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PARP1-stabilised FOXQ1 promotes ovarian cancer progression by activating the LAMB3/WNT/β-catenin signalling pathway

Oncogene volume 43, pages 866–883 (2024)Cite this article

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Abstract

Metastasis is an important factor that causes ovarian cancer (OC) to become the most lethal malignancy of the female reproductive system, but its molecular mechanism is not fully understood. In this study, through bioinformatics analysis, as well as analysis of tissue samples and clinicopathological characteristics and prognosis of patients in our centre, it was found that Forkhead box Q1 (FOXQ1) was correlated with metastasis and prognosis of OC. Through cell function experiments and animal experiments, the results show that FOXQ1 can promote the progression of ovarian cancer in vivo and in vitro. Through RNA-seq, chromatin immunoprecipitation sequencing (ChIP-seq), Kyoto Encyclopedia of Genes and Genomes (KEGG), gene set enrichment analysis (GSEA), Western blotting (WB), quantitative real-time polymerase chain reaction (qRT‒PCR), immunohistochemistry (IHC), luciferase assay, and ChIP-PCR, it was demonstrated that FOXQ1 can mediate the WNT/β-catenin pathway by targeting the LAMB promoter region. Through coimmunoprecipitation (Co-IP), mass spectrometry (MS), ubiquitination experiments, and immunofluorescence (IF), the results showed that PARP1 could stabilise FOXQ1 expression via the E3 ubiquitin ligase Hsc70-interacting protein (CHIP). Finally, the whole mechanism pathway was verified by animal drug combination experiments and clinical specimen prognosis analysis. In summary, our results suggest that PARP1 can promote ovarian cancer progression through the LAMB3/WNT/β-catenin pathway by stabilising FOXQ1 expression.

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Fig. 1: FOXQ1 is overexpressed in OC and clinically associated with patient prognosis.
Fig. 2: FOXQ1 promotes OC cell proliferation in vitro and in vivo.
Fig. 3: FOXQ1 promotes OC migration, invasion and metastasis in vitro and in vivo.
Fig. 4: FOXQ1 promotes LAMB3 transcription by binding to its promoter region.
Fig. 5: LAMB3 is overexpressed in OC and clinically associated with patient prognosis.
Fig. 6: The oncogenic effects of FOXQ1 are mediated via the LAMB3/WNT//β-catenin pathway.
Fig. 7: PARP1 can inhibit the ubiquitination-mediated degradation of FOXQ1 by targeting the E3 ubiquitin ligase CHIP.
Fig. 8: PARP1 is overexpressed in OC and clinically associated with patient prognosis.
Fig. 9: The PARP1/FOXQ1/LAMB3/WNT/β-catenin signalling pathway was supported by animal models and clinical samples.

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Data availability

The data that support the results of this study are available from the corresponding author upon reasonable request.

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Funding

This work was supported, in part, by grants from the National Natural Science Foundation of China (No. 81972431, 82272898, 82203723, 82203723); Shanghai Sailing Program (No. 20YF1408000); Shanghai Anticancer Association EYAS PROJECT (No. SACA-CY19A07); The Foundation of Shanghai Municipal Health Bureau (No. 20204Y0268; No. 20224Y0233); Shanghai Anti-Cancer Association “Young eagle” program (No. SACA-CY23C06); and the Female Tumour Project of Shanghai Key Clinical Specialty (No. SHSLCZDZK06301).

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  1. These authors contributed equally: Jiangchun Wu, Yong Wu, Siyu Chen.

  2. These authors jointly supervised this work: Lingfang Xia, Xiaohua Wu.

Authors and Affiliations

  1. Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, 200032, China

    Jiangchun Wu, Yong Wu, Siyu Chen, Qinhao Guo, Yang Shao, Chaohua Liu, Kailin Lin, Simin Wang, Jun Zhu, Xiaojun Chen, Xingzhu Ju, Lingfang Xia & Xiaohua Wu

  2. Department of Gynecologic Oncology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai, 200032, China

    Jiangchun Wu, Yong Wu, Siyu Chen, Qinhao Guo, Chaohua Liu, Simin Wang, Jun Zhu, Xiaojun Chen, Xingzhu Ju, Lingfang Xia & Xiaohua Wu

  3. Cancer Institute, Fudan University Shanghai Cancer Center, Shanghai, 200032, China

    Yang Shao & Chaohua Liu

  4. Department of Thoracic Surgery, Fudan University Shanghai Cancer Center, Shanghai, China; State Key Laboratory of Genetic Engineering, Fudan University Shanghai Cancer Center, Shanghai, 200032, China

    Kailin Lin

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Contributions

JW, YW: Conceptualisation, Data curation, Investigation, Writing - original draft. YS, CL: Conceptualisation, Data curation, Investigation, Writing - original draft, Formal analysis, Methodology, Resources, Software, Validation, Visualisation. QG, SC, SW, XJ, JZ: Conceptualisation, funding acquisition, project administration, supervision, writing - original draft, writing - review & editing. XW: Conceptualisation, funding acquisition, project administration, supervision, writing - original draft, writing - review & editing.

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Correspondence to Xiaohua Wu.

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Wu, J., Wu, Y., Chen, S. et al. PARP1-stabilised FOXQ1 promotes ovarian cancer progression by activating the LAMB3/WNT/β-catenin signalling pathway. Oncogene 43, 866–883 (2024). https://doi.org/10.1038/s41388-024-02943-3

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