Multi-omic profiling reveals the endogenous and neoplastic responses to immunotherapies in cutaneous T cell lymphoma

Cell Rep Med. 2024 May 21;5(5):101527. doi: 10.1016/j.xcrm.2024.101527. Epub 2024 Apr 25.

Abstract

Cutaneous T cell lymphomas (CTCLs) are skin cancers with poor survival rates and limited treatments. While immunotherapies have shown some efficacy, the immunological consequences of administering immune-activating agents to CTCL patients have not been systematically characterized. We apply a suite of high-dimensional technologies to investigate the local, cellular, and systemic responses in CTCL patients receiving either mono- or combination anti-PD-1 plus interferon-gamma (IFN-γ) therapy. Neoplastic T cells display no evidence of activation after immunotherapy. IFN-γ induces muted endogenous immunological responses, while anti-PD-1 elicits broader changes, including increased abundance of CLA+CD39+ T cells. We develop an unbiased multi-omic profiling approach enabling discovery of immune modules stratifying patients. We identify an enrichment of activated regulatory CLA+CD39+ T cells in non-responders and activated cytotoxic CLA+CD39+ T cells in leukemic patients. Our results provide insights into the effects of immunotherapy in CTCL patients and a generalizable framework for multi-omic analysis of clinical trials.

Keywords: checkpoint blockade; cutaneous T cell lymphoma; human immunology; immunotherapy; multi-omics; single cell; systems biology.

MeSH terms

  • Female
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Immunotherapy* / methods
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Lymphoma, T-Cell, Cutaneous* / immunology
  • Lymphoma, T-Cell, Cutaneous* / pathology
  • Lymphoma, T-Cell, Cutaneous* / therapy
  • Male
  • Multiomics
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor / immunology
  • Programmed Cell Death 1 Receptor / metabolism
  • Skin Neoplasms / drug therapy
  • Skin Neoplasms / immunology
  • Skin Neoplasms / pathology
  • Skin Neoplasms / therapy

Substances

  • Interferon-gamma
  • Programmed Cell Death 1 Receptor
  • Immune Checkpoint Inhibitors