The role of interleukin-10 in the regulation of the systemic inflammatory response following trauma-hemorrhage

Biochim Biophys Acta. 2004 May 24;1689(1):22-32. doi: 10.1016/j.bbadis.2004.01.003.

Abstract

Pro-inflammatory cytokine release after shock is central in the development of subsequent multiple organ dysfunction syndrome. Some studies suggest that interleukin-10 (IL-10) is an immunosuppressive mediator after injury or sepsis, while others suggest that IL-10 is an important regulator of the pro-inflammatory response. We hypothesized that in a model of trauma and hemorrhagic shock (TH), IL-10 regulates pro-inflammatory cytokine activity via an autocrine effect on cytokine mRNA transcription in Kupffer cells early after TH. To study this, male C3H/HeN mice were sham-operated or subjected to TH. Plasma levels of TNF-alpha, IL-6 and PGE(2) were elevated following TH. A sharp peak in IL-10 levels was observed at 2 h after the insult. Kupffer cell (KC) depletion prior to TH reduced plasma IL-6, IL-10 and TNF-alpha levels, whereas treatment with anti-IL-10 after TH increased IL-6 and TNF-alpha levels. Kupffer cell mRNA expression for IL-6, IL-10 and TNF-alpha was elevated in the TH group and further increased by anti-IL-10 treatment. These findings indicate that KC-dependent IL-10 regulates the early systemic inflammatory response after TH. Thus, while IL-10 is an important mediator of immunosuppression following traumatic injury, it also is beneficial with regard to its ability to counter-regulate the early inflammatory response under such conditions.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Cells, Cultured
  • DNA-Binding Proteins / metabolism
  • Gene Expression Regulation
  • Hemorrhage / blood*
  • Hemorrhage / complications
  • Hemorrhage / pathology*
  • Inflammation Mediators / blood*
  • Interleukin-10 / blood*
  • Interleukin-10 / immunology*
  • Interleukin-6 / blood
  • Interleukin-6 / genetics
  • Kupffer Cells / metabolism
  • Male
  • Mice
  • Mice, Inbred C3H
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, Interleukin / genetics
  • Receptors, Interleukin-10
  • Repressor Proteins / genetics
  • STAT3 Transcription Factor
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Trans-Activators / metabolism
  • Transcription Factors / genetics
  • Transcription, Genetic
  • Tumor Necrosis Factor-alpha / analysis
  • Tumor Necrosis Factor-alpha / genetics
  • Wounds and Injuries / blood*
  • Wounds and Injuries / complications
  • Wounds and Injuries / pathology*

Substances

  • DNA-Binding Proteins
  • Inflammation Mediators
  • Interleukin-6
  • RNA, Messenger
  • Receptors, Interleukin
  • Receptors, Interleukin-10
  • Repressor Proteins
  • STAT3 Transcription Factor
  • Socs3 protein, mouse
  • Stat3 protein, mouse
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Trans-Activators
  • Transcription Factors
  • Tumor Necrosis Factor-alpha
  • Interleukin-10