Endogenous attenuation of allergic lung inflammation by syndecan-1

J Immunol. 2005 May 1;174(9):5758-65. doi: 10.4049/jimmunol.174.9.5758.

Abstract

The airway plays a vital role in allergic lung diseases by responding to inhaled allergens and initiating allergic inflammation. Various proinflammatory functions of the airway epithelium have been identified, but, equally important, anti-inflammatory mechanisms must also exist. We show in this study that syndecan-1, the major heparan sulfate proteoglycan of epithelial cells, attenuates allergic lung inflammation. Our results show that syndecan-1-null mice instilled with allergens exhibit exaggerated airway hyperresponsiveness, glycoprotein hypersecretion, eosinophilia, and lung IL-4 responses. However, administration of purified syndecan-1 ectodomains, but not ectodomain core proteins devoid of heparan sulfate, significantly inhibits these inflammatory responses. Furthermore, syndecan-1 ectodomains are shed into the airway when wild-type mice are intranasally instilled with several biochemically distinct inducers of allergic lung inflammation. Our results also show that syndecan-1 ectodomains bind to the CC chemokines (CCL7, CCL11, and CCL17) implicated in allergic diseases, inhibit CC chemokine-mediated T cell migration, and suppress allergen-induced accumulation of Th2 cells in the lung through their heparan sulfate chains. Together, these findings uncover an endogenous anti-inflammatory mechanism of the airway epithelium where syndecan-1 ectodomains attenuate allergic lung inflammation via suppression of CC chemokine-mediated Th2 cell recruitment to the lung.

Publication types

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

MeSH terms

  • Adjuvants, Immunologic / deficiency
  • Adjuvants, Immunologic / genetics
  • Adjuvants, Immunologic / metabolism
  • Adjuvants, Immunologic / physiology*
  • Administration, Intranasal
  • Amino Acid Sequence
  • Animals
  • Antigens, Fungal / administration & dosage
  • Aspergillus fumigatus / immunology
  • Cell Migration Inhibition
  • Chemokines, CC / antagonists & inhibitors
  • Chemokines, CC / metabolism
  • Gene Deletion
  • Heparan Sulfate Proteoglycans / physiology
  • Inflammation Mediators / metabolism
  • Inflammation Mediators / physiology*
  • Interleukin-4 / biosynthesis
  • Lung / immunology*
  • Lung / metabolism
  • Lung / pathology*
  • Membrane Glycoproteins / deficiency
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Membrane Glycoproteins / physiology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Molecular Sequence Data
  • Ovalbumin / administration & dosage
  • Peptide Fragments / metabolism
  • Peptide Fragments / physiology
  • Protein Binding / immunology
  • Protein Structure, Tertiary
  • Proteoglycans / deficiency
  • Proteoglycans / genetics
  • Proteoglycans / metabolism
  • Proteoglycans / physiology*
  • Respiratory Hypersensitivity / genetics
  • Respiratory Hypersensitivity / immunology
  • Respiratory Hypersensitivity / pathology*
  • Respiratory Hypersensitivity / prevention & control*
  • Syndecan-1
  • Syndecans
  • Th2 Cells / immunology
  • Th2 Cells / metabolism
  • Th2 Cells / pathology

Substances

  • Adjuvants, Immunologic
  • Antigens, Fungal
  • Chemokines, CC
  • Heparan Sulfate Proteoglycans
  • Inflammation Mediators
  • Membrane Glycoproteins
  • Peptide Fragments
  • Proteoglycans
  • Sdc1 protein, mouse
  • Syndecan-1
  • Syndecans
  • Interleukin-4
  • Ovalbumin