Inhibiting the programmed death 1 pathway rescues Mycobacterium tuberculosis-specific interferon γ-producing T cells from apoptosis in patients with pulmonary tuberculosis

J Infect Dis. 2013 Aug 15;208(4):603-15. doi: 10.1093/infdis/jit206. Epub 2013 May 9.

Abstract

Background: Overexpression of programmed death 1 (PD-1) receptor is thought to inhibit the effector T-cell response in human tuberculosis. However, the precise mechanism of such inhibition remains unclear. The present study addresses the role of PD-1 in dampening host T-cell function among patients with pulmonary tuberculosis.

Methods: Expression of PD-1 and its ligands (PD-L1/L2) on T cells, B cells, and monocytes was evaluated by flow cytometry (FACS). In vitro stimulation of peripheral blood mononuclear cells in the presence of Mycobacterium tuberculosis antigens was performed with and without blocking PD-1, and intracellular cytokine production was measured by FACS.

Results: We showed higher frequencies of T cells, monocytes, and B cells expressing PD-1 and its ligand(s) among patients with pulmonary tuberculosis. Infections with live M. tuberculosis upregulated PD-L1 expression on monocytes. In vitro PD-1 blocking rescued M. tuberculosis-specific interferon γ (IFN-γ)-producing T cells from undergoing apoptosis. The number of PD-1-expressing T cells decreased significantly during therapy and inversely correlated with IFN-γ-dominant T-cell response against M. tuberculosis.

Conclusions: Manipulation of PD-1 signaling may restore the host T-cell response and thus may have therapeutic potential. PD-1 also may serve as a biomarker to monitor host immunity among patients with tuberculosis during therapy and vaccine studies.

Keywords: APCs and apoptosis; T cells; Tuberculosis; programmed death-1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Apoptosis*
  • B-Lymphocytes / chemistry
  • B-Lymphocytes / immunology
  • Cytokines / biosynthesis
  • Female
  • Flow Cytometry
  • Humans
  • Interferon-gamma / metabolism*
  • Male
  • Middle Aged
  • Monocytes / chemistry
  • Monocytes / immunology
  • Mycobacterium tuberculosis / immunology*
  • Programmed Cell Death 1 Receptor / analysis
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor / immunology*
  • T-Lymphocytes / chemistry
  • T-Lymphocytes / immunology*
  • Tuberculosis, Pulmonary / immunology*
  • Young Adult

Substances

  • Cytokines
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor
  • Interferon-gamma