Lack of PD-L1 expression by iNKT cells improves the course of influenza A infection

PLoS One. 2013;8(3):e59599. doi: 10.1371/journal.pone.0059599. Epub 2013 Mar 15.

Abstract

There is evidence indicating that invariant Natural Killer T (iNKT) cells play an important role in defense against influenza A virus (IAV). However, the effect of inhibitory receptor, programmed death-1 (PD-1), and its ligands, programmed death ligand (PD-L) 1 and 2 on iNKT cells in protection against IAV remains to be elucidated. Here we investigated the effects of these co-stimulatory molecules on iNKT cells in the response to influenza. We discovered that compare to the wild type, PD-L1 deficient mice show reduced sensitivity to IAV infection as evident by reduced weight loss, decreased pulmonary inflammation and cellular infiltration. In contrast, PD-L2 deficient mice showed augmented weight loss, pulmonary inflammation and cellular infiltration compare to the wild type mice after influenza infection. Adoptive transfer of iNKT cells from wild type, PD-L1 or PD-L2 deficient mice into iNKT cell deficient mice recapitulated these findings. Interestingly, in our transfer system PD-L1(-/-)-derived iNKT cells produced high levels of interferon-gamma whereas PD-L2(-/-)-derived iNKT cells produced high amounts of interleukin-4 and 13 suggesting a role for these cytokines in sensitivity to influenza. We identified that PD-L1 negatively regulates the frequency of iNKT cell subsets in the lungs of IAV infected mice. Altogether, these results demonstrate that lack of PD-L1 expression by iNKT cells reduces the sensitivity to IAV and that the presence of PD-L2 is important for dampening the deleterious inflammatory responses after IAV infection. Our findings potentially have clinical implications for developing new therapies for influenza.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B7-H1 Antigen / deficiency*
  • B7-H1 Antigen / genetics*
  • Cytokines / metabolism
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology
  • Dendritic Cells / virology
  • Female
  • Gene Expression Regulation / immunology*
  • Gene Knockout Techniques
  • Influenza A Virus, H1N1 Subtype / physiology*
  • Lung / immunology
  • Lung / metabolism
  • Lung / virology
  • Mice
  • Mice, Inbred BALB C
  • Natural Killer T-Cells / cytology
  • Natural Killer T-Cells / immunology
  • Natural Killer T-Cells / metabolism*
  • Natural Killer T-Cells / virology*
  • Orthomyxoviridae Infections / immunology*
  • Orthomyxoviridae Infections / metabolism
  • Programmed Cell Death 1 Ligand 2 Protein / deficiency
  • Programmed Cell Death 1 Ligand 2 Protein / genetics

Substances

  • B7-H1 Antigen
  • Cd274 protein, mouse
  • Cytokines
  • Pdcd1lg2 protein, mouse
  • Programmed Cell Death 1 Ligand 2 Protein