Heterogeneity of tertiary lymphoid structures predicts the response to neoadjuvant therapy and immune microenvironment characteristics in triple-negative breast cancer

Br J Cancer. 2025 Feb;132(3):295-310. doi: 10.1038/s41416-024-02917-y. Epub 2024 Dec 10.

Abstract

Background: Tertiary lymphoid structures (TLSs) impact cancer outcomes, including in triple-negative breast cancer (TNBC), where their role in immune modulation during neoadjuvant therapy (NAT) is underexplored.

Methods: This study employed single-cell RNA sequencing (scRNA-seq), multiplex immunofluorescence (mIF) staining, and radiomic techniques to evaluate TLSs and the tumour microenvironment (TME) in TNBC patient samples before and after NAT.

Results: The presence of TLSs in TNBC was associated with B-cell maturation and T-cell activation. Compared with TLS-low TNBC, TLS-high TNBC showed significantly greater expression of immunoglobulin family genes (IGHM and IGHG1) in B cells and greater cytotoxicity of neoantigen-specific CD8 + T cells (neoTCR8). Additionally, mIF revealed notable differences between TLSs and the TME in TNBC. Although CD8 + T-cell levels do not predict the NAT response effectively, TLS maturity strongly correlated with better NAT outcomes and prognosis (P < 0.05). An imaging biomarker scoring system was also developed to predict TLS status and NAT efficacy.

Conclusion: Our results demonstrated changes in TLSs and the TME in TNBC patients post-NAT. These findings confirm the predictive value of mature TLSs (mTLSs) and support the use of personalised immunotherapy based on post-NAT immune characteristics, thereby improving clinical outcomes.

MeSH terms

  • B-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Female
  • Humans
  • Middle Aged
  • Neoadjuvant Therapy / methods
  • Prognosis
  • Tertiary Lymphoid Structures* / genetics
  • Tertiary Lymphoid Structures* / immunology
  • Tertiary Lymphoid Structures* / pathology
  • Triple Negative Breast Neoplasms* / drug therapy
  • Triple Negative Breast Neoplasms* / genetics
  • Triple Negative Breast Neoplasms* / immunology
  • Triple Negative Breast Neoplasms* / pathology
  • Triple Negative Breast Neoplasms* / therapy
  • Tumor Microenvironment* / immunology