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Survivin degradation by bergenin overcomes pemetrexed resistance

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Abstract

Purpose

Chemoresistance is a primary factor for treatment failure and tumor recurrence in non-small cell lung cancer (NSCLC) patients. The oncoprotein survivin is commonly upregulated in human malignancies and is associated with poor prognosis, but its effect on carcinogenesis and chemoresistance in NSCLC is not yet evident, and to explore an effective inhibitor targeting survivin expression is urgently needed.

Methods

The protumor characteristics of survivin and antitumor activities of bergenin in NSCLC cells were examined by MTS, colony formation assays, immunoblot, immunohistochemistry, and in vivo xenograft development.

Results

Survivin was upregulated in non-small cell lung cancer (NSCLC) tissues, while its depletion inhibited NSCLC tumorigenesis. The current study focused on bergenin, identifying its effective antitumor effect on NSCLC cells both in vivo and in vitro. The results showed that bergenin could inhibit cell proliferation and induce the intrinsic pathway of apoptosis via downregulating survivin. Mechanistically, bergenin reduced the phosphorylation of survivin via inhibiting the Akt/Wee1/CDK1 signaling pathway, thus resulting in enhanced interaction between survivin and E3 ligase Fbxl7 to promote survivin ubiquitination and degradation. Furthermore, bergenin promoted chemoresistance in NSCLC cells re-sensitized to pemetrexed treatment.

Conclusions

Survivin overexpression is required for maintaining multiple malignant phenotypes of NSCLC cells. Bergenin exerts a potent antitumor effect on NSCLC via targeting survivin, rendering it a promising agent for the treatment of NSCLC.

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Data availability

The datasets used and analyzed in this study are available from the corresponding authors on request.

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Funding

This work was supported by the National Natural Science Foundation of China (No. 81972837 and 82003203), the Natural Science Foundation of Hunan Province (Nos. 2021JJ31011 and 2021JJ41058) and the Hunan Province Natural Science Foundation Youth Fund Project, China (No. 2021JJ40943).

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  1. Xiaoying Li, Qi Liang and Li Zhou contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, The Third Xiangya Hospital of Central South University, Changsha, Hunan, 410013, People’s Republic of China

    Xiaoying Li, Qi Liang, Yu Gan, Shuangze Han, Jinzhuang Liao, Ruirui Wang & Wei Li

  2. Cell Transplantation and Gene Therapy Institute, The Third Xiangya Hospital, Central South University, Changsha, Hunan, 410013, People’s Republic of China

    Xiaoying Li, Qi Liang, Yu Gan, Jinzhuang Liao, Ruirui Wang & Wei Li

  3. Department of Pathology, National Clinical Research Center for Geriatric Disorders, Xiangya Hospital of Central South University, Changsha, Hunan, 410008, People’s Republic of China

    Li Zhou

  4. Department of Thoracic Surgery, Hunan Chest Hospital, Changsha, Hunan, 410006, People’s Republic of China

    Gaoyan Deng

  5. Department of Ultrasonography, Hunan Chest Hospital, Changsha, Hunan, 410006, People’s Republic of China

    Yeqing Xiao

  6. Department of Ultrasound, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, 430022, People’s Republic of China

    Shuangze Han

  7. Department of Otolaryngology Head and Neck Surgery, The Third Xiangya Hospital, Central South University, Changsha, Hunan, 410013, People’s Republic of China

    Xiang Qing

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  1. Xiaoying Li
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Contributions

All authors contributed to the study’s conception and design. Material preparation, data collection and analysis were performed by [Xiaoying Li], [Qi Liang], [Li Zhou], [Gaoyan Deng], [Yeqing Xiao], [Yu Gan], [Shuangze Han], [Jinzhuang Liao], [Ruirui Wang], [Xiang Qing] and [Wei Li]. Writing, review, and/or revision of the manuscript was written by [Xiaoying Li], [Qi Liang], [Li Zhou], [Xiang Qing] and [Wei Li]. All authors read and approved the final manuscript.

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Correspondence to Xiang Qing or Wei Li.

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The animal experiments were approved by the Institutional Animal Care and Use Committee (IACUC) of the Third Xiangya Hospital of Central South University (Changsha, China). Informed consent was obtained from all patients.

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Li, X., Liang, Q., Zhou, L. et al. Survivin degradation by bergenin overcomes pemetrexed resistance. Cell Oncol. 46, 1837–1853 (2023). https://doi.org/10.1007/s13402-023-00850-5

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