Single-cell and spatial transcriptome analyses reveal tertiary lymphoid structures linked to tumour progression and immunotherapy response in nasopharyngeal carcinoma

Nat Commun. 2024 Sep 4;15(1):7713. doi: 10.1038/s41467-024-52153-4.

Abstract

Tertiary lymphoid structures are immune cell aggregates linked with cancer outcomes, but their interactions with tumour cell aggregates are unclear. Using nasopharyngeal carcinoma as a model, here we analyse single-cell transcriptomes of 343,829 cells from 77 biopsy and blood samples and spatially-resolved transcriptomes of 31,316 spots from 15 tumours to decipher their components and interactions with tumour cell aggregates. We identify essential cell populations in tertiary lymphoid structure, including CXCL13+ cancer-associated fibroblasts, stem-like CXCL13+CD8+ T cells, and B and T follicular helper cells. Our study shows that germinal centre reaction matures plasma cells. These plasma cells intersperse with tumour cell aggregates, promoting apoptosis of EBV-related malignant cells and enhancing immunotherapy response. CXCL13+ cancer-associated fibroblasts promote B cell adhesion and antibody production, activating CXCL13+CD8+ T cells that become exhausted in tumour cell aggregates. Tertiary lymphoid structure-related cell signatures correlate with prognosis and PD-1 blockade response, offering insights for therapeutic strategies in cancers.

MeSH terms

  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes* / metabolism
  • Chemokine CXCL13* / genetics
  • Chemokine CXCL13* / metabolism
  • Disease Progression
  • Fibroblasts / immunology
  • Fibroblasts / metabolism
  • Gene Expression Profiling
  • Humans
  • Immunotherapy* / methods
  • Nasopharyngeal Carcinoma* / genetics
  • Nasopharyngeal Carcinoma* / immunology
  • Nasopharyngeal Carcinoma* / metabolism
  • Nasopharyngeal Carcinoma* / pathology
  • Nasopharyngeal Carcinoma* / therapy
  • Nasopharyngeal Neoplasms* / genetics
  • Nasopharyngeal Neoplasms* / immunology
  • Nasopharyngeal Neoplasms* / pathology
  • Nasopharyngeal Neoplasms* / therapy
  • Prognosis
  • Single-Cell Analysis*
  • Tertiary Lymphoid Structures* / genetics
  • Tertiary Lymphoid Structures* / immunology
  • Transcriptome
  • Tumor Microenvironment / genetics
  • Tumor Microenvironment / immunology

Substances

  • Chemokine CXCL13
  • CXCL13 protein, human