (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc= GSE189487).

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Acknowledgements

This study was supported by the Henan Provincial Science and Technology Research Project (221100310100).

Author information

Author notes

  1. These authors contributed equally: Yuqing Ren, Ruijie Ming, Anning Zuo.

Authors and Affiliations

  1. Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, China

    Yuqing Ren, Anning Zuo, Shutong Liu, Yuhao Ba, Yuyuan Zhang, Yukang Chen, Hui Xu, Xinwei Han & Zaoqu Liu

  2. Department of Respiratory and Critical Care Medicine, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, China

    Yuqing Ren & Yi Yue

  3. Interventional Institute of Zhengzhou University, Zhengzhou, Henan, China

    Yuqing Ren, Yuyuan Zhang, Xinwei Han & Zaoqu Liu

  4. Interventional Treatment and Clinical Research Center of Henan Province, Zhengzhou, Henan, China

    Yuqing Ren, Yuyuan Zhang, Xinwei Han & Zaoqu Liu

  5. Department of Pulmonary and Critical Care Medicine, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China

    Yuqing Ren

  6. Department of Oncology, Chongqing University Three Gorges Hospital, Chongqing, China

    Ruijie Ming

  7. School of Medicine, Chongqing University, Chongqing, China

    Ruijie Ming

  8. Longgang District Maternity & Child Healthcare Hospital of Shenzhen City (Longgang Maternity and Child Institute of Shantou University Medical College), Shantou, China

    Teng Pan

  9. The Department of Oncology, Zhujiang Hospital, Southern Medical University, Guangzhou, China

    Peng Luo

  10. Department of Neurosurgery, Xiangya Hospital, Central South University, Changsha, Hunan, China

    Quan Cheng

  11. Richard Dimbleby Department of Cancer Research, Comprehensive Cancer Centre, Kings College London, London, United Kingdom

    Jinhai Deng

  12. National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China

    Siyuan Weng

  13. Department of Breast Medical Oncology, Cancer Research Center, Shandong Cancer Hospital and Institute, Shandong First Medical University and Shandong Academy of Medical Sciences, Jinan, Shandong Province, China

    Dongdong Zhou

  14. Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China

    Zaoqu Liu

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Contributions

ZQL conceived, designed, and supervised the research. XWH and DDZ provided project guidance and funding support. YQR and RJM conducted the bioinformatics analysis. ANZ, YHB, STL and HX performed the experiments, with ANZ conducting the statistical analysis of experimental trials. YQR, RJM, and DDZ wrote the manuscript. RJM, PL and QC offered research guidance. YYZ, YY, SYW, JHD, TP, and YKC collected the data. ZQL, RJM and DDZ revised the manuscript.

Corresponding authors

Correspondence to Xinwei Han, Dongdong Zhou or Zaoqu Liu.

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The authors declare no competing interests.

Ethics approval and consent to participate

All human tissue samples were obtained with written informed consent from each patient and approved by the Ethics Committee (Approval Nos. HLugA120PG01: 2020-0930; HLugA030PG04-2: 2021-0215; HLugA180Su07: 2022-0401). All animal experiments were approved by the Institutional Animal Care and Use Committee of Zhengzhou University (Ethical Approval No. 2019-KY-383) and conducted in strict accordance with the National Institutes of Health (NIH) guidelines for animal care and use.

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Ren, Y., Ming, R., Zuo, A. et al. Cancer-associated fibroblasts drive lung adenocarcinoma progression via THBS2-mediated epithelial-mesenchymal transition. Oncogene (2025). https://doi.org/10.1038/s41388-025-03569-9

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