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Single-cell landscape of undifferentiated pleomorphic sarcoma

Oncogene (2024)Cite this article

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Abstract

Undifferentiated pleomorphic sarcoma (UPS) is a highly aggressive malignant soft tissue tumor with a poor prognosis; however, the identity and heterogeneity of tumor populations remain elusive. Here, eight major cell clusters were identified through the RNA sequencing of 79,569 individual cells of UPS. UPS originates from mesenchymal stem cells (MSCs) and features undifferentiated subclusters. UPS subclusters were predicted to exist in two bulk RNA datasets, and had a prognostic value in The Cancer Genome Atlas (TCGA) dataset. The functional heterogeneity of malignant UPS cells and the immune microenvironment were characterized. Additionally, the fused cells were innovatively detected by expressing both monocyte/macrophage markers and other subcluster-associated genes. Based on the ligand–receptor interaction analysis, cellular interactions with epidermal growth factor receptor (EGFR) and vascular endothelial growth factor receptor (VEGFR) were abundant. Furthermore, 73% of patients with UPS (48/66) showed positive EGFR expression, which was associated with a poor prognosis. EGFR blockade with cetuximab inhibited tumor growth in a patient-derived xenograft model. Our transcriptomic studies delineate the landscape of UPS intratumor heterogeneity and serve as a foundational resource for further discovery and therapeutic exploration.

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Fig. 1: Single-cell transcriptomic profiling of undifferentiated pleomorphic sarcoma (UPS).
Fig. 2: Single-cell transcriptomic profiling of tumor cells, fibroblasts, and mesenchymal stem cells (MSCs).
Fig. 3: Developmental trajectories of UPS.
Fig. 4: UPS is characterized by undifferentiated subclusters with different prognoses.
Fig. 5: Non-negative matrix factorization (NMF) programs reveal functional heterogeneity of UPS malignant cells.
Fig. 6: Single-cell transcriptomic profiling of T cells in UPS.
Fig. 7: Cell fusion is a new pathological feature of UPS.
Fig. 8: Anti-epidermal growth factor receptor (EGFR) treatment in UPS.

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Data availability

Single-cell sequencing data of human UPS specimens has been deposited at Genome Sequence Archive (GSA) with the identifier: HRA004389. Bulk expression data from complex genetics sarcomas including UPS was downloaded from GSE:21050. TCGA-SARC RNA-seq and survival data were downloaded from the Genomic Data Commons (GDC) (https://portal.gdc.cancer.gov/).

Code availability

Codes used to conduct analyses and generate results of this article is deposited at https://github.com/luyifei111/scUPS.

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Acknowledgements

We would like to appreciate BioRender.com, with which some of the icons and elements of diagrams were created. This study was supported by grants from the Genertec Guozhong Healthcare (Grant No. GZKJ-KJXX-QTHT-20220016) (Y.C.), Industry-University Research Innovation Foundation of Science and Technology Development Center of the Ministry of Education (Grant No. 2021JH013) (Y.C.), National Natural Science Foundation of China (Grant No.82373385) (Y.C.).

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Authors and Affiliations

  1. Department of Pediatric Surgery, Children’s Hospital of Fudan University, and Shanghai Key Laboratory of Birth Defects, Shanghai, 201102, China

    Yifei Lu, Deqian Chen, Yong Zhan, Ran Yang, Enqing Zhou, Shuyang Dai, Yi Li & Rui Dong

  2. Department of Musculoskeletal Oncology, Shanghai Cancer Center, and Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, 200032, China

    Bingnan Wang, Yong Chen & Biqiang Zheng

  3. Department of Animal Experimental Center, Fudan University Shanghai Cancer Center, Shanghai, 201102, China

    Wenjun Chai & Mingxia Yan

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Contributions

Yifei Lu: Methodology, Software, Validation, Formal analysis, Investigation, Data Curation, Writing - Original Draft, Visualization. Deqian Chen: Methodology, Software, Data Curation, Visualization. Bingnan Wang: Validation, Investigation. Wenjun Chai: Methodology, Visualization. Mingxia Yan: Validation, Visualization. Yong Chen: Conceptualization, Funding acquisition. Yong Zhan: Validation, Data Curation. Ran Yang: Data Curation. Enqing Zhou: Data Curation. Shuyang Dai: Data Curation. Yi Li: Data Curation. Rui Dong: Conceptualization, Methodology, Investigation, Resources, Writing - Review & Editing, Supervision, Project administration Biqiang Zheng: Conceptualization, Methodology, Investigation, Resources, Writing - Review & Editing, Supervision, Project administration, Funding acquisition.

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Correspondence to Rui Dong or Biqiang Zheng.

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Lu, Y., Chen, D., Wang, B. et al. Single-cell landscape of undifferentiated pleomorphic sarcoma. Oncogene (2024). https://doi.org/10.1038/s41388-024-03001-8

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