PD-1 Deficiency Promotes Macrophage Activation and T-Helper Cell Type 1/T-Helper Cell Type 17 Response in Pneumocystis Pneumonia

Am J Respir Cell Mol Biol. 2020 Jun;62(6):767-782. doi: 10.1165/rcmb.2019-0234OC.

Abstract

Pneumocystis is an unusual, opportunistic fungal pathogen capable of causing Pneumocystis pneumonia (PCP) in immunocompromised hosts. Although PCP was discovered >100 years ago, its pathogenesis remains unclear. The inhibitory receptor PD-1 (programmed death 1), a negative regulator of activated T cells, has been reported to take part in tumor escape, immune tolerance, and infection immunity. In this study, we examined the role of the PD-1/PD-L1 (programmed death-ligand 1) pathway in patients with PCP and in mice. The expression levels of PD-1/PD-L1 in patients with PCP and in mice were measured by real-time PCR and flow cytometry. The effects of PD-1 deficiency are demonstrated using wild-type and PD-1-/- mice. Our data show that Pneumocystis infection promotes PD-1/PD-L1 expression; PD-1 deficiency enhances the phagocytic function of macrophages and the pulmonary T-helper cell type 1 (Th1)/Th17 response, which might contribute to Pneumocystis clearance; and PD-1 deficiency affects the polarization of macrophages. PCP mice treated with anti-PD-1 antibody showed improved pulmonary clearance of Pneumocystis. Collectively, our results demonstrate that the PD-1/PD-L1 pathway plays a role in regulating the innate and adaptive immune responses, suggesting that manipulation of this pathway may constitute an immunotherapeutic strategy for PCP.

Keywords: PD-1; Pneumocystis; T cell; macrophage; pneumonia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptive Immunity
  • Adult
  • Aged
  • Animals
  • Antibodies, Fungal / blood
  • B7-H1 Antigen / biosynthesis
  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / physiology*
  • Female
  • Humans
  • Immunity, Innate
  • Immunocompromised Host
  • Immunotherapy
  • Lung / immunology
  • Lung / metabolism
  • Lung / microbiology
  • Macrophage Activation / physiology*
  • Macrophages / microbiology
  • Male
  • Mice
  • Mice, Knockout
  • Middle Aged
  • Nitric Oxide / metabolism
  • Opportunistic Infections / immunology
  • Pneumocystis / immunology
  • Pneumonia, Pneumocystis / genetics
  • Pneumonia, Pneumocystis / immunology*
  • Programmed Cell Death 1 Receptor / biosynthesis
  • Programmed Cell Death 1 Receptor / deficiency*
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / physiology
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction
  • Th1 Cells / immunology*
  • Th17 Cells / immunology*

Substances

  • Antibodies, Fungal
  • B7-H1 Antigen
  • CD274 protein, human
  • Cd274 protein, mouse
  • PDCD1 protein, human
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • Nitric Oxide