IL-6 trans-signaling promotes pancreatitis-associated lung injury and lethality

J Clin Invest. 2013 Mar;123(3):1019-31. doi: 10.1172/JCI64931. Epub 2013 Feb 15.

Abstract

Acute lung injury (ALI) is an inflammatory disease with a high mortality rate. Although typically seen in individuals with sepsis, ALI is also a major complication in severe acute pancreatitis (SAP). The pathophysiology of SAP-associated ALI is poorly understood, but elevated serum levels of IL-6 is a reliable marker for disease severity. Here, we used a mouse model of acute pancreatitis-associated (AP-associated) ALI to determine the role of IL-6 in ALI lethality. Il6-deficient mice had a lower death rate compared with wild-type mice with AP, while mice injected with IL-6 were more likely to develop lethal ALI. We found that inflammation-associated NF-κB induced myeloid cell secretion of IL-6, and the effects of secreted IL-6 were mediated by complexation with soluble IL-6 receptor, a process known as trans-signaling. IL-6 trans-signaling stimulated phosphorylation of STAT3 and production of the neutrophil attractant CXCL1 in pancreatic acinar cells. Examination of human samples revealed expression of IL-6 in combination with soluble IL-6 receptor was a reliable predictor of ALI in SAP. These results demonstrate that IL-6 trans-signaling is an essential mediator of ALI in SAP across species and suggest that therapeutic inhibition of IL-6 may prevent SAP-associated ALI.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acinar Cells / metabolism
  • Acute Lung Injury / etiology*
  • Acute Lung Injury / immunology
  • Acute Lung Injury / metabolism
  • Acute Lung Injury / pathology
  • Aminosalicylic Acids / pharmacology
  • Animals
  • Benzenesulfonates / pharmacology
  • Chemokine CXCL1 / metabolism
  • Humans
  • Interleukin-6 / metabolism
  • Interleukin-6 / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Myeloid Cells / metabolism
  • NF-kappa B / metabolism
  • Pancreas / pathology
  • Pancreatitis / complications*
  • Pancreatitis / immunology
  • Pancreatitis / metabolism
  • Pancreatitis / pathology
  • Phenylurea Compounds / pharmacology
  • Phosphorylation
  • Protein Processing, Post-Translational
  • Receptors, Interleukin-6 / metabolism
  • Receptors, Interleukin-8B / antagonists & inhibitors
  • Receptors, Interleukin-8B / metabolism
  • STAT3 Transcription Factor / antagonists & inhibitors
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction

Substances

  • Aminosalicylic Acids
  • Benzenesulfonates
  • Chemokine CXCL1
  • Cxcl1 protein, mouse
  • Interleukin-6
  • NF-kappa B
  • NSC 74859
  • Phenylurea Compounds
  • Receptors, Interleukin-6
  • Receptors, Interleukin-8B
  • SB 225002
  • STAT3 Transcription Factor
  • Stat3 protein, mouse
  • interleukin-6, mouse