Targeting inducible costimulator expressed on CXCR5+PD-1+ TH cells suppresses the progression of pemphigus vulgaris

J Allergy Clin Immunol. 2020 Nov;146(5):1070-1079.e8. doi: 10.1016/j.jaci.2020.03.036. Epub 2020 Apr 18.

Abstract

Background: Pemphigus vulgaris (PV) is an autoimmune bullous disease mediated by autoantibodies against desmoglein 3 (DSG3). Inducible costimulator (ICOS) is a costimulatory receptor expressed on T cells and influences the activity of T follicular helper (TFH) cells in various autoimmune diseases, but the roles of ICOS and TFH cells in PV remain unclear.

Objective: We examined the immunological characteristics, antigen specificity, and pathogenicity of CD4+ T-cell subpopulations, as well as the therapeutic effect of anti-ICOS blocking antibodies in PV.

Methods: A mouse model of PV was established by adoptive transfer of immune cells from the skin-draining lymph nodes or spleens of DSG3-expressing skin-grafted Dsg3-/- mice into Rag1-/- mice. The TFH cells and CD4+ T cells in PBMCs from PV patients were examined by flow cytometry.

Results: Among CD4+ T cells from the mouse model, ICOS-positive TFH cells were associated with B-cell differentiation and were required for disease induction. Using an MHC class II tetramer, DSG3-specific ICOS+ TFH cells were found to be associated with anti-DSG3 antibody production and expanded in the absence of B cells. In human PV, the frequency of ICOS+CXCR5+PD-1+ memory CD4+ T cells correlated with the autoantibody level. Treatment with anti-ICOS blocking antibodies targeting ICOS+ TFH cells decreased the anti-DSG3 antibody level and delayed disease progression in vivo.

Conclusions: Mouse Dsg3-specific ICOS+ TFH cells and human ICOS+CXCR5+PD-1+ TH cells are associated with the anti-DSG3 antibody response in PV. ICOS expressed on CXCR5+PD-1+ TH cells may be a therapeutic target for PV.

Keywords: T follicular helper cell; desmoglein; humoral immunity; inducible costimulator; pemphigus vulgaris.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / therapeutic use*
  • Antibodies, Blocking / therapeutic use*
  • Autoantibodies / metabolism
  • Desmoglein 3 / genetics
  • Desmoglein 3 / metabolism*
  • Disease Models, Animal
  • Disease Progression
  • Flow Cytometry
  • Germinal Center / immunology*
  • Humans
  • Immunologic Memory
  • Inducible T-Cell Co-Stimulator Protein / immunology
  • Inducible T-Cell Co-Stimulator Protein / metabolism*
  • Mice
  • Mice, Knockout
  • Pemphigus / immunology
  • Pemphigus / therapy*
  • Programmed Cell Death 1 Receptor / metabolism
  • Receptors, CXCR5 / metabolism
  • Th1 Cells / immunology
  • Th1 Cells / metabolism*

Substances

  • Anti-Inflammatory Agents
  • Antibodies, Blocking
  • Autoantibodies
  • CXCR5 protein, mouse
  • Desmoglein 3
  • Dsg3 protein, mouse
  • Icos protein, mouse
  • Inducible T-Cell Co-Stimulator Protein
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • Receptors, CXCR5