Programmed Death-1 antibody blocks therapeutic effects of T-regulatory cells in cockroach antigen-induced allergic asthma

Am J Respir Cell Mol Biol. 2010 Oct;43(4):432-42. doi: 10.1165/rcmb.2009-0258OC. Epub 2009 Nov 9.

Abstract

We recently reported that the adoptive transfer of T-regulatory cells (Tregs) isolated from lung and spleen tissue of green fluorescent protein-transgenic mice reversed airway hyperresponsiveness and airway inflammation. Because Programmed Death-1 (PD-1) is a pivotal receptor regulating effector T-cell activation by Tregs, we evaluated whether PD-1 is involved in the therapeutic effect of naturally occurring Tregs (NTregs) and inducible Tregs (iTregs) in cockroach (CRA)-sensitized and challenged mice. The CD4(+)CD25(+) NTregs and CD4(+)CD25(-) iTregs isolated from the lungs and spleens of BALB/c mice were adoptively transferred into CRA-sensitized and CRA-challenged mice with and without anti-PD-1 antibody (100 μg/mice). The CD4(+)CD25(+) T cells in the lung were phenotyped after adoptive transfer. Concentrations of IL-4, IL-5, IL-10, IFN-γ, and IL-13 in bronchoalveolar lavage fluid (BALF) were measured using ELISA. The NTregs and iTregs from either lung or spleen tissue reversed airway hyperresponsiveness for at least 4 wk. However, the therapeutic effect was blocked by administering the anti-PD-1 antibody. The administration of Tregs-recipient mice with anti-PD-1 antibody significantly decreased cytotoxic T-lymphocyte antigen-4 expression, with low concentrations of Forkhead-winged transcriptional factor box 3 (Foxp3) mRNA transcripts in lung CD4(+)CD25(+) T cells. These mice had substantially higher concentrations of BALF IL-4, IL-5, and IL-13, but significantly decreased levels of BALF IL-10. Adoptive therapy recipients without the anti-PD-1 antibody exhibited high levels of CTLA-4 expression and Foxp3 transcripts in lung CD4(+)CD25(+) T cells, with a significant decrease in BALF IL-4, IL-5, and IL-13 concentrations and a substantial increase in BALF IL-10 concentrations. These data suggest that the reversal of airway hyperresponsiveness and airway inflammation by Tregs is mediated in part by PD-1, because other costimulatory molecules (e.g., inducible costimulatory molecule [ICOS] or CTLA-4) have been shown to play a role in Treg-mediated suppression.

Publication types

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

MeSH terms

  • Adoptive Transfer
  • Allergens / immunology*
  • Animals
  • Antibodies / immunology*
  • Antibodies / pharmacology
  • Antigens, CD / metabolism
  • Antigens, Plant
  • Antigens, Surface / immunology*
  • Antigens, Surface / metabolism*
  • Apoptosis Regulatory Proteins / antagonists & inhibitors
  • Apoptosis Regulatory Proteins / immunology*
  • Apoptosis Regulatory Proteins / metabolism*
  • Asthma / immunology*
  • Asthma / pathology
  • Asthma / physiopathology
  • Bronchial Hyperreactivity / complications
  • Bronchial Hyperreactivity / immunology
  • Bronchial Hyperreactivity / pathology
  • Bronchoalveolar Lavage Fluid / cytology
  • CD4 Antigens / metabolism
  • CTLA-4 Antigen
  • Cell Separation
  • Cockroaches / immunology*
  • Cytokines / metabolism
  • Female
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / metabolism
  • Gene Expression Regulation
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Lung / immunology
  • Lung / pathology
  • Mice
  • Mice, Inbred BALB C
  • Programmed Cell Death 1 Receptor
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology*

Substances

  • Allergens
  • Antibodies
  • Antigens, CD
  • Antigens, Plant
  • Antigens, Surface
  • Apoptosis Regulatory Proteins
  • CD4 Antigens
  • CTLA-4 Antigen
  • Ctla4 protein, mouse
  • Cytokines
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Interleukin-2 Receptor alpha Subunit
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • allergen CRa, cockroach