Lung inflammation promotes metastasis through neutrophil protease-mediated degradation of Tsp-1

Proc Natl Acad Sci U S A. 2015 Dec 29;112(52):16000-5. doi: 10.1073/pnas.1507294112. Epub 2015 Dec 14.

Abstract

Inflammation is inextricably associated with primary tumor progression. However, the contribution of inflammation to tumor outgrowth in metastatic organs has remained underexplored. Here, we show that extrinsic inflammation in the lungs leads to the recruitment of bone marrow-derived neutrophils, which degranulate azurophilic granules to release the Ser proteases, elastase and cathepsin G, resulting in the proteolytic destruction of the antitumorigenic factor thrombospondin-1 (Tsp-1). Genetic ablation of these neutrophil proteases protected Tsp-1 from degradation and suppressed lung metastasis. These results provide mechanistic insights into the contribution of inflammatory neutrophils to metastasis and highlight the unique neutrophil protease-Tsp-1 axis as a potential antimetastatic therapeutic target.

Keywords: inflammation; metastasis; neutrophils; proteases; thrombospondin-1.

Publication types

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

MeSH terms

  • Animals
  • Blotting, Western
  • Bone Marrow Transplantation
  • Cathepsin G / metabolism
  • Cell Line, Tumor
  • Female
  • Flow Cytometry
  • Gene Expression
  • Leukocyte Elastase / metabolism
  • Lipopolysaccharides / administration & dosage
  • Lung Neoplasms / metabolism*
  • Lung Neoplasms / secondary
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasms, Experimental / metabolism
  • Neoplasms, Experimental / pathology
  • Neutrophils / drug effects
  • Neutrophils / enzymology
  • Neutrophils / metabolism*
  • Peptide Hydrolases / metabolism*
  • Pneumonia / metabolism*
  • Proteolysis
  • Reverse Transcriptase Polymerase Chain Reaction
  • Serine Proteases / metabolism
  • Thrombospondin 1 / genetics
  • Thrombospondin 1 / metabolism*

Substances

  • Lipopolysaccharides
  • Thrombospondin 1
  • Peptide Hydrolases
  • Serine Proteases
  • Cathepsin G
  • Leukocyte Elastase