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Cellular and Molecular Biology

Identification of increased dedifferentiation along the Prom1+ cancer cells in Müllerian adenosarcoma with sarcomatous overgrowth

British Journal of Cancer volume 132, pages 438–449 (2025)Cite this article

Subjects

Abstract

Background

Müllerian adenosarcoma (MA) is a rare tumour accounts for 5–7% of uterine sarcomas. Tumours with sarcomatous overgrowth (MASO) or high-grade tend to be aggressive. However, the tumour aetiology is elusive.

Methods

Single-cell RNA sequencing and bioinformatics were used to analyse the MASO and paired normal tissues. Expression and clinical significance of key genes were analysed by TCGA data and immunohistochemistry. In vitro experiment was used to verify the effect of E2F1 in cell dedifferentiation.

Results

We prove malignant stromal cells originate from fibrous tissue, Prom1-derived with complex intra-tumoral heterogeneity. Along the developmental trajectory, we discover three phenotypes of Prom1+ cancer cells (differentiation-like, intermediate-like, dedifferentiation-like). A distinct HMGB2/3+ subtype of Prom1+ cluster is predominant dedifferentiation-like cancer cells, with high proliferation and stemness traits at the tail of trajectory. E2F1 is a master transcription factor for Prom1 lineage dedifferentiation, which could occupy the HMGB2/3 promoter to enhance their transcription, facilitating the stemness and self-renewal of cancer cells. Gene signature of Prom1 lineage is associated with poorer prognosis in uterine malignancies. The expression of Prom1 and HMGB3 was verified by immunohistochemistry.

Conclusions

Our study reveal the heterogeneity and dynamics of Prom1 lineage cells, which are key to tailor efficient therapies for MASO.

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Fig. 1: Clinicopathological manifestations of the MASO samples.
Fig. 2: The cellular composition from a recurrent MASO patient.
Fig. 3: Identification of Prom1+ cancer cells in MASO.
Fig. 4: Pseudotime analysis of Prom1+ cancer cells in MASO.
Fig. 5: E2F1 cooperate with HMGB2/3 to promote cell stemness.
Fig. 6: Prognosis analysis of Prom1+ cancer cell in uterine malignancies.
Fig. 7: Cell communications in MASO.
Fig. 8: Schematic summary of the evolutionary process of Prom1 lineage in MASO.

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Data availability

The raw scRNA-seq data generated in this study have been deposited in the Genome Sequence Archive (GSA, https://ngdc.cncb.ac.cn/gsa/). The accession number is HRA008869. All other data supporting the findings of this study are available from the corresponding author upon reasonable request.

Code availability

The codes used in this study have been reported previously and are available as described in the corresponding “Methods” section.

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Funding

This work was supported by Major Scientific Research Program for Young and Middle-aged Health Professionals of Fujian Province, China (2022ZQNZD008); Joint Funds for the Innovation of Science and Technology, Fujian Province, China (2021Y9209); Funds for Advanced Cancer Center, Fujian Province, China (F2125Y-GSP02-01); National Natural Science Foundation of China (82374081); High-level Talents Training Project of Fujian Cancer Hospital (2022YNG04); the Natural Science Foundation of Fujian Province (2024J011096, 2024J011098); Innovative Medicine Subject of Fujian Provincial Health Commission (2024CXA034).

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Author notes

  1. These authors contributed equally: Xingming Ye, Jianfeng Zheng, Dan Hu, Li Liu.

Authors and Affiliations

  1. Department of Gynecology, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, China

    Xingming Ye, Jianfeng Zheng, Li Liu, Xintong Cai, Jie Lin & Yang Sun

  2. Fujian Provincial Key Laboratory of Tumor Biotherapy, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, China

    Xingming Ye, Jianfeng Zheng, Yangmei Xu, Qinying Liu & Yang Sun

  3. Department of Pathology, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, China

    Dan Hu

  4. Geneplus-Beijing Institute, Beijing, China

    Fukun Chen & Lifeng Li

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  1. Xingming Ye
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  2. Jianfeng Zheng
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Contributions

Xingming Ye, Jianfeng Zheng and Li Liu conceived and designed this study; Dan Hu and Jie Lin performed pathological examinations; Xingming Ye, Jianfeng Zheng, Fukun Chen and Lifeng Li analysed the data; Qinying Liu and Yangmei Xu wrote the manuscript; Dan Hu, Xintong Cai and Jianfeng Zheng collected the samples and conducted the experiments; Yang Sun provided funding and offered administrative support. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yang Sun.

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This study was conducted in compliance with institutional policy to protect patients’ private information and was approved by the Institutional Review Board of Fujian Cancer Hospital (K2022-052-01), informed consent was also obtained from each patient.

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Ye, X., Zheng, J., Hu, D. et al. Identification of increased dedifferentiation along the Prom1+ cancer cells in Müllerian adenosarcoma with sarcomatous overgrowth. Br J Cancer 132, 438–449 (2025). https://doi.org/10.1038/s41416-025-02943-4

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