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FOXM1 promotes neurofibromatosis type 1-associated malignant peripheral nerve sheath tumor progression in a NUF2-dependent manner

Cancer Gene Therapy volume 30, pages 1390–1402 (2023)Cite this article

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Abstract

Malignant peripheral nerve sheath tumors (MPNSTs) are aggressive soft-tissue sarcomas characterized by poor prognosis and low drug response rates. Traditional chemo/radiotherapies show only mild benefits for patients with MPNSTs, and no targeted therapy is available in the clinic. A better understanding of the molecular background of MPNSTs is critical for the development of effective targeted therapies. Forkhead box M1 (FOXM1) has been implicated in the progression of many human malignancies, though its role in MPNSTs is unclear. In this study, using four Gene Expression Omnibus (GEO) datasets and a tissue microarray, we demonstrated that FOXM1 upregulation was associated with poor prognosis in patients with MPNSTs. FOXM1 overexpression and knockdown regulated the proliferation and colony formation of MPNST cells. Using bioinformatics analysis and luciferase reporter assays, we identified NUF2 as a direct downstream target of FOXM1. Both in vitro and in vivo experiments demonstrated that the induction of MPNST cell proliferation by FOXM1 was dependent on elevated NUF2 expression, as NUF2 knockdown abolished the FOXM1-induced proliferation of MPNST cells. Our study showed that the FOXM1–NUF2 axis mediates human MPNST progression and could be a potential therapeutic target.

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Fig. 1: Upregulation of FOXM1 is correlated with poor prognosis in MPNST patients.
Fig. 2: FOXM1 promotes NF1-associated MPNST cell proliferation in vitro.
Fig. 3: FOXM1 upregulates the expression of NUF2 by binding to its promotor site.
Fig. 4: NUF2 promotes NF1 - associated MPNST cell proliferation in vitro.
Fig. 5: NUF2 is required for FOXM1-induced proliferation of NF1- associated MPNST cells in vitro.
Fig. 6: FOXM1–NUF2 axis promotes NF1-associated MPNST progression in vivo.
Fig. 7: Upregulation of NUF2 is correlated with poor prognosis in MPNST patients.

Data availability

The datasets analyzed during the current study are available from the corresponding author upon reasonable request.

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Acknowledgements

The authors would like to thank Prof. Vincent Keng and Prof. Jilong Yang for providing cell lines.

Funding

This work was supported by grants from the National Natural Science Foundation of China (82102344; 82172228), the Shanghai Rising Star Program supported by the Science and Technology Commission of Shanghai Municipality (20QA1405600); Science and Technology Commission of Shanghai Municipality (19JC1413); Natural Science Foundation of Shanghai (22ZR1422300); “Chenguang Program” supported by Shanghai Education Development Foundation (SHEDF) (19CG18); Shanghai Municipal Key Clinical Specialty (shslczdzk00901); Innovative research team of high-level local universities in Shanghai (SSMU-ZDCX20180700); the Project of Biobank (YBKA201901) from Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine.

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  1. These authors contributed equally: Rehanguli Aimaier, Man-Hon Chung, Yihui Gu, Qingxiong Yu.

Authors and Affiliations

  1. Department of Plastic and Reconstructive Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

    Rehanguli Aimaier, Man-Hon Chung, Yihui Gu, Chengjiang Wei, Zizhen Guo, Yuehua Li, Wei Wang, Qingfeng Li & Zhichao Wang

  2. Department of Facial Plastic and Reconstructive Surgery, Eye & ENT Hospital, Fudan University, Shanghai, China

    Qingxiong Yu

  3. Department of Plastic Surgery, The Third Xiangya Hospital, Central South University, Changsha, Hunan, China

    Haibo Li

  4. Department of Pathology, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

    Manmei Long

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Contributions

QL, ZW, and RH contributed to the conceptualization and design of the experiment. RH, MC, YG, QY, YL, HL, and ZG contributed to the methodology, investigation, and data curation. YG, QY, CW, ML, and WW contributed to the software, validation, and visualization. QL and ZW contributed to the supervision and funding acquisition. All authors participated in data analysis and wrote and approved the final version of the paper.

Corresponding authors

Correspondence to Qingfeng Li or Zhichao Wang.

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The study was approved by the Ethics Committee of Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine. Informed consent was obtained from all subjects involved in the study. The animal study protocol was approved by the Shanghai Medical Experimental Animal Care Commission (IACUC: 2019-0008).

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Aimaier, R., Chung, MH., Gu, Y. et al. FOXM1 promotes neurofibromatosis type 1-associated malignant peripheral nerve sheath tumor progression in a NUF2-dependent manner. Cancer Gene Ther 30, 1390–1402 (2023). https://doi.org/10.1038/s41417-023-00645-8

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