IL-10 Has Differential Effects on the Innate and Adaptive Immune Systems of Septic Patients

J Immunol. 2019 Oct 15;203(8):2088-2099. doi: 10.4049/jimmunol.1900637. Epub 2019 Sep 9.

Abstract

Sepsis, a disease of divergent pro- and anti-inflammatory-mediated pathways, has a high prevalence of morbidity and mortality, yet an understanding of potential unifying mediators between these pathways that may improve clinical outcomes is largely unclear. IL-10 has classically been designated an immunosuppressive cytokine, although recent data suggest that under certain conditions IL-10 can be immune stimulatory. We sought to further investigate the effect of IL-10 on innate and adaptive immunity in an in vitro human observational cohort study in patients with sepsis via modulation of IL-10 on IFN-γ production by T cells and TNF-α production and HLA-DR expression by monocytes. These results were compared with critically ill nonseptic patients and healthy volunteers. ELISpot analysis was performed using PBMC fraction from patient whole-blood samples. Finally, to provide additional potential clinical relevance, we examined the effect of IL-10 on T cell IFN-γ production in an in vivo cecal ligation and puncture model of sepsis using C57 black/J6 female mice. We found that inhibition of IL-10 significantly increased both production of T cell IFN-γ and monocyte TNF-α, whereas addition of IL-10 increased T cell IFN-γ production but decreased monocyte production of TNF-α and HLA-DR expression. There was no significant effect of IL-10 on control cohorts. IL-10-treated septic mice demonstrated increased IFN-γ production in splenocytes. Thus, IL-10 demonstrates both pro- and anti-inflammatory effects in the septic microenvironment, which is likely cell and context dependent. Further elucidation of relevant signaling pathways may direct future therapeutic targets.

Publication types

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

MeSH terms

  • Adaptive Immunity / immunology
  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Cohort Studies
  • Disease Models, Animal
  • Female
  • Humans
  • Interferon-gamma / biosynthesis
  • Interleukin-10 / antagonists & inhibitors
  • Interleukin-10 / blood
  • Interleukin-10 / immunology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Prospective Studies
  • Sepsis / immunology*
  • Young Adult

Substances

  • IL10 protein, human
  • Interleukin-10
  • Interferon-gamma