Predicting antigen-specific T-cell immunity against Wilms tumor 1 in hematologic cancer

Leukemia. 2025 Nov;39(11):2767-2778. doi: 10.1038/s41375-025-02727-y. Epub 2025 Aug 22.

Abstract

Wilms tumor 1 (WT1) is a tumor-associated antigen expressed in solid tumors and hematological malignancies. T-cell immunotherapies targeting WT1 are currently under development. To analyze endogenous T-cell responses against WT1, we trained computational models capable of detecting WT1-specific T-cell responses from T-cell receptor (TCR) sequencing data. We peptide-pulsed healthy donor and acute myeloid leukemia (AML) patient samples with VLDFAPPGA (VLD, WT137-45) and RMFPNAPYL (RMF, WT1126-134) peptides, then sequenced the WT1 dextramer-positive CD8 + T-cells with single-cell RNA + TCRαβ sequencing. The TCRGP machine-learning TCR-classification method was trained with epitope-specific and control TCR repertoires, and we obtained AUROC values of 0.74 (VLD) and 0.75 (RMF), allowing reliable identification of WT1-specific T-cells. In bulk TCRβ sequenced patient samples (AML n = 21, chronic myeloid leukemia (CML) n = 26, and myelodysplastic syndrome n = 25), the median WT1-specific T-cell abundance was similar to healthy controls, but their VLD and RMF-specific TCR repertoires exhibited higher clonality with two patients presenting up to 13% of WT1-specific T-cells. ScRNA+TCRαβ sequencing of AML bone marrow T-cells revealed that WT1-specific T-cells predominantly exhibit an effector or terminal effector memory phenotype. In conclusion, our novel computational models enable large-scale WT1-specific T-cell identification from TCR sequencing datasets and leukemia-antigen-specific immune response monitoring.

MeSH terms

  • Antigens, Neoplasm* / immunology
  • CD8-Positive T-Lymphocytes* / immunology
  • Epitopes, T-Lymphocyte / immunology
  • Hematologic Neoplasms* / immunology
  • Hematologic Neoplasms* / pathology
  • Humans
  • Machine Learning
  • Receptors, Antigen, T-Cell, alpha-beta / genetics
  • Receptors, Antigen, T-Cell, alpha-beta / immunology
  • T-Lymphocytes* / immunology
  • WT1 Proteins* / immunology

Substances

  • WT1 Proteins
  • WT1 protein, human
  • Antigens, Neoplasm
  • Epitopes, T-Lymphocyte
  • Receptors, Antigen, T-Cell, alpha-beta