IL-1 regulates in vivo C-X-C chemokine induction and neutrophil sequestration following endotoxemia

J Endotoxin Res. 2002;8(1):59-67.

Abstract

The influx of neutrophils into tissues in response to inflammatory stimuli involves C-X-C chemokines. Interleukin-1 (IL-1) stimulates chemokine production in vitro, but its role in vivo on chemokine production is not as clearly understood. We hypothesized that IL-1 mediates in vivo tissue C-X-C chemokine production induced by systemic lipopolysaccharide (LPS). IL-1 activity was blocked by IL-1 receptor antagonist (IL-1Ra). Rats were injected with Salmonella typhi LPS (0.5 mg/kg) with and without prior administration of IL-1Ra. Cytokine-induced neutrophil chemoattractant-1 (CINC-1) and macrophage inflammatory protein-2 (MIP-2) protein and mRNA levels, tissue neutrophil accumulation, and indices of organ injury were measured. LPS administration resulted in increased plasma, lung, and liver IL-1beta that was decreased by Il-1Ra. LPS also induced an increase in plasma, lung, and liver CINC-1 and MIP-2 protein and mRNA. However, IL-1Ra had no effect on LPS-induced plasma or lung tissue CINC-1 levels. In contrast, IL-1Ra pretreatment did significantly decrease CINC-1 protein expression in the liver (45% decrease) and MIP-2 protein expression in plasma (100% decrease), lung (72% decrease) and liver (100% decrease) compared to LPS- treated controls. Steady-state mRNA levels by Northern blot analysis of both CINC-1 and MIP-2 in lung and liver were similar to the protein findings. Pretreatment with IL-1Ra also resulted in a 47% and 59% decrease in lung and liver neutrophil accumulation, respectively, following LPS. In addition, indices of both lung and liver injury were decreased in animals pretreated with IL-1Ra. In summary, LPS induces IL-1beta and MIP-2 expression in the lung and liver, both of which are IL-1 dependent. Although lung neutrophil accumulation in both lung and liver after LPS is also IL-1 mediated, lung CINC-1 levels were unaffected by IL-1Ra. These data suggest that IL-1 regulates tissue chemokine expression and neutrophil accumulation after LPS.

Publication types

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

MeSH terms

  • Animals
  • Chemokine CXCL1
  • Chemokine CXCL2
  • Chemokines, CXC / biosynthesis*
  • Chemokines, CXC / genetics
  • Chemotactic Factors / biosynthesis*
  • Chemotactic Factors / genetics
  • Disease Models, Animal
  • Endotoxemia / chemically induced
  • Endotoxemia / metabolism*
  • Growth Substances / biosynthesis*
  • Growth Substances / genetics
  • Humans
  • Intercellular Signaling Peptides and Proteins*
  • Interleukin 1 Receptor Antagonist Protein
  • Lipopolysaccharides / pharmacology
  • Liver / drug effects
  • Liver / metabolism
  • Lung / drug effects
  • Lung / metabolism
  • Male
  • Monokines / biosynthesis
  • Monokines / genetics
  • Neutrophil Infiltration / drug effects
  • Neutrophil Infiltration / physiology*
  • Neutrophils / drug effects
  • Neutrophils / enzymology
  • Peroxidase / metabolism
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Interleukin-1 / antagonists & inhibitors
  • Receptors, Interleukin-1 / metabolism*
  • Recombinant Proteins
  • Salmonella typhimurium / immunology
  • Sialoglycoproteins / pharmacology

Substances

  • CXCL1 protein, human
  • Chemokine CXCL1
  • Chemokine CXCL2
  • Chemokines, CXC
  • Chemotactic Factors
  • Cxcl1 protein, rat
  • Cxcl2 protein, rat
  • Growth Substances
  • IL1RN protein, human
  • Intercellular Signaling Peptides and Proteins
  • Interleukin 1 Receptor Antagonist Protein
  • Lipopolysaccharides
  • Monokines
  • RNA, Messenger
  • Receptors, Interleukin-1
  • Recombinant Proteins
  • Sialoglycoproteins
  • Peroxidase