Spatiotemporal single-cell analysis decodes cellular dynamics underlying different responses to immunotherapy in colorectal cancer

Cancer Cell. 2024 Jul 8;42(7):1268-1285.e7. doi: 10.1016/j.ccell.2024.06.009.

Abstract

Expanding the efficacy of immune checkpoint blockade (ICB) in colorectal cancer (CRC) presses for a comprehensive understanding of treatment responsiveness. Here, we analyze multiple sequential single-cell samples from 22 patients undergoing PD-1 blockade to map the evolution of local and systemic immunity of CRC patients. In tumors, we identify coordinated cellular programs exhibiting distinct response associations. Specifically, exhausted T (Tex) or tumor-reactive-like CD8+ T (Ttr-like) cells are closely related to treatment efficacy, and Tex cells show correlated proportion changes with multiple other tumor-enriched cell types following PD-1 blockade. In addition, we reveal the less-exhausted phenotype of blood-associated Ttr-like cells in tumors and find that their higher abundance suggests better treatment outcomes. Finally, a higher major histocompatibility complex (MHC) II-related signature in circulating CD8+ T cells at baseline is linked to superior responses. Our study provides insights into the spatiotemporal cellular dynamics following neoadjuvant PD-1 blockade in CRC.

Keywords: eoadjuvant immunotherapy; sequential multi-model single-cell sequencing; systemic immunity.

MeSH terms

  • CD8-Positive T-Lymphocytes* / immunology
  • Colorectal Neoplasms* / drug therapy
  • Colorectal Neoplasms* / immunology
  • Colorectal Neoplasms* / pathology
  • Colorectal Neoplasms* / therapy
  • Female
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Immunotherapy* / methods
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Male
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor / immunology
  • Single-Cell Analysis* / methods

Substances

  • Immune Checkpoint Inhibitors
  • Programmed Cell Death 1 Receptor