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Assessment of human leukocyte antigen-based neoantigen presentation to determine pan-cancer response to immunotherapy

Author

Listed:
  • Jiefei Han

    (Chinese Academy of Medical Sciences and Peking Union Medical College
    Capital Medical University)

  • Yiting Dong

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Xiuli Zhu

    (Geneplus-Beijing Institute
    University of Chinese Academy of Sciences
    Chinese Academy of Sciences and China National Center for Bioinformation)

  • Alexandre Reuben

    (The University of Texas M. D. Anderson Cancer Center)

  • Jianjun Zhang

    (The University of Texas M. D. Anderson Cancer Center)

  • Jiachen Xu

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Hua Bai

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Jianchun Duan

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Rui Wan

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Jie Zhao

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Jing Bai

    (Geneplus-Beijing Institute)

  • Xuefeng Xia

    (Geneplus-Beijing Institute)

  • Xin Yi

    (Geneplus-Beijing Institute)

  • Chao Cheng

    (Baylor College of Medicine)

  • Jie Wang

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Zhijie Wang

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

Abstract

Despite the central role of human leukocyte antigen class I (HLA-I) in tumor neoantigen presentation, quantitative determination of presentation capacity remains elusive. Based on a pooled pan-cancer genomic dataset of 885 patients treated with immune checkpoint inhibitors (ICIs), we developed a score integrating the binding affinity of neoantigens to HLA-I, as well as HLA-I allele divergence, termed the HLA tumor-Antigen Presentation Score (HAPS). Patients with a high HAPS were more likely to experience survival benefit following ICI treatment. Analysis of the tumor microenvironment indicated that the antigen presentation pathway was enriched in patients with a high HAPS. Finally, we built a neural network incorporating factors associated with neoantigen production, presentation, and recognition, which exhibited potential for differentiating cancer patients likely to benefit from ICIs. Our findings highlight the clinical utility of evaluating HLA-I tumor antigen presentation capacity and describe how ICI response may depend on HLA-mediated immunity.

Suggested Citation

  • Jiefei Han & Yiting Dong & Xiuli Zhu & Alexandre Reuben & Jianjun Zhang & Jiachen Xu & Hua Bai & Jianchun Duan & Rui Wan & Jie Zhao & Jing Bai & Xuefeng Xia & Xin Yi & Chao Cheng & Jie Wang & Zhijie W, 2024. "Assessment of human leukocyte antigen-based neoantigen presentation to determine pan-cancer response to immunotherapy," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45361-5
    DOI: 10.1038/s41467-024-45361-5
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    References listed on IDEAS

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    1. Marta Łuksza & Zachary M. Sethna & Luis A. Rojas & Jayon Lihm & Barbara Bravi & Yuval Elhanati & Kevin Soares & Masataka Amisaki & Anton Dobrin & David Hoyos & Pablo Guasp & Abderezak Zebboudj & Rebec, 2022. "Neoantigen quality predicts immunoediting in survivors of pancreatic cancer," Nature, Nature, vol. 606(7913), pages 389-395, June.
    2. Mahesh Yadav & Suchit Jhunjhunwala & Qui T. Phung & Patrick Lupardus & Joshua Tanguay & Stephanie Bumbaca & Christian Franci & Tommy K. Cheung & Jens Fritsche & Toni Weinschenk & Zora Modrusan & Ira M, 2014. "Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing," Nature, Nature, vol. 515(7528), pages 572-576, November.
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