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USP22 Deubiquitinates CD274 to Suppress Anticancer Immunity

Xing Huang, Qi Zhang, Yu Lou, Junli Wang, Xinyu Zhao, Lin Wang, Xiaozhen Zhang, Shanshan Li, Yulan Zhao, Qi Chen, Tingbo Liang and Xueli Bai
Xing Huang
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
2The Key Laboratory of Developmental Genes and Human Disease, Institute of Life Sciences, Southeast University, Nanjing, Jiangsu, China.
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  • ORCID record for Xing Huang
  • For correspondence: dr.huangxing@foxmail.com liangtingbo@zju.edu.cn shirleybai@zju.edu.cn
Qi Zhang
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
3Department of Hepatobiliary and Pancreatic Surgery, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
4Innovation Center for the Study of Pancreatic Diseases, Zhejiang Province, Hangzhou, Zhejiang, China.
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Yu Lou
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
3Department of Hepatobiliary and Pancreatic Surgery, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
4Innovation Center for the Study of Pancreatic Diseases, Zhejiang Province, Hangzhou, Zhejiang, China.
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Junli Wang
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
3Department of Hepatobiliary and Pancreatic Surgery, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
4Innovation Center for the Study of Pancreatic Diseases, Zhejiang Province, Hangzhou, Zhejiang, China.
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Xinyu Zhao
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
3Department of Hepatobiliary and Pancreatic Surgery, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
4Innovation Center for the Study of Pancreatic Diseases, Zhejiang Province, Hangzhou, Zhejiang, China.
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Lin Wang
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
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Xiaozhen Zhang
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
3Department of Hepatobiliary and Pancreatic Surgery, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
4Innovation Center for the Study of Pancreatic Diseases, Zhejiang Province, Hangzhou, Zhejiang, China.
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Shanshan Li
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
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Yulan Zhao
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
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Qi Chen
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
3Department of Hepatobiliary and Pancreatic Surgery, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
4Innovation Center for the Study of Pancreatic Diseases, Zhejiang Province, Hangzhou, Zhejiang, China.
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Tingbo Liang
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
3Department of Hepatobiliary and Pancreatic Surgery, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
4Innovation Center for the Study of Pancreatic Diseases, Zhejiang Province, Hangzhou, Zhejiang, China.
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  • For correspondence: dr.huangxing@foxmail.com liangtingbo@zju.edu.cn shirleybai@zju.edu.cn
Xueli Bai
1Zhejiang Provincial Key Laboratory of Pancreatic Disease, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
3Department of Hepatobiliary and Pancreatic Surgery, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.
4Innovation Center for the Study of Pancreatic Diseases, Zhejiang Province, Hangzhou, Zhejiang, China.
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  • For correspondence: dr.huangxing@foxmail.com liangtingbo@zju.edu.cn shirleybai@zju.edu.cn
DOI: 10.1158/2326-6066.CIR-18-0910
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Abstract

PD-1 (CD279)–PD-L1 (CD274) inhibitory signaling is critical for cancer immune evasion, and thus has become one of the major targets in anticancer immunotherapy. There are several studies that demonstrate the potent effects of posttranslational modifications of CD274 on immune inactivation and suppression, such as ubiquitination, phosphorylation, glycosylation, and palmitoylation. However, the regulatory mechanisms for CD274 deubiquitination are still largely unclear. Here, we identified ubiquitin-specific protease 22 (USP22) as a novel deubiquitinase of CD274. USP22 directly interacted with the C terminus of CD274, inducing its deubiquitination and stabilization. Across multiple cancer types, USP22 was highly expressed and frequently altered in liver cancer, closely correlating with poor prognosis of these patients. Genetic depletion of USP22 inhibited liver cancer growth in an immune system–dependent manner, increased tumor immunogenicity and tumor-infiltrating lymphocytes, and improved therapeutic efficacy of CD274-targeted immunotherapy and CDDP-based chemotherapy in mice. We demonstrate that targeting USP22 is a promising strategy to potentiate anticancer immunity for CD274-amplified cancer.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Immunology Research Online (http://cancerimmunolres.aacrjournals.org/).

  • Cancer Immunol Res 2019;XX:XX–XX

  • Received December 19, 2018.
  • Revision received April 8, 2019.
  • Accepted August 5, 2019.
  • Published first August 9, 2019.
  • ©2019 American Association for Cancer Research.
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This OnlineFirst version was published on September 9, 2019
doi: 10.1158/2326-6066.CIR-18-0910

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USP22 Deubiquitinates CD274 to Suppress Anticancer Immunity
Xing Huang, Qi Zhang, Yu Lou, Junli Wang, Xinyu Zhao, Lin Wang, Xiaozhen Zhang, Shanshan Li, Yulan Zhao, Qi Chen, Tingbo Liang and Xueli Bai
Cancer Immunol Res September 9 2019 DOI: 10.1158/2326-6066.CIR-18-0910

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USP22 Deubiquitinates CD274 to Suppress Anticancer Immunity
Xing Huang, Qi Zhang, Yu Lou, Junli Wang, Xinyu Zhao, Lin Wang, Xiaozhen Zhang, Shanshan Li, Yulan Zhao, Qi Chen, Tingbo Liang and Xueli Bai
Cancer Immunol Res September 9 2019 DOI: 10.1158/2326-6066.CIR-18-0910
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