Mature tertiary lymphoid structures evoke intra-tumoral T and B cell responses via progenitor exhausted CD4+ T cells in head and neck cancer

Nat Commun. 2025 May 7;16(1):4228. doi: 10.1038/s41467-025-59341-w.

Abstract

Tumor tertiary lymphoid structures (TLS), especially mature TLS (mTLS), have been associated with better prognosis and improved responses to immune checkpoint blockade (ICB), but the underlying mechanisms remain incompletely understood. Here, by performing single-cell RNA, antigen receptor sequencing and spatial transcriptomics on tumor tissue from head and neck squamous cell carcinoma (HNSCC) patients with different statuses of TLS, we observe that mTLS are enriched with stem-like T cells, and B cells at various maturation stages. Notably, progenitor exhausted CD4+ T cells, with features resembling follicular helper T cells, support these responses, by activating B cells to produce plasma cells in the germinal center, and interacting with DC-LAMP+ dendritic cells to support CD8+ T cell activation. Conversely, non-mTLS tumors do not promote local anti-tumor immunity which is abundant of immunosuppressive cells or a lack of stem-like B and T cells. Furthermore, patients with mTLS manifest improved overall survival and response to ICB compared to those with non-mTLS. Overall, our study provides insights into mechanisms underlying mTLS-mediated intra-tumoral immunity events against cancer.

MeSH terms

  • B-Lymphocytes* / immunology
  • CD4-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Dendritic Cells / immunology
  • Female
  • Head and Neck Neoplasms* / drug therapy
  • Head and Neck Neoplasms* / genetics
  • Head and Neck Neoplasms* / immunology
  • Head and Neck Neoplasms* / pathology
  • Humans
  • Immune Checkpoint Inhibitors / therapeutic use
  • Lymphocyte Activation / immunology
  • Male
  • Middle Aged
  • Squamous Cell Carcinoma of Head and Neck* / drug therapy
  • Squamous Cell Carcinoma of Head and Neck* / genetics
  • Squamous Cell Carcinoma of Head and Neck* / immunology
  • Squamous Cell Carcinoma of Head and Neck* / pathology
  • Tertiary Lymphoid Structures* / immunology
  • Tertiary Lymphoid Structures* / pathology

Substances

  • Immune Checkpoint Inhibitors