Interleukin-2 immunotherapy reveals human regulatory T cell subsets with distinct functional and tissue-homing characteristics

Immunity. 2024 Sep 10;57(9):2232-2250.e10. doi: 10.1016/j.immuni.2024.07.016. Epub 2024 Aug 12.

Abstract

Due to its stimulatory potential for immunomodulatory CD4+ regulatory T (Treg) cells, low-dose interleukin-2 (IL-2) immunotherapy has gained considerable attention for the treatment of autoimmune diseases. In this investigator-initiated single-arm non-placebo-controlled phase-2 clinical trial of low-dose IL-2 immunotherapy in systemic lupus erythematosus (SLE) patients, we generated a comprehensive atlas of in vivo human immune responses to low-dose IL-2. We performed an in-depth study of circulating and cutaneous immune cells by imaging mass cytometry, high-parameter flow cytometry, transcriptomics, and targeted serum proteomics. Low-dose IL-2 stimulated various circulating immune cells, including Treg cells with a skin-homing phenotype that appeared in the skin of SLE patients in close interaction with endothelial cells. Analysis of surface proteins and transcriptomes revealed different IL-2-driven Treg cell activation programs, including gut-homing CD38+, skin-homing HLA-DR+, and highly proliferative inflammation-homing CD38+ HLA-DR+ Treg cells. Collectively, these data define the distinct human Treg cell subsets that are responsive to IL-2 immunotherapy.

Keywords: IL-2; SLE; Treg; clinical trial; epigenomics; imaging mass cytometry; interleukin-2; lupus; regulatory T cell; transcriptomics.

Publication types

  • Clinical Trial, Phase II

MeSH terms

  • Adult
  • Female
  • Humans
  • Immunotherapy* / methods
  • Interleukin-2* / immunology
  • Lupus Erythematosus, Systemic* / immunology
  • Lupus Erythematosus, Systemic* / therapy
  • Lymphocyte Activation / immunology
  • Male
  • Skin* / immunology
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • T-Lymphocytes, Regulatory* / immunology

Substances

  • Interleukin-2