Nasal anti-CD3 antibody ameliorates lupus by inducing an IL-10-secreting CD4+ CD25- LAP+ regulatory T cell and is associated with down-regulation of IL-17+ CD4+ ICOS+ CXCR5+ follicular helper T cells

J Immunol. 2008 Nov 1;181(9):6038-50. doi: 10.4049/jimmunol.181.9.6038.

Abstract

Lupus is an Ab-mediated autoimmune disease. One of the potential contributors to the development of systemic lupus erythematosus is a defect in naturally occurring CD4(+)CD25(+) regulatory T cells. Thus, the generation of inducible regulatory T cells that can control autoantibody responses is a potential avenue for the treatment of systemic lupus erythematosus. We have found that nasal administration of anti-CD3 mAb attenuated lupus development as well as arrested ongoing lupus in two strains of lupus-prone mice. Nasal anti-CD3 induced a CD4(+)CD25(-)latency-associated peptide (LAP)(+) regulatory T cell that secreted high levels of IL-10 and suppressed disease in vivo via IL-10- and TFG-beta-dependent mechanisms. Disease suppression also occurred following adoptive transfer of CD4(+)CD25(-)LAP(+) regulatory T cells from nasal anti-CD3-treated animals to lupus-prone mice. Animals treated with nasal anti-CD3 had less glomerulonephritis and diminished levels of autoantibodies as measured by both ELISA and autoantigen microarrays. Nasal anti-CD3 affected the function of CD4(+)ICOS(+)CXCR5(+) follicular helper T cells that are required for autoantibody production. CD4(+)ICOS(+)CXCR5(+) follicular helper T cells express high levels of IL-17 and IL-21 and these cytokines were down-regulated by nasal anti-CD3. Our results demonstrate that nasal anti-CD3 induces CD4(+)CD25(-)LAP(+) regulatory T cells that suppress lupus in mice and that it is associated with down-regulation of T cell help for autoantibody production.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antibodies, Monoclonal / administration & dosage*
  • Antibodies, Monoclonal / therapeutic use
  • Antigens, Differentiation, T-Lymphocyte / biosynthesis
  • Antigens, Differentiation, T-Lymphocyte / metabolism
  • CD3 Complex / immunology*
  • CD4 Antigens / biosynthesis
  • Cells, Cultured
  • Down-Regulation / immunology*
  • Female
  • Germinal Center / cytology
  • Germinal Center / immunology
  • Germinal Center / metabolism
  • Growth Inhibitors / administration & dosage*
  • Growth Inhibitors / therapeutic use
  • Inducible T-Cell Co-Stimulator Protein
  • Interleukin-10 / metabolism*
  • Interleukin-17 / antagonists & inhibitors
  • Interleukin-17 / biosynthesis
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Latent TGF-beta Binding Proteins / biosynthesis
  • Lupus Erythematosus, Systemic / genetics
  • Lupus Erythematosus, Systemic / immunology*
  • Lupus Erythematosus, Systemic / prevention & control
  • Male
  • Mice
  • Mice, Inbred NZB
  • Nasal Mucosa / immunology*
  • Receptors, CXCR5 / antagonists & inhibitors
  • Receptors, CXCR5 / biosynthesis
  • T-Lymphocytes, Helper-Inducer / cytology
  • T-Lymphocytes, Helper-Inducer / immunology*
  • T-Lymphocytes, Helper-Inducer / metabolism
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Antibodies, Monoclonal
  • Antigens, Differentiation, T-Lymphocyte
  • CD3 Complex
  • CD4 Antigens
  • CXCR5 protein, mouse
  • Growth Inhibitors
  • Icos protein, mouse
  • Inducible T-Cell Co-Stimulator Protein
  • Interleukin-17
  • Interleukin-2 Receptor alpha Subunit
  • Latent TGF-beta Binding Proteins
  • Receptors, CXCR5
  • Interleukin-10