Immune checkpoint therapy responders display early clonal expansion of tumor infiltrating lymphocytes

Oncoimmunology. 2024 Apr 26;13(1):2345859. doi: 10.1080/2162402X.2024.2345859. eCollection 2024.

Abstract

Immune checkpoint therapy (ICT) causes durable tumour responses in a subgroup of patients, but it is not well known how T cell receptor beta (TCRβ) repertoire dynamics contribute to the therapeutic response. Using murine models that exclude variation in host genetics, environmental factors and tumour mutation burden, limiting variation between animals to naturally diverse TCRβ repertoires, we applied TCRseq, single cell RNAseq and flow cytometry to study TCRβ repertoire dynamics in ICT responders and non-responders. Increased oligoclonal expansion of TCRβ clonotypes was observed in responding tumours. Machine learning identified TCRβ CDR3 signatures unique to each tumour model, and signatures associated with ICT response at various timepoints before or during ICT. Clonally expanded CD8+ T cells in responding tumours post ICT displayed effector T cell gene signatures and phenotype. An early burst of clonal expansion during ICT is associated with response, and we report unique dynamics in TCRβ signatures associated with ICT response.

Keywords: Immune checkpoint therapy; T cell receptor (TCR) sequencing; T cells; immune repertoire; machine learning; tumour-infiltrating lymphocytes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Female
  • Humans
  • Immune Checkpoint Inhibitors* / pharmacology
  • Immune Checkpoint Inhibitors* / therapeutic use
  • Lymphocytes, Tumor-Infiltrating* / drug effects
  • Lymphocytes, Tumor-Infiltrating* / immunology
  • Lymphocytes, Tumor-Infiltrating* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Receptors, Antigen, T-Cell, alpha-beta* / genetics
  • Receptors, Antigen, T-Cell, alpha-beta* / metabolism

Substances

  • Immune Checkpoint Inhibitors
  • Receptors, Antigen, T-Cell, alpha-beta

Grants and funding

The work was supported by the Cancer Council Western Australia, Department of Health, Government of Western Australia, National Health and Medical Research Council, Cancer Research Trust WA, UWA Raine Medical Research Foundation, Simon Lee Foundation, U.S. Department of Defense, and icare NSW Dust Diseases Board