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Abstract
Oral squamous cell carcinoma (OSCC) is the most common type of oral malignancy, and metastasis accounts for the poor prognosis of OSCC. Autophagy is considered to facilitate OSCC development by mitigating various cellular stresses; nevertheless, the mechanisms of autophagy in OSCC cell proliferation and metastasis remain unknown. In our study, high-sensitivity label-free quantitative proteomics analysis revealed nuclear protein 1 (NUPR1) as the most significantly upregulated protein in formalin-fixed paraffin-embedded tumour samples derived from OSCC patients with or without lymphatic metastasis. Moreover, NUPR1 is aberrantly expressed in the OSCC tissues and predicts low overall survival rates for OSCC patients. Notably, based on tandem mass tag-based quantitative proteomic analysis between stable NUPR1 knockdown OSCC cells and scrambled control OSCC cells, we confirmed that NUPR1 maintained autophagic flux and lysosomal functions by directly increasing transcription factor E3 (TFE3) activity, which promoted OSCC cell proliferation and metastasis in vitro and in vivo. Collectively, our data revealed that the NUPR1–TFE3 axis is a critical regulator of the autophagic machinery in OSCC progression, and this study may provide a potential therapeutic target for the treatment of OSCC.
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1 Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Research Unit of Oral and Maxillofacial Regenerative Medicine, Chinese Academy of Medical Sciences, Department of Oral and Maxillofacial-Head Neck Oncology, Shanghai, China (GRID:grid.16821.3c) (ISNI:0000 0004 0368 8293); Zhang Zhiyuan Academician Workstation, Hainan Western Central Hospital, Shanghai Ninth People’s Hospital, Department of Oral and Maxillofacial Surgery, Danzhou, China (GRID:grid.412523.3) (ISNI:0000 0004 0386 9086); The Second Xiangya Hospital of Central South University, Department of Oral and Maxillofacial Surgery, Changsha, China (GRID:grid.452708.c) (ISNI:0000 0004 1803 0208)
2 Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Research Unit of Oral and Maxillofacial Regenerative Medicine, Chinese Academy of Medical Sciences, Department of Oral and Maxillofacial-Head Neck Oncology, Shanghai, China (GRID:grid.16821.3c) (ISNI:0000 0004 0368 8293); Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Department of Oral Pathology, Shanghai, China (GRID:grid.16821.3c) (ISNI:0000 0004 0368 8293)
3 The Second Xiangya Hospital of Central South University, Department of Oral and Maxillofacial Surgery, Changsha, China (GRID:grid.452708.c) (ISNI:0000 0004 1803 0208)
4 Third Military Medical University, Department of Occupational Health, Chongqing, China (GRID:grid.410570.7) (ISNI:0000 0004 1760 6682)
5 The Second Xiangya Hospital of Central South University, Department of Pathology, Changsha, China (GRID:grid.452708.c) (ISNI:0000 0004 1803 0208)
6 Guangxi University, School of Medicine, Nanning, China (GRID:grid.256609.e) (ISNI:0000 0001 2254 5798)
7 Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Research Unit of Oral and Maxillofacial Regenerative Medicine, Chinese Academy of Medical Sciences, Department of Oral and Maxillofacial-Head Neck Oncology, Shanghai, China (GRID:grid.16821.3c) (ISNI:0000 0004 0368 8293)
8 Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Research Unit of Oral and Maxillofacial Regenerative Medicine, Chinese Academy of Medical Sciences, Department of Oral and Maxillofacial-Head Neck Oncology, Shanghai, China (GRID:grid.16821.3c) (ISNI:0000 0004 0368 8293); Zhang Zhiyuan Academician Workstation, Hainan Western Central Hospital, Shanghai Ninth People’s Hospital, Department of Oral and Maxillofacial Surgery, Danzhou, China (GRID:grid.412523.3) (ISNI:0000 0004 0386 9086)
9 Affiliated Hospital of Guilin Medical University, Department of Oral and Maxillofacial Surgery, Guilin, China (GRID:grid.443385.d) (ISNI:0000 0004 1798 9548)
10 Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, Third Military Medical University, Chongqing, China (GRID:grid.416208.9) (ISNI:0000 0004 1757 2259)
11 First Affiliated Hospital and Department of Environmental Medicine, School of Public Health, School of Medicine, Zhejiang University, Department of Emergency Medicine, Hangzhou, China (GRID:grid.13402.34) (ISNI:0000 0004 1759 700X)