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LncRNA PRBC induces autophagy to promote breast cancer progression through modulating PABPC1-mediated mRNA stabilization

Oncogene volume 43, pages 1019–1032 (2024)Cite this article

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Abstract

Breast cancer is one of the major malignant tumors among women worldwide. Long noncoding RNAs (lncRNAs) have been documented as significant modulators in the development and progression of various cancers; however, the contribution of lncRNAs to breast cancer remains largely unknown. In this study, we found a novel lncRNA (NONHSAT137675) whose expression was significantly increased in the breast cancer tissues. We named the novel lncRNA as lncRNA PRBC (PABPC1-related lncRNA in breast cancer) and identified it as a key lncRNA associated with breast cancer progression and prognosis. Functional analysis displayed that lncRNA PRBC could promote autophagy and progression of breast cancer. Mechanistically, we verified that lncRNA PRBC physically interacted with PABPC1 through RIP assay, and PABPC1 overexpression could reverse the inhibiting effect of lncRNA PRBC knockdown on the malignant behaviors in breast cancer cells. Knockdown of lncRNA PRBC interfered the translocation of PABPC1 from nucleus to cytoplasm as indicated by western blot and IF assays. Significantly, the cytoplasmic location of PABPC1 was required for the interaction between PABPC1 and AGO2, which could be enhanced by lncRNA PRBC overexpression, leading to strengthened recruitment of mRNA to RNA-induced silencing complex (RISC) and thus reinforcing the inhibition efficiency of miRNAs. In general, lncRNA PRBC played a critical role in malignant progression of breast cancer by inducing the cytoplasmic translocation of PABPC1 to further regulate the function of downstream miRNAs. This study provides novel insight on the molecular mechanism of breast cancer progression, and lncRNA PRBC might be a promising therapeutic target and prognostic predictor for breast cancer.

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Fig. 1: LncRNA PRBC is upregulated in breast cancer, and associated with poor prognosis of breast cancer patients.
Fig. 2: LncRNA PRBC knockdown attenuates malignant phenotypes of breast cancer cells.
Fig. 3: LncRNA PRBC promotes breast cancer progression through inducing autophagy.
Fig. 4: LncRNA PRBC physically interacts with PABPC1 protein and regulates its subcellular location.
Fig. 5: PABPC1 knockdown inhibits breast cancer progression and autophagy.
Fig. 6: PABPC1 regulates the biological function of lncRNA PRBC in breast cancer.
Fig. 7: LncRNA PRBC overexpression promotes breast cancer progression in vivo.

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Data availability

The data in this study are available from the corresponding author upon reasonable request.

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Acknowledgements

This work was supported by Special Foundation for Taishan Scholars (No. ts20190971), Special Support Plan for National High Level Talents (Ten Thousand Talents Program W01020103), Foundation from Clinical Research Center of Shandong University (No.2020SDUCRCA015), Qilu Hospital Clinical New Technology Developing Foundation (No. 2019-3).

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  1. These authors contributed equally: Yiran Liang, Bing Chen.

Authors and Affiliations

  1. Department of Breast Surgery, General Surgery, Qilu Hospital of Shandong University, Jinan, Shandong, 250012, P.R. China

    Yiran Liang, Fanchao Xu, Li Long, Fangzhou Ye, Yajie Wang, Dan Luo, Yaming Li, Yuhan Jin, Lei Wang, Xiaoli Kong & Qifeng Yang

  2. Biological Resource Center, Qilu Hospital of Shandong University, Jinan, Shandong, 250012, P.R. China

    Bing Chen, Wenjing Zhao, Lijuan Wang & Qifeng Yang

  3. Department of Breast Surgery, Mianyang Central Hospital, Mianyang, Sichuan, 621000, P.R. China

    Li Long

  4. Department of Pathology, Qilu Hospital of Shandong University, Jinan, Shandong, 250012, P.R. China

    Peng Su

  5. Research Institute of Breast Cancer, Shandong University, Jinan, Shandong, 250012, P.R. China

    Qifeng Yang

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Contributions

YL, BC, PS and QY conceived the study. FX, LL, YW, DL, FY, YL, YJ and LW helped to perform the experiments. YL, BC, WZ and LW analyzed the data. XK and PS collected clinical samples. YL, BC, PS and QY wrote and revised the paper. All authors have read and approved the final manuscript.

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Correspondence to Peng Su or Qifeng Yang.

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Liang, Y., Chen, B., Xu, F. et al. LncRNA PRBC induces autophagy to promote breast cancer progression through modulating PABPC1-mediated mRNA stabilization. Oncogene 43, 1019–1032 (2024). https://doi.org/10.1038/s41388-024-02971-z

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