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Immune escape of head and neck cancer mediated by the impaired MHC-I antigen presentation pathway

Oncogene volume 43, pages 388–394 (2024)Cite this article

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Abstract

Tumor immune evasion is a hallmark of Head and Neck Cancers. The advent of immune checkpoint inhibitors (ICIs) in the first-line setting has transformed the management of these tumors. Unfortunately, the response rate of Head and Neck Squamous Cell Carcinomas (HNSCC) to ICIs is below 15%, regardless of the human papillomavirus (HPV) status, which might be partially related with impaired antigen presentation machinery (APM). Mechanistically, HNSCC cells are usually defective in the expression of MHC-I associated APM, while this transcriptional pathway is critical for the activation of tumor-killing effector T-cells. To specifically illuminate the phenomenon and seek for therapeutic strategies, this review summarizes the most recently identified role of genetic and functional dysregulation of the MHC-I pathway, specifically through changes at the genetic, epigenetic, post-transcriptional, and post-translational levels, which substantially contributes to HNSCC immune escape and ICI resistance. Several treatment modalities can be potentially exploited to restore APM signaling in tumors, which improves anti-tumor immunity through the activation of interferons, vaccines or rimantadine against HPV and the inhibition of EGFR, SHP-2, PI3K and MEK. Additionally, the combinatorial use of radiotherapy or cytotoxic agents with ICIs can synergize to potentiate APM signaling. Future directions would include further dissection of MHC-I related APM signaling in HNSCC and whether reversing this inhibition in combination with ICIs would elicit a more robust immune response leading to improved response rates in HNSCC.

Therapeutic approaches to restore the MHC-I antigen presentation machinery in Head and Neck Cancer. (Red color texts represent the according strategies and the outcomes).

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Fig. 1: Schematic image illuminating the physiological MHC-I antigen presentation of altered proteins from tumor cell to cytotoxic T cell mediated by several pivotal APM proteins and MHC-I complex.
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Acknowledgements

We would like to thank all authors of these original studies who conducted these relevant researches referenced in this review. This work is supported by National Natural Science Foundation of China (82272899, 81902782 are awarded to XL, 81730030 is awarded to QC, 82203180 is awarded to YQ), Research Funding from West China School/Hospital of Stomatology Sichuan University (No.RCDWJS2022-16, to XL), the 14th special grant from China Postdoctoral Science Foundation (2021T140484, to XL), Postdoctoral Research Funding of Sichuan University (2022SCU12132, to XL), Research and Exploration Program of West China Hospital of Stomatology of Sichuan University(No. RD-02-202204, to XL), Key Research Program of Sichuan Provincial Science and Technology Agency (2023YFS0127, to XL) and the CAMS Innovation Fund for Medical Sciences(CIFMS,2019-I2M-5-004, to QC).

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  1. These authors contributed equally: Xiaobo Luo, Yan Qiu.

Authors and Affiliations

  1. State Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases & Research Unit of Oral Carcinogenesis and Management & Chinese Academy of Medical Sciences, Department of Oral Medicine, West China Hospital of Stomatology, Sichuan University, Chengdu, 610041, Sichuan, China

    Xiaobo Luo, Qiuhao Wang & Qianming Chen

  2. Department of Pathology, West China Hospital, Sichuan University, Chengdu, 610041, China

    Yan Qiu

  3. Department of Periodontics and Oral Medicine, Department of Otolaryngology–Head and Neck Surgery, Rogel Cancer Center, the University of Michigan, Ann Arbor, MI, 48109, USA

    Zackary R. Fitzsimonds & Yu Leo Lei

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XL and YQ contributed to the conception, design, drafting and revision of the manuscript; YLL and QC contributed to the conception, review, and revision of the manuscript; ZRF, QW contributed to the revision and figure production of the manuscript; All authors read and approved the final manuscript. XL and YQ made equal contributions as co-first authors.

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Correspondence to Qianming Chen or Yu Leo Lei.

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YLL co-founded and serves on the Scientific Advisory Board of Saros Therapeutics. All other authors declare no conflicts of interest with relevance to this article. No medical writer or generative AI tool was involved in the preparation of the manuscript.

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Luo, X., Qiu, Y., Fitzsimonds, Z.R. et al. Immune escape of head and neck cancer mediated by the impaired MHC-I antigen presentation pathway. Oncogene 43, 388–394 (2024). https://doi.org/10.1038/s41388-023-02912-2

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