Delayed resolution of lung inflammation in Il-1rn-/- mice reflects elevated IL-17A/granulocyte colony-stimulating factor expression

Am J Respir Cell Mol Biol. 2012 Oct;47(4):436-44. doi: 10.1165/rcmb.2012-0104OC. Epub 2012 May 16.

Abstract

IL-1 has been associated with acute lung injury (ALI) in both humans and animal models, but further investigation of the precise mechanisms involved is needed, and may identify novel therapeutic targets. To discover the IL-1 mediators essential to the initiation and resolution phases of acute lung inflammation, knockout mice (with targeted deletions for either the IL-1 receptor-1, i.e., Il-1r1(-/-), or the IL-1 receptor antagonist, i.e., Il-1rn(-/-)) were exposed to aerosolized LPS, and indices of lung and systemic inflammation were examined over the subsequent 48 hours. The resultant cell counts, histology, protein, and RNA expression of key cytokines were measured. Il-1r1(-/-) mice exhibited decreased neutrophil influx, particularly at 4 and 48 hours after exposure to LPS, as well as reduced bronchoalveolar lavage (BAL) expression of chemokines and granulocyte colony-stimulating factor (G-CSF). On the contrary, Il-1rn(-/-) mice demonstrated increased BAL neutrophil counts, increased BAL total protein, and greater evidence of histologic injury, all most notably 2 days after LPS exposure. Il-1rn(-/-) mice also exhibited higher peripheral neutrophil counts and greater numbers of granulocyte receptor-1 cells in their bone marrow, potentially reflecting their elevated plasma G-CSF concentrations. Furthermore, IL-17A expression was increased in the BAL and lungs of Il-1rn(-/-) mice after exposure to LPS, likely because of increased numbers of γδ T cells in the Il-1rn(-/-) lungs. Blockade with IL-17A monoclonal antibody before LPS exposure decreased the resultant BAL neutrophil counts and lung G-CSF expression in Il-1rn(-/-) mice, 48 hours after exposure to LPS. In conclusion, Il-1rn(-/-) mice exhibit delayed resolution in acute lung inflammation after exposure to LPS, a process that appears to be mediated via the G-CSF/IL-17A axis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Lung Injury / blood
  • Acute Lung Injury / immunology
  • Acute Lung Injury / metabolism
  • Analysis of Variance
  • Animals
  • Bone Marrow Cells / metabolism
  • Bone Marrow Cells / pathology
  • Bronchoalveolar Lavage Fluid / chemistry
  • Chemokines, CXC / metabolism
  • Gene Expression
  • Granulocyte Colony-Stimulating Factor / blood
  • Granulocyte Colony-Stimulating Factor / genetics
  • Granulocyte Colony-Stimulating Factor / metabolism*
  • Interleukin 1 Receptor Antagonist Protein / deficiency*
  • Interleukin 1 Receptor Antagonist Protein / genetics
  • Interleukin 1 Receptor Antagonist Protein / pharmacology
  • Interleukin-17 / genetics
  • Interleukin-17 / metabolism*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism
  • Leukocyte Count
  • Lipopolysaccharides / pharmacology
  • Lung / immunology
  • Lung / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Neutrophils / pathology
  • Pneumonia / blood
  • Pneumonia / immunology*
  • Pneumonia / metabolism
  • Receptors, Interleukin-1 Type I / deficiency
  • Receptors, Interleukin-1 Type I / genetics

Substances

  • Chemokines, CXC
  • Il17a protein, mouse
  • Il1rn protein, mouse
  • Interleukin 1 Receptor Antagonist Protein
  • Interleukin-17
  • Interleukin-1beta
  • Lipopolysaccharides
  • Receptors, Interleukin-1 Type I
  • Granulocyte Colony-Stimulating Factor