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Ubiquitin-specific protease 54 regulates GLUT1-mediated aerobic glycolysis to inhibit lung adenocarcinoma progression by modifying p53 degradation

Oncogene (2024)Cite this article

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Abstract

Lung adenocarcinoma (LUAD) is one of the most prevalent types of cancer. Ubiquitination is crucial in modulating cell proliferation and aerobic glycolysis in cancer. The frequency of TP53 mutations in LUAD is approximately 50%. Currently, therapeutic targets for wild-type (WT) p53-expressing LUAD are limited. In the present study, we systemically explored the expression of ubiquitin-specific protease genes using public datasets. Then, we focused on ubiquitin-specific protease 54 (USP54), and explored its prognostic significance in LUAD patients using public datasets, analyses, and an independent cohort from our center. We found that the expression of USP54 was lower in LUAD tissues compared with that in the paracancerous tissues. Low USP54 expression levels were linked to a malignant phenotype and worse survival in patients with LUAD. The results of functional experiments revealed that up-regulation of USP54 suppressed LUAD cell proliferation in vivo and in vitro. USP54 directly interacted with p53 protein and the levels of ubiquitinated p53 were inversely related to USP54 levels, consistent with a role of USP54 in deubiquitinating p53 in p53-WT LUAD cells. Moreover, up-regulation of the USP54 expression inhibited aerobic glycolysis in LUAD cells. Importantly, we confirmed that USP54 inhibited aerobic glycolysis and the growth of tumor cells by a p53-mediated decrease in glucose transporter 1 (GLUT1) expression in p53-WT LUAD cells. Altogether, we determined a novel mechanism of survival in the p53-WT LUAD cells to endure the malnourished tumor microenvironment and provided insights into the role of USP54 in the adaptation of p53-WT LUAD cells to metabolic stress.

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Fig. 1: Comprehensive analysis of the ubiquitin-specific protease genes in lung adenocarcinoma.
Fig. 2: Relative USP54 expression in lung adenocarcinoma and its clinical significance.
Fig. 3: USP54 inhibits the growth of lung adenocarcinoma cells in vitro and in vivo.
Fig. 4: USP54 increases p53 protein concentrations and USP54 directly interacts with p53 in the p53-WT lung adenocarcinoma cells.
Fig. 5: USP54 increases p53 protein concentrations by inhibiting the ubiquitination and degradation of p53 in p53-wild type lung adenocarcinoma cells.
Fig. 6: USP54 inhibits aerobic glycolysis and promotes mitochondrial respiration in the LUAD cells.
Fig. 7: USP54 inhibits tumor cell growth and aerobic glycolysis by decreasing GLUT1 expression via p53 in lung adenocarcinoma cells.
Fig. 8: A model summarizing the role of USP54 in LUAD.

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Data availability

All data analyzed or generated in this study are included in this manuscript for publication. Other datasets used or analyzed (or both) in this study can be obtained from the corresponding authors upon reasonable request.

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Acknowledgements

The authors are grateful to the work staff from the biobank and pathology department of Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College for providing samples.

Funding

This work was supported by the National Key R&D Program of China (2021YFF1201300), National Natural Science Foundation of China (82122053, 82188102), Natural Science Foundation of Jiangxi Province (20212BCJ23022), R&D Program of Beijing Municipal Education Commission (KJZD20191002302), CAMS Initiative for Innovative Medicine (2021-I2M-1-012, 2022-I2M-2-001), Key-Area Research and Development Program of Guangdong Province (2021B0101420005), Shenzhen Science and Technology Program (ZDSYS20220606101604009, RCJC20221008092811025, KCXFZ20201221173008022), Shenzhen High-level Hospital Construction Fund (CFA202201001, SZ2020ZD001), Shenzhen Clinical Research Center for Cancer (No.〔2021〕287), and Sanming Project of Medicine in Shenzhen (SZSM202211011).

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  1. These authors contributed equally: Leifeng Chen, Lin Zhang

Authors and Affiliations

  1. Department of Thoracic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, 100021, Beijing, China

    Leifeng Chen, Haihua He & Jie He

  2. Department of Oncology, Renmin Hospital of Wuhan University, Wuhan, 430060, China

    Leifeng Chen & Haihua He

  3. Laboratory of Translational Medicine, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, 100021, Beijing, China

    Leifeng Chen, Haihua He, Fei Shao & Jie He

  4. Medical Center for Cardiovascular Diseases, Neurological Diseases and Tumors of Jiangxi Province, the Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, 330006, China

    Leifeng Chen

  5. Department of Thoracic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital & Shenzhen Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Shenzhen, 518116, China

    Lin Zhang & Zhentao Yu

  6. Cancer Center, Renmin Hospital of Wuhan University, Wuhan 430060, China

    Lin Zhang & Jie He

  7. Central Laboratory & Shenzhen Key Laboratory of Epigenetics and Precision Medicine for Cancers, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital & Shenzhen Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Shenzhen, 518116, China

    Yibo Gao

  8. Laboratory of Thoracic Oncology & Department of Thoracic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China

    Yibo Gao

  9. Translational Medicine Platform, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China

    Yibo Gao

  10. State Key Laboratory of Molecular Oncology, National Cancer Center, National Clinical Research Center for Cancer, Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China

    Yibo Gao & Jie He

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Contributions

All authors listed have contributed intellectually, directly, and substantially to this research and are authorized to publish it. Conception and design: LC and YG. Performing the experiments: LC and LZ. Provision of study materials or patients: LZ, ZY and FS. Analysis and interpretation of data: LC and HH. Writing and reviewing the manuscript: LC, LZ and YG. Supervision: YG and JH. All authors have read and approved the final manuscript.

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Correspondence to Yibo Gao or Jie He.

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Human tissues were used in accordance with the guidelines of the Declaration of Helsinki, and informed consent was waived by the Independent Ethics Committee of Cancer Hospital, Chinese Academy of Medical Sciences, considering the retrospective nature of the study. The approval to use these samples for further analysis was also obtained from the same committee. Animal experiments were approved by the same committee.

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Chen, L., Zhang, L., He, H. et al. Ubiquitin-specific protease 54 regulates GLUT1-mediated aerobic glycolysis to inhibit lung adenocarcinoma progression by modifying p53 degradation. Oncogene (2024). https://doi.org/10.1038/s41388-024-03047-8

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