Post-sepsis immunosuppression depends on NKT cell regulation of mTOR/IFN-γ in NK cells

J Clin Invest. 2020 Jun 1;130(6):3238-3252. doi: 10.1172/JCI128075.

Abstract

As treatment of the early, inflammatory phase of sepsis improves, post-sepsis immunosuppression and secondary infection have increased in importance. How early inflammation drives immunosuppression remains unclear. Although IFN-γ typically helps microbial clearance, we found that increased plasma IFN-γ in early clinical sepsis was associated with the later development of secondary Candida infection. Consistent with this observation, we found that exogenous IFN-γ suppressed macrophage phagocytosis of zymosan in vivo, and antibody blockade of IFN-γ after endotoxemia improved survival of secondary candidemia. Transcriptomic analysis of innate lymphocytes during endotoxemia suggested that NKT cells drove IFN-γ production by NK cells via mTORC1. Activation of invariant NKT (iNKT) cells with glycolipid antigen drove immunosuppression. Deletion of iNKT cells in Cd1d-/- mice or inhibition of mTOR by rapamycin reduced immunosuppression and susceptibility to secondary Candida infection. Thus, although rapamycin is typically an immunosuppressive medication, in the context of sepsis, rapamycin has the opposite effect. These results implicated an NKT cell/mTOR/IFN-γ axis in immunosuppression following endotoxemia or sepsis. In summary, in vivo iNKT cells activated mTORC1 in NK cells to produce IFN-γ, which worsened macrophage phagocytosis, clearance of secondary Candida infection, and mortality.

Keywords: Fungal infections; Immunology; Infectious disease; Macrophages; NK T cells.

Publication types

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

MeSH terms

  • Animals
  • Antigens, CD1d / genetics
  • Antigens, CD1d / immunology
  • Candida / immunology
  • Candidiasis / genetics
  • Candidiasis / immunology
  • Candidiasis / pathology
  • Female
  • Humans
  • Immune Tolerance*
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology*
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / pathology
  • Male
  • Mice
  • Mice, Knockout
  • Natural Killer T-Cells / immunology*
  • Natural Killer T-Cells / pathology
  • Sepsis / genetics
  • Sepsis / immunology*
  • Sepsis / pathology
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • TOR Serine-Threonine Kinases / genetics
  • TOR Serine-Threonine Kinases / immunology*

Substances

  • Antigens, CD1d
  • CD1d antigen, mouse
  • IFNG protein, mouse
  • Interferon-gamma
  • mTOR protein, mouse
  • TOR Serine-Threonine Kinases