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USP10 promotes migration and cisplatin resistance in esophageal squamous cell carcinoma cells

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Abstract

Cisplatin-based chemotherapy is the main treatment option for advanced or metastatic esophageal squamous cell carcinoma (ESCC). However, most ESCC patients develop drug resistance within 2 years after receiving cisplatin chemotherapy. Ubiquitin-specific protease 10 (USP10) is abnormally expressed in a variety of cancers, but the mechanistic roles of USP10 in ESCC are still obscure. Here, the effects of USP10 on the migration and cisplatin resistance of ESCC in vivo and in vitro and the underlying mechanisms have been investigated by bioinformatics analysis, RT-PCR, western blotting, immunoprecipitation, immunohistochemistry, cell migration and MTS cell proliferation assays, deubiquitination assay, and mouse tail vein injection model. USP10 was significantly up-regulated in ESCC tissues compared with adjacent normal tissues in both public databases and clinical samples and was closely associated with overall survival. Subsequent results revealed that USP10 contributed to the migration and cisplatin resistance of ESCC cells, while knocking down USP10 in cisplatin-resistant cells exhibited opposite effects in vitro and in vivo. Further Co-IP experiments showed that integrin β1 and YAP might be targets for USP10 deubiquitination. Moreover, deficiency of USP10 significantly inhibited the migrative and chemo-resistant abilities of ESCC cells, which could be majorly reversed by integrin β1 or YAP reconstitution. Altogether, USP10 was required for migration and cisplatin resistance in ESCC through deubiquinating and stabilizing integrin β1/YAP, highlighting that inhibition of USP10 may be a potential therapeutic strategy for ESCC.

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Abbreviations

AML:

Acute myeloid leukemia

DUBs:

Deubiquitinating enzyme

HEEC:

Human esophageal epithelial cells

USP10:

Ubiquitin-specific protease 10

YAP:

Yes-associated protein

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Funding

This study is partly supported by grants from the National Natural Science Foundation of China (Grant No. 32201047 to Q.H.), the Natural Science Foundation of Jiangsu Province (Grant No. BK20221373 to S.H.), the key project of Jiangsu Provincial Health Commission (Grant No. ZD2021038 to B.D.), and Postgraduate Research & Practice Innovation Program of Jiangsu Province (Grant No. SCJX23_2033 to C.L.).

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Author notes

  1. Sicong Hou and Tiantian Zhao have contributed equally to this work.

Authors and Affiliations

  1. Department of Gastroenterology, Affiliated Hospital of Yangzhou University, Yangzhou University, Yangzhou, 225001, Jiangsu Province, China

    Sicong Hou, Tiantian Zhao, Bin Deng, Caimin Li & Wenqian Li

  2. Department of Clinical Medicine, Medical College, Yangzhou University, Yangzhou, 225009, Jiangsu Province, China

    Tiantian Zhao, Caimin Li & Wenqian Li

  3. Department of Laboratory Medicine, The First People’s Hospital of Yancheng, Yancheng, 224006, Jiangsu Province, China

    Haifeng Huang

  4. Department of Laboratory Medicine, Yancheng First Hospital, Affiliated Hospital of Nanjing University Medical School, Yancheng, 224006, Jiangsu Province, China

    Haifeng Huang

  5. Department of Laboratory Medicine, Institute of Translational Medicine, Medical College, Yangzhou University, Yangzhou, 225001, China

    Qinglei Hang

  6. Jiangsu Key Laboratory of Integrated Traditional Chinese and Western Medicine for Prevention and Treatment of Senile Diseases, Yangzhou, 225001, China

    Qinglei Hang

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  1. Sicong Hou
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Contributions

SH and TZ: contributed to conceptualization, methodology, writing, and original draft preparation. CL and WL: contributed to investigation. BD and HH: contributed to validation. QH: contributed to supervision and editing.

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Correspondence to Qinglei Hang.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of Affiliated Hospital of Yangzhou University. The guidelines for the care and use of animals were approved by the Medicine Animal Welfare Committee of Yangzhou University.

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Hou, S., Zhao, T., Deng, B. et al. USP10 promotes migration and cisplatin resistance in esophageal squamous cell carcinoma cells. Med Oncol 41, 33 (2024). https://doi.org/10.1007/s12032-023-02272-7

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