PD-1 suppresses human CD38+ circulating Tfr cells and regulates humoral immunity

J Immunother Cancer. 2025 Jan 11;13(1):e010026. doi: 10.1136/jitc-2024-010026.

Abstract

Background: Anti-programmed cell death protein 1 (anti-PD-1) antibodies have achieved revolutionary success in cancer therapy. However, the impact of anti-PD-1 therapy on host humoral immunity in humans during cancer immunotherapy requires further investigation.

Methods: We evaluated immunoglobulin titers by ELISA and screened the immune landscape of immune cells from 25 healthy donors and 50 cases including 25 new-onset hepatocellular carcinoma (HCC) patients prior to systemic treatment and 25 HCC patients undergoing anti-PD-1 therapy by multicolor flow cytometry. Flow or beads sorted cells were cultured ex vivo for proliferation and functional analysis.

Results: Anti-PD-1 therapy significantly increased the levels of IgG and IgA in the periphery of HCC patients. Anti-PD-1 treatment led to an increase in plasmablasts and a notable rise in circulating T follicular regulatory (cTfr) cells, while changes in circulating B cells, T follicular helper cells, or regulatory T cells were not significant. Anti-PD-1 therapy also influenced the proliferation and function of cTfr cells, promoting the differentiation of CD38+ cTfr cells. We observed that the CD38+ Tfr cell subset in the peripheral blood can promote plasmablast differentiation, associated with altered antibody production.

Conclusions: Together, these data demonstrate the immunomodulatory role of PD-1 in restricting the differentiation and function of human cTfr cells and in regulating humoral immunity.

Keywords: Humoral; Immune Checkpoint Inhibitor; T regulatory cell - Treg.

MeSH terms

  • ADP-ribosyl Cyclase 1* / metabolism
  • Adult
  • Aged
  • Carcinoma, Hepatocellular / drug therapy
  • Carcinoma, Hepatocellular / immunology
  • Carcinoma, Hepatocellular / pathology
  • Female
  • Humans
  • Immunity, Humoral*
  • Liver Neoplasms / drug therapy
  • Liver Neoplasms / immunology
  • Male
  • Membrane Glycoproteins / metabolism
  • Middle Aged
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor* / metabolism

Substances

  • Programmed Cell Death 1 Receptor
  • ADP-ribosyl Cyclase 1
  • PDCD1 protein, human
  • CD38 protein, human
  • Membrane Glycoproteins