Particulate Matter Increases the Severity of Bleomycin-Induced Pulmonary Fibrosis through KC-Mediated Neutrophil Chemotaxis

Int J Mol Sci. 2019 Dec 28;21(1):227. doi: 10.3390/ijms21010227.

Abstract

Background: Although particular matter (PM) increases incidence and severity of idiopathic pulmonary fibrosis, the underlying mechanism remains elusive.

Methods: The effects of PM were evaluated in a murine model of bleomycin-induced pulmonary fibrosis. Mice were divided into four groups, receiving: (1) Saline (control), (2) bleomycin, (3) PM, or (4) bleomycin plus PM (Bleo+PM). Additional groups of Bleo+PM mice were treated with sivelestat (an inhibitor of neutrophil elastase) or reparixin (a C-X-C motif chemokine receptor 2 antagonist), or were genetically modified with keratinocyte chemoattractant (KC) deletion.

Results: Pulmonary fibrosis was not observed in the control or PM groups. Bleomycin induced pulmonary fibrosis within 14 days. The Bleo+PM group showed worse pulmonary fibrosis when compared to the bleomycin group. Analyses of immune cell profile and chemokine/cytokine concentrations at day 2-bronchoalveolar lavage fluid (BALF) revealed that the Bleo+PM group had increased neutrophil number and elastase level and KC concentration compared to the bleomycin group. Neutrophil elastase activated the Smad2/Smad3/α-SMA pathway to induce collagen deposition, while sivelestat abrogated the increased severity of pulmonary fibrosis caused by PM. Chemotaxis assay revealed that BALF of the Bleo+PM group recruited neutrophil, which was dependent on KC. Further, genetic KC deletion or pharmaceutical inhibition of KC binding to CXCR2 with reparixin ameliorated the PM-induced increased severity of pulmonary fibrosis.

Conclusions: These data provide evidence that the PM-induced increased severity of pulmonary fibrosis depends on KC-mediated neutrophil chemotaxis and give additional mechanic insight that will aid in the development of therapeutic strategies.

Keywords: idiopathic pulmonary fibrosis; neutrophil elastase; particulate matter; sivelestat.

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Animals
  • Bleomycin / toxicity
  • Cells, Cultured
  • Chemokine CXCL1 / genetics
  • Chemokine CXCL1 / metabolism*
  • Chemotaxis*
  • Collagen / genetics
  • Collagen / metabolism
  • Glycine / analogs & derivatives
  • Glycine / pharmacology
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neutrophils / drug effects*
  • Neutrophils / metabolism
  • Neutrophils / physiology
  • Particulate Matter / toxicity*
  • Pulmonary Fibrosis / etiology*
  • Pulmonary Fibrosis / metabolism
  • Pulmonary Fibrosis / pathology
  • Smad Proteins / genetics
  • Smad Proteins / metabolism
  • Sulfonamides / pharmacology

Substances

  • Actins
  • Chemokine CXCL1
  • Cxcl1 protein, mouse
  • Particulate Matter
  • Smad Proteins
  • Sulfonamides
  • Bleomycin
  • Collagen
  • sivelestat
  • Glycine
  • reparixin