Elevated expression of NEU1 sialidase in idiopathic pulmonary fibrosis provokes pulmonary collagen deposition, lymphocytosis, and fibrosis

Am J Physiol Lung Cell Mol Physiol. 2016 May 15;310(10):L940-54. doi: 10.1152/ajplung.00346.2015. Epub 2016 Mar 18.

Abstract

Idiopathic pulmonary fibrosis (IPF) poses challenges to understanding its underlying cellular and molecular mechanisms and the development of better therapies. Previous studies suggest a pathophysiological role for neuraminidase 1 (NEU1), an enzyme that removes terminal sialic acid from glycoproteins. We observed increased NEU1 expression in epithelial and endothelial cells, as well as fibroblasts, in the lungs of patients with IPF compared with healthy control lungs. Recombinant adenovirus-mediated gene delivery of NEU1 to cultured primary human cells elicited profound changes in cellular phenotypes. Small airway epithelial cell migration was impaired in wounding assays, whereas, in pulmonary microvascular endothelial cells, NEU1 overexpression strongly impacted global gene expression, increased T cell adhesion to endothelial monolayers, and disrupted endothelial capillary-like tube formation. NEU1 overexpression in fibroblasts provoked increased levels of collagen types I and III, substantial changes in global gene expression, and accelerated degradation of matrix metalloproteinase-14. Intratracheal instillation of NEU1 encoding, but not control adenovirus, induced lymphocyte accumulation in bronchoalveolar lavage samples and lung tissues and elevations of pulmonary transforming growth factor-β and collagen. The lymphocytes were predominantly T cells, with CD8(+) cells exceeding CD4(+) cells by nearly twofold. These combined data indicate that elevated NEU1 expression alters functional activities of distinct lung cell types in vitro and recapitulates lymphocytic infiltration and collagen accumulation in vivo, consistent with mechanisms implicated in lung fibrosis.

Keywords: fibroblasts; fibrosis; inflammation.

Publication types

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

MeSH terms

  • A549 Cells
  • Animals
  • Cell Movement
  • Endothelial Cells / enzymology
  • Endothelium, Vascular / pathology
  • Female
  • Fibrillar Collagens / metabolism
  • Fibroblasts / enzymology
  • Gene Expression
  • HEK293 Cells
  • Humans
  • Idiopathic Pulmonary Fibrosis / enzymology*
  • Idiopathic Pulmonary Fibrosis / immunology
  • Idiopathic Pulmonary Fibrosis / pathology
  • Lung / blood supply
  • Lung / enzymology*
  • Lung / pathology
  • Lymphocytes / immunology
  • Lymphocytosis / enzymology*
  • Mice, Inbred C57BL
  • Microvessels / pathology
  • Neuraminidase / genetics
  • Neuraminidase / metabolism*

Substances

  • Fibrillar Collagens
  • NEU1 protein, human
  • Neuraminidase