Spred-2 deficiency exacerbates lipopolysaccharide-induced acute lung inflammation in mice

PLoS One. 2014 Oct 2;9(9):e108914. doi: 10.1371/journal.pone.0108914. eCollection 2014.

Abstract

Background: Acute respiratory distress syndrome (ARDS) is a severe and life-threatening acute lung injury (ALI) that is caused by noxious stimuli and pathogens. ALI is characterized by marked acute inflammation with elevated alveolar cytokine levels. Mitogen-activated protein kinase (MAPK) pathways are involved in cytokine production, but the mechanisms that regulate these pathways remain poorly characterized. Here, we focused on the role of Sprouty-related EVH1-domain-containing protein (Spred)-2, a negative regulator of the Ras-Raf-extracellular signal-regulated kinase (ERK)-MAPK pathway, in lipopolysaccharide (LPS)-induced acute lung inflammation.

Methods: Wild-type (WT) mice and Spred-2(-/-) mice were exposed to intratracheal LPS (50 µg in 50 µL PBS) to induce pulmonary inflammation. After LPS-injection, the lungs were harvested to assess leukocyte infiltration, cytokine and chemokine production, ERK-MAPK activation and immunopathology. For ex vivo experiments, alveolar macrophages were harvested from untreated WT and Spred-2(-/-) mice and stimulated with LPS. In in vitro experiments, specific knock down of Spred-2 by siRNA or overexpression of Spred-2 by transfection with a plasmid encoding the Spred-2 sense sequence was introduced into murine RAW264.7 macrophage cells or MLE-12 lung epithelial cells.

Results: LPS-induced acute lung inflammation was significantly exacerbated in Spred-2(-/-) mice compared with WT mice, as indicated by the numbers of infiltrating leukocytes, levels of alveolar TNF-α, CXCL2 and CCL2 in a later phase, and lung pathology. U0126, a selective MEK/ERK inhibitor, reduced the augmented LPS-induced inflammation in Spred-2(-/-) mice. Specific knock down of Spred-2 augmented LPS-induced cytokine and chemokine responses in RAW264.7 cells and MLE-12 cells, whereas Spred-2 overexpression decreased this response in RAW264.7 cells.

Conclusions: The ERK-MAPK pathway is involved in LPS-induced acute lung inflammation. Spred-2 controls the development of LPS-induced lung inflammation by negatively regulating the ERK-MAPK pathway. Thus, Spred-2 may represent a therapeutic target for the treatment of ALI.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Disease
  • Animals
  • Butadienes / pharmacology
  • Cell Line
  • Chemokine CCL2 / metabolism
  • Chemokine CXCL2 / metabolism
  • Disease Progression*
  • Enzyme Activation / drug effects
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Lipopolysaccharides
  • Macrophages, Alveolar / drug effects
  • Macrophages, Alveolar / metabolism
  • Macrophages, Alveolar / pathology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nitriles / pharmacology
  • Pneumonia / enzymology
  • Pneumonia / metabolism*
  • Pneumonia / pathology*
  • Repressor Proteins / deficiency*
  • Repressor Proteins / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Butadienes
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Chemokine CXCL2
  • Lipopolysaccharides
  • Nitriles
  • Repressor Proteins
  • Spred2 protein, mouse
  • Tumor Necrosis Factor-alpha
  • U 0126
  • Extracellular Signal-Regulated MAP Kinases

Grants and funding

This work was supported in part by grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and a Grant-in-Aid for Scientific Research (B) (25293095). There were no further internal or external sources of funding. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.