HLA Ligand Atlas: a benign reference of HLA-presented peptides to improve T-cell-based cancer immunotherapy
Open accessAbstract
Background: The human leucocyte antigen (HLA) complex controls adaptive immunity by presenting defined fractions of the intracellular and extracellular protein content to immune cells. Understanding the benign HLA ligand repertoire is a prerequisite to define safe T-cell-based immunotherapies against cancer. Due to the poor availability of benign tissues, if available, normal tissue adjacent to the tumor has been used as a benign surrogate when defining tumor-associated antigens. However, this comparison has proven to be insufficient and even resulted in lethal outcomes. In order to match the tumor immunopeptidome with an equivalent counterpart, we created the HLA Ligand Atlas, the first extensive collection of paired HLA-I and HLA-II immunopeptidomes from 227 benign human tissue samples. This dataset facilitates a balanced comparison between tumor and benign tissues on HLA ligand level. Methods: Human tissue samples were obtained from 16 subjects at autopsy, five thymus samples and two ovary samples originating from living donors. HLA ligands were isolated via immunoaffinity purification and analyzed in over 1200 liquid chromatography mass spectrometry runs. Experimentally and computationally reproducible protocols were employed for data acquisition and processing. Results: The initial release covers 51 HLA-I and 86 HLA-II allotypes presenting 90,428 HLA-I- and 142,625 HLA-II ligands. The HLA allotypes are representative for the world population. We observe that immunopeptidomes differ considerably between tissues and individuals on source protein and HLA-ligand level. Moreover, we discover 1407 HLA-I ligands from non-canonical genomic regions. Such peptides were previously described in tumors, peripheral blood mononuclear cells (PBMCs), healthy lung tissues and cell lines. In a case study in glioblastoma, we show that potential on-target off-tumor adverse events in immunotherapy can be avoided by comparing tumor immunopeptidomes to the provided multi-tissue reference. Conclusion: Given that T-cell-based immunotherapies, such as CAR-T cells, affinity-enhanced T cell transfer, cancer vaccines and immune checkpoint inhibition, have significant side effects, the HLA Ligand Atlas is the first step toward defining tumor-associated targets with an improved safety profile. The resource provides insights into basic and applied immune-associated questions in the context of cancer immunotherapy, infection, transplantation, allergy and autoimmunity. It is publicly available and can be browsed in an easy-to-use web interface at https://hla-ligand-atlas.org .
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One peptide of the CTLA-4 transmembrane domain has been described as present on thymic tissue.
“Indeed, one peptide of the CTLA-4 transmembrane domain has been described as present on thymic tissue [45].”
From Preclinical development of an mRNA-based multiepitope immunotherapeutic for glioblastoma (2025) · cites this paper as [45]
The Results section describes HLA-presented peptides from benign tissues, and the Methods section confirms that thymus samples were analyzed. However, searches for CTLA-4, its alternative name, and transmembrane peptides found no passage identifying a CTLA-4 transmembrane-domain peptide in thymic tissue. (LLM, conf=0.73)
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“Indeed, one peptide of the CTLA-4 transmembrane domain has been described as present on thymic tissue [45].”
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- Authors
- Marcu, A., Bichmann, L., Kuchenbecker, L., Kowalewski, D. J., Freudenmann, L. K., Backert, L., Mühlenbruch, L., Szolek, A., Lübke, M., Wagner, P., Engler, T., Matovina, S., Wang, J., Hauri-Hohl, M., Martin, R., Kapolou, K., Walz, J. S., Velz, J., Moch, H., Regli, L., Silginer, M., Weller, M., Löffler, M. W., Erhard, F., Schlosser, A., Kohlbacher, O., Stevanović, S., Rammensee, H.-G., & Neidert, M. C.
- Affiliations
- University of Tübingen (DE)
- Applied Bioinformatics, Department of Computer Science, University of Tübingen, Tübingen, Germany
- German Cancer Research Center (DE)
- Universitätsklinikum Tübingen (DE)
- University of Zurich (CH)
- University Children's Hospital Zurich (CH)
- Neuroimmunology and MS Research, Neurology Clinic, University Hospital Zurich, University of Zurich, Zurich, Switzerland
- Department of Immunology, Interfaculty Institute for Cell Biology, University of Tübingen, Tübingen, Germany
- University of Würzburg (DE)
- Rudolf Virchow Center - Center for Integrative and Translational Bioimaging, Julius-Maximilians-University Würzburg, Würzburg, Germany
- Corresponding author
- Marcu, Ana
- ORCID
- Marcu, Ana
- Bichmann, Leon
- Kuchenbecker, Leon
- Kowalewski, Daniel Johannes
- Freudenmann, Lena Katharina
- Backert, Linus
- Szolek, András
- Lübke, Maren
- Wagner, Philipp
- Engler, Tobias
- Matovina, Sabine
- Wang, Jian
- Hauri-Hohl, Mathias
- Walz, Juliane Sarah
- Velz, Julia
- Moch, Holger
- Regli, Luca
- Silginer, Manuela
- Weller, Michael
- Löffler, Markus W.
- Erhard, Florian
- Kohlbacher, Oliver
- Stevanović, Stefan
- Rammensee, Hans-Georg
- Neidert, Marian Christoph
- Venue
- Journal for ImmunoTherapy of Cancer
- Publisher
- BMJ
- Published
- 2021-04
- Volume
- 9
- Issue
- 4
- Pages
- e002071
- ISSN
- 2051-1426 (ISSN-L)
- PMC
- PMC8054196
- OpenAlex
- W3156888771
- Cited by
- 250
- References
- 71
- Citations by year
- 2026: 41 · 2025: 54 · 2024: 32 · 2023: 61 · 2022: 33 · 2021: 28 · 2020: 1
- FWCI
- 12.09
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Journal for ImmunoTherapy of Cancer (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Online Publication Service of Würzburg University (Würzburg University) (submittedVersion, cc-by)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by)
- ETH Zürich Research Collection (cc-by)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- German Ministry for Research and Education (de.NBI - FKZ: 31A535A)
- Bosch Research Foundation
- Deutsche Forschungsgemeinschaft (de.NBI - FKZ: 31A535A)
- European Research Council (AdG 339842 MUTAEDITING)
- Boehringer Ingelheim Fonds for Basic Research in Medicine
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › vaccines and immunoinformatics approaches
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Keywords
- HLA-presented peptides, immunopeptidome, HLA class I, HLA class II, tumor immunopeptidome, on-target off-tumor toxicity, cancer immunotherapy safety, glioblastoma, chimeric antigen receptor T cells, cancer vaccines, immune checkpoint blockade, T cell-based immunotherapy
- MeSH terms
- Receptors, Chimeric Antigen, Aged, Aged, 80 and over, Antigens, Neoplasm, Chromatography, Liquid, Female, HLA Antigens, Humans, Infant, Infant, Newborn, Ligands, Male, Middle Aged, Neoplasms, Peptides, T-Lymphocytes, Immunotherapy, Adoptive, Proteome, Databases, Protein, Proteomics, Tandem Mass Spectrometry
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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