Overexpression of sICAM-1 in the alveolar epithelial space results in an exaggerated inflammatory response and early death in Gram negative pneumonia

Respir Res. 2011 Jan 19;12(1):12. doi: 10.1186/1465-9921-12-12.

Abstract

Background: A sizeable body of data demonstrates that membrane ICAM-1 (mICAM-1) plays a significant role in host defense in a site-specific fashion. On the pulmonary vascular endothelium, mICAM-1 is necessary for normal leukocyte recruitment during acute inflammation. On alveolar epithelial cells (AECs), we have shown previously that the presence of normal mICAM-1 is essential for optimal alveolar macrophage (AM) function. We have also shown that ICAM-1 is present in the alveolar space as a soluble protein that is likely produced through cleavage of mICAM-1. Soluble intercellular adhesion molecule-1 (sICAM-1) is abundantly present in the alveolar lining fluid of the normal lung and could be generated by proteolytic cleavage of mICAM-1, which is highly expressed on type I AECs. Although a growing body of data suggesting that intravascular sICAM-1 has functional effects, little is known about sICAM-1 in the alveolus. We hypothesized that sICAM-1 in the alveolar space modulates the innate immune response and alters the response to pulmonary infection.

Methods: Using the surfactant protein C (SPC) promoter, we developed a transgenic mouse (SPC-sICAM-1) that constitutively overexpresses sICAM-1 in the distal lung, and compared the responses of wild-type and SPC-sICAM-1 mice following intranasal inoculation with K. pneumoniae.

Results: SPC-sICAM-1 mice demonstrated increased mortality and increased systemic dissemination of organisms compared with wild-type mice. We also found that inflammatory responses were significantly increased in SPC-sICAM-1 mice compared with wild-type mice but there were no difference in lung CFU between groups.

Conclusions: We conclude that alveolar sICAM-1 modulates pulmonary inflammation. Manipulating ICAM-1 interactions therapeutically may modulate the host response to Gram negative pulmonary infections.

Publication types

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

MeSH terms

  • Acrylamides / metabolism*
  • Animals
  • Cells, Cultured
  • Chemokine CXCL2 / metabolism
  • Chemotaxis
  • Disease Models, Animal
  • Epithelial Cells / immunology*
  • Epithelial Cells / microbiology
  • Immunity, Innate*
  • Inflammation Mediators / metabolism
  • Klebsiella Infections / genetics
  • Klebsiella Infections / immunology*
  • Klebsiella Infections / microbiology
  • Klebsiella pneumoniae / pathogenicity*
  • Macrophages, Alveolar / immunology
  • Macrophages, Alveolar / microbiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Phagocytosis
  • Pneumonia, Bacterial / genetics
  • Pneumonia, Bacterial / immunology*
  • Pneumonia, Bacterial / microbiology
  • Promoter Regions, Genetic
  • Pulmonary Alveoli / immunology*
  • Pulmonary Alveoli / microbiology
  • Pulmonary Surfactant-Associated Protein C / genetics
  • Time Factors
  • Tumor Necrosis Factor-alpha / metabolism
  • Up-Regulation
  • beta-Alanine / analogs & derivatives*
  • beta-Alanine / genetics
  • beta-Alanine / metabolism

Substances

  • 2-(2,6-dichloro-4-((3-furan-2-ylacryloylamino)methyl)benzoylamino)-3-((thiazolidine-4-carbonyl)amino)propionic acid
  • Acrylamides
  • Chemokine CXCL2
  • Cxcl2 protein, mouse
  • Inflammation Mediators
  • Pulmonary Surfactant-Associated Protein C
  • SFTPC protein, human
  • Tumor Necrosis Factor-alpha
  • beta-Alanine