Monocyte chemoattractant protein 1 regulates pulmonary host defense via neutrophil recruitment during Escherichia coli infection

Infect Immun. 2011 Jul;79(7):2567-77. doi: 10.1128/IAI.00067-11. Epub 2011 Apr 25.

Abstract

Neutrophil accumulation is a critical event to clear bacteria. Since uncontrolled neutrophil recruitment can cause severe lung damage, understanding neutrophil trafficking mechanisms is important to attenuate neutrophil-mediated damage. While monocyte chemoattractant protein 1 (MCP-1) is known to be a monocyte chemoattractant, its role in pulmonary neutrophil-mediated host defense against Gram-negative bacterial infection is not understood. We hypothesized that MCP-1/chemokine (C-C motif) ligand 2 is important for neutrophil-mediated host defense. Reduced bacterial clearance in the lungs was observed in MCP-1(-/-) mice following Escherichia coli infection. Neutrophil influx, along with cytokines/chemokines, leukotriene B(4) (LTB(4)), and vascular cell adhesion molecule 1 levels in the lungs, was reduced in MCP-1(-/-) mice after infection. E. coli-induced activation of NF-κB and mitogen-activated protein kinases in the lung was also reduced in MCP-1(-/-) mice. Administration of intratracheal recombinant MCP-1 (rMCP-1) to MCP-1(-/-) mice induced pulmonary neutrophil influx and cytokine/chemokine responses in the presence or absence of E. coli infection. Our in vitro migration experiment demonstrates MCP-1-mediated neutrophil chemotaxis. Notably, chemokine receptor 2 is expressed on lung and blood neutrophils, which are increased upon E. coli infection. Furthermore, our findings show that neutrophil depletion impairs E. coli clearance and that exogenous rMCP-1 after infection improves bacterial clearance in the lungs. Overall, these new findings demonstrate that E. coli-induced MCP-1 causes neutrophil recruitment directly via chemotaxis as well as indirectly via modulation of keratinocyte cell-derived chemokine, macrophage inflammatory protein 2, and LTB(4).

Publication types

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

MeSH terms

  • Animals
  • Bone Marrow Transplantation
  • Bronchoalveolar Lavage Fluid / immunology
  • Bronchoalveolar Lavage Fluid / microbiology
  • Chemokine CCL2 / immunology*
  • Chemokine CCL2 / metabolism*
  • Chemokine CXCL2 / analysis
  • Escherichia coli / immunology*
  • Escherichia coli Infections / immunology*
  • Escherichia coli Infections / microbiology
  • Leukotriene B4 / analysis
  • Lung / immunology
  • Lung / metabolism
  • Lung / microbiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitogen-Activated Protein Kinases / metabolism
  • NF-kappa B / metabolism
  • Neutrophil Infiltration*
  • Pneumonia, Bacterial / immunology*
  • Pneumonia, Bacterial / metabolism
  • Pneumonia, Bacterial / microbiology
  • Vascular Cell Adhesion Molecule-1 / analysis

Substances

  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Chemokine CXCL2
  • NF-kappa B
  • Vascular Cell Adhesion Molecule-1
  • Leukotriene B4
  • Mitogen-Activated Protein Kinases