CTLA4Ig inhibits effector T cells through regulatory T cells and TGF-β

J Immunol. 2013 Sep 15;191(6):3082-9. doi: 10.4049/jimmunol.1300830. Epub 2013 Aug 16.

Abstract

The CD28 costimulatory receptor is a critical regulator of T cell function, making it an attractive therapeutic target for the treatment of immune-mediated diseases. CTLA4Ig, now approved for use in humans, prevents naive T cell activation by binding to B7 proteins and blocking engagement of CD28. However, CTLA4Ig suppresses inflammation even if administered when disease is established, suggesting alternative mechanisms. We identified a novel, CD28-independent mechanism by which CTLA4Ig inhibits activated T cells. We show that in vitro, CTLA4Ig synergizes with NO from bone marrow-derived macrophages to inhibit T cell proliferation. Depletion of regulatory T cells (Tregs) or interference with TGF-β signaling abrogated the inhibitory effect of CTLA4Ig. Parallel in vivo experiments using an allergic airway inflammation model demonstrated that this novel mechanism required both macrophages and regulatory T cells. Furthermore, CTLA4Ig was ineffective in SMAD3-deficient mice, supporting a requirement for TGF-β signaling. Thus, in addition to preventing naive T cells from being fully activated, CTLA4Ig can turn off already activated effector T cells by an NO/regulatory T cell/TGF-β-dependent pathway. This mechanism is similar to cell-extrinsic effects of endogenous CTLA4 and may be particularly important in the ability of CTLA4Ig to treat chronic inflammatory disease.

Publication types

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

MeSH terms

  • Adoptive Transfer
  • Animals
  • Anti-Inflammatory Agents / pharmacology*
  • CTLA-4 Antigen / immunology*
  • Coculture Techniques
  • Disease Models, Animal
  • Flow Cytometry
  • Immunoconjugates / pharmacology
  • Immunoglobulin G / pharmacology*
  • Lymphocyte Activation / drug effects*
  • Lymphocyte Activation / immunology
  • Macrophages
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Recombinant Fusion Proteins / pharmacology
  • Respiratory Hypersensitivity / immunology
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology*
  • Transforming Growth Factor beta / immunology*

Substances

  • Anti-Inflammatory Agents
  • CTLA-4 Antigen
  • Ctla4 protein, mouse
  • Immunoconjugates
  • Immunoglobulin G
  • Recombinant Fusion Proteins
  • Transforming Growth Factor beta