PD-1 suppresses protective immunity to Streptococcus pneumoniae through a B cell-intrinsic mechanism

J Immunol. 2015 Mar 1;194(5):2289-99. doi: 10.4049/jimmunol.1401673. Epub 2015 Jan 26.

Abstract

Despite the emergence of the programmed cell death 1 (PD-1):PD-1 ligand (PD-L) regulatory axis as a promising target for treating multiple human diseases, remarkably little is known about how this pathway regulates responses to extracellular bacterial infections. We found that PD-1(-/-) mice, as well as wild-type mice treated with a PD-1 blocking Ab, exhibited significantly increased survival against lethal Streptococcus pneumoniae infection following either priming with low-dose pneumococcal respiratory infection or S. pneumoniae-capsular polysaccharide immunization. Enhanced survival in mice with disrupted PD-1:PD-L interactions was explained by significantly increased proliferation, isotype switching, and IgG production by pneumococcal capsule-specific B cells. Both PD-L, B7-H1 and B7-DC, contributed to PD-1-mediated suppression of protective capsule-specific IgG. Importantly, PD-1 was induced on capsule-specific B cells and suppressed IgG production and protection against pneumococcal infection in a B cell-intrinsic manner. To our knowledge, these results provide the first demonstration of a physiologic role for B cell-intrinsic PD-1 expression in vivo. In summary, our study reveals that B cell-expressed PD-1 plays a central role in regulating protection against S. pneumoniae, and thereby represents a promising target for bolstering immunity to encapsulated bacteria.

Publication types

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

MeSH terms

  • Animals
  • Antibodies, Bacterial / biosynthesis*
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / microbiology
  • B7-H1 Antigen / genetics
  • B7-H1 Antigen / immunology*
  • Gene Expression Regulation
  • Immunity, Humoral / drug effects
  • Immunization
  • Immunoglobulin G / biosynthesis
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Pneumococcal Infections / genetics
  • Pneumococcal Infections / immunology
  • Pneumococcal Infections / mortality
  • Pneumococcal Infections / prevention & control*
  • Pneumococcal Vaccines / administration & dosage*
  • Polysaccharides, Bacterial / administration & dosage
  • Programmed Cell Death 1 Ligand 2 Protein / genetics
  • Programmed Cell Death 1 Ligand 2 Protein / immunology
  • Programmed Cell Death 1 Receptor / deficiency
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / immunology*
  • Signal Transduction
  • Streptococcus pneumoniae / immunology
  • Survival Analysis

Substances

  • Antibodies, Bacterial
  • B7-H1 Antigen
  • Cd274 protein, mouse
  • Immunoglobulin G
  • Pdcd1 protein, mouse
  • Pneumococcal Vaccines
  • Polysaccharides, Bacterial
  • Programmed Cell Death 1 Ligand 2 Protein
  • Programmed Cell Death 1 Receptor