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

Monty Mazer, Jaqueline Unsinger, Anne Drewry, Andrew Walton, Dale Osborne, Theresa Blood, Richard Hotchkiss and Kenneth E. Remy
J Immunol September 9, 2019, ji1900637; DOI: https://doi.org/10.4049/jimmunol.1900637
Monty Mazer
*Division of Critical Care Medicine, Department of Pediatrics, School of Medicine, Washington University, St. Louis, MO 63110; and
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Jaqueline Unsinger
†Department of Anesthesiology, School of Medicine, Washington University, St. Louis, MO 63110
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Anne Drewry
†Department of Anesthesiology, School of Medicine, Washington University, St. Louis, MO 63110
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Andrew Walton
†Department of Anesthesiology, School of Medicine, Washington University, St. Louis, MO 63110
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Dale Osborne
†Department of Anesthesiology, School of Medicine, Washington University, St. Louis, MO 63110
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Theresa Blood
†Department of Anesthesiology, School of Medicine, Washington University, St. Louis, MO 63110
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Richard Hotchkiss
†Department of Anesthesiology, School of Medicine, Washington University, St. Louis, MO 63110
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Kenneth E. Remy
*Division of Critical Care Medicine, Department of Pediatrics, School of Medicine, Washington University, St. Louis, MO 63110; and
†Department of Anesthesiology, School of Medicine, Washington University, St. Louis, MO 63110
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Key Points

  • IL-10 inhibition increases T cell IFN-γ and monocyte TNF-α in septic patients.

  • rhIL-10 increases T cell production of IFN-γ in septic patient PBMCs.

  • rhIL-10 decreases monocyte TNF-α production and HLA-DR expression in sepsis.

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.

Footnotes

  • This work was supported by R35 (Maximizing Investigators' Research Award) GM126928-01 from the National Institute of General Medical Sciences (to R.H.).

  • The online version of this article contains supplemental material.

  • Received June 7, 2019.
  • Accepted August 14, 2019.
  • Copyright © 2019 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 206 (5)
The Journal of Immunology
Vol. 206, Issue 5
1 Mar 2021
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IL-10 Has Differential Effects on the Innate and Adaptive Immune Systems of Septic Patients
Monty Mazer, Jaqueline Unsinger, Anne Drewry, Andrew Walton, Dale Osborne, Theresa Blood, Richard Hotchkiss, Kenneth E. Remy
The Journal of Immunology September 9, 2019, ji1900637; DOI: 10.4049/jimmunol.1900637

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IL-10 Has Differential Effects on the Innate and Adaptive Immune Systems of Septic Patients
Monty Mazer, Jaqueline Unsinger, Anne Drewry, Andrew Walton, Dale Osborne, Theresa Blood, Richard Hotchkiss, Kenneth E. Remy
The Journal of Immunology September 9, 2019, ji1900637; DOI: 10.4049/jimmunol.1900637
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