Human microvascular pericyte basement membrane remodeling regulates neutrophil recruitment

Microcirculation. 2015 Jan;22(1):54-67. doi: 10.1111/micc.12173.

Abstract

Objective: Neutrophil extravasation at post-capillary venules, consisting of EC, PC, and the shared ECM, increases following fibrotic remodeling in the lung, liver, and skin. The role of fibrotic pericyte-derived ECM in regulating EC activation and neutrophil recruitment remains unexplored.

Methods: To elucidate the role of human pericyte-derived ECM in EC activation, we characterized PC-derived ECM following transforming growth factor-β1, IL-1β, CCL2, or bleomycin activation, and examined surface adhesion molecule expression and neutrophil recruitment by EC cultured on PC-ECM.

Results: Pro-inflammatory activation of PC-induced deposition of compositionally distinct ECM compared with non-activated control. Bleomycin activation induced fibronectin-rich and collagen-poor ECM remodeling by PC, facilitating increased neutrophil transendothelial migration when compared with non-activated pericyte ECM (49.9 ± 3.4% versus 29.7 ± 1.4%). Increases in fibronectin compared to collagen I, are largely responsible for ECM-regulated neutrophil recruitment, as EC cultured on fibronectin supported increased neutrophil transmigration compared to collagen I (51.6 ± 6.2% versus 28.0 ± 4.8%). We attribute this difference to increased expression of ICAM-1 and its redistribution to EC borders.

Conclusions: This is the first demonstration of human pericyte sensitivity to inflammatory stimuli, inducing fibrotic matrix deposition that regulates EC adhesion molecule expression and neutrophil recruitment.

Keywords: ICAM-1; extracellular matrix; fibronectin; fibrosis; transmigration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibiotics, Antineoplastic / pharmacology
  • Basement Membrane / metabolism*
  • Bleomycin / pharmacology
  • Chemokine CCL2 / metabolism
  • Extracellular Matrix / metabolism*
  • Humans
  • Intercellular Adhesion Molecule-1 / biosynthesis*
  • Interleukin-1beta / metabolism
  • Neutrophils / cytology
  • Neutrophils / metabolism*
  • Pericytes / cytology
  • Pericytes / metabolism*
  • Transendothelial and Transepithelial Migration / drug effects
  • Transendothelial and Transepithelial Migration / physiology*
  • Transforming Growth Factor beta1 / metabolism

Substances

  • Antibiotics, Antineoplastic
  • CCL2 protein, human
  • Chemokine CCL2
  • ICAM1 protein, human
  • IL1B protein, human
  • Interleukin-1beta
  • TGFB1 protein, human
  • Transforming Growth Factor beta1
  • Bleomycin
  • Intercellular Adhesion Molecule-1