CD4 T cells promote rather than control tuberculosis in the absence of PD-1-mediated inhibition

J Immunol. 2011 Feb 1;186(3):1598-607. doi: 10.4049/jimmunol.1003304. Epub 2010 Dec 20.

Abstract

Although CD4 T cells are required for host resistance to Mycobacterium tuberculosis, they may also contribute to pathology. In this study, we examine the role of the inhibitory receptor PD-1 and its ligand PD-L1 during M. tuberculosis infection. After aerosol exposure, PD-1 knockout (KO) mice develop high numbers of M. tuberculosis-specific CD4 T cells but display markedly increased susceptibility to infection. Importantly, we show that CD4 T cells themselves drive the increased bacterial loads and pathology seen in infected PD-1 KO mice, and PD-1 deficiency in CD4 T cells is sufficient to trigger early mortality. PD-L1 KO mice also display enhanced albeit less severe susceptibility, indicating that T cells are regulated by multiple PD ligands during M. tuberculosis infection. M. tuberculosis-specific CD8 T cell responses were normal in PD-1 KO mice, and CD8 T cells only had a minor contribution to the exacerbated disease in the M. tuberculosis-infected PD-1 KO and PD-L1 KO mice. Thus, in the absence of the PD-1 pathway, M. tuberculosis benefits from CD4 T cell responses, and host resistance requires inhibition by PD-1 to prevent T cell-driven exacerbation of the infection.

Publication types

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

MeSH terms

  • Aerosols
  • Animals
  • Antigens, Surface / metabolism
  • Antigens, Surface / physiology*
  • Apoptosis Regulatory Proteins / deficiency*
  • Apoptosis Regulatory Proteins / metabolism
  • Apoptosis Regulatory Proteins / physiology*
  • B7-1 Antigen / metabolism
  • B7-1 Antigen / physiology
  • B7-H1 Antigen
  • CD4 Lymphocyte Count
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / microbiology*
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / pathology
  • Epitopes, T-Lymphocyte / genetics
  • Epitopes, T-Lymphocyte / immunology
  • Genetic Predisposition to Disease
  • Membrane Glycoproteins / metabolism
  • Membrane Glycoproteins / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Mycobacterium tuberculosis / growth & development
  • Mycobacterium tuberculosis / immunology*
  • Necrosis
  • Peptides / metabolism
  • Peptides / physiology
  • Programmed Cell Death 1 Receptor
  • Tuberculosis, Pulmonary / immunology*
  • Tuberculosis, Pulmonary / pathology*
  • Tuberculosis, Pulmonary / prevention & control

Substances

  • Aerosols
  • Antigens, Surface
  • Apoptosis Regulatory Proteins
  • B7-1 Antigen
  • B7-H1 Antigen
  • Cd274 protein, mouse
  • Epitopes, T-Lymphocyte
  • Membrane Glycoproteins
  • Pdcd1 protein, mouse
  • Peptides
  • Programmed Cell Death 1 Receptor