Sialylated keratan sulfate proteoglycans are Siglec-8 ligands in human airways

Glycobiology. 2018 Oct 1;28(10):786-801. doi: 10.1093/glycob/cwy057.

Abstract

Human siglecs are a family of 14 sialic acid-binding proteins, most of which are expressed on subsets of immune cells where they regulate immune responses. Siglec-8 is expressed selectively on human allergic inflammatory cells-primarily eosinophils and mast cells-where engagement causes eosinophil apoptosis and inhibits mast cell mediator release. Evidence supports a model in which human eosinophils and mast cells bind to Siglec-8 sialoglycan ligands on inflammatory target tissues to resolve allergic inflammation and limit tissue damage. To identify Siglec-8-binding sialoglycans from human airways, proteins extracted from postmortem human trachea were resolved by size-exclusion chromatography and composite agarose-acrylamide gel electrophoresis, blotted and probed by Siglec-8-Fc blot overlay. Three size classes of Siglec-8 ligands were identified: 250 kDa, 600 kDa and 1 MDa, each of which was purified by affinity chromatography using a recombinant pentameric form of Siglec-8. Proteomic mass spectrometry identified all size classes as the proteoglycan aggrecan, a finding validated by immunoblotting. Glycan array studies demonstrated Siglec-8 binding to synthetic glycans with a terminal Neu5Acα2-3(6-sulfo)-Gal determinant, a quantitatively minor terminus on keratan sulfate (KS) chains of aggrecan. Treating human tracheal extracts with sialidase or keratanase eliminated Siglec-8 binding, indicating sialylated KS chains as Siglec-8-binding determinants. Treating human tracheal histological sections with keratanase also completely eliminated the binding of Siglec-8-Fc. Finally, Siglec-8 ligand purified from human trachea extracts induced increased apoptosis of freshly isolated human eosinophils in vitro. We conclude that sialylated KS proteoglycans are endogenous human airway ligands that bind Siglec-8 and may regulate allergic inflammation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Antigens, CD / chemistry*
  • Antigens, CD / isolation & purification
  • Antigens, CD / metabolism
  • Antigens, Differentiation, B-Lymphocyte / chemistry*
  • Antigens, Differentiation, B-Lymphocyte / isolation & purification
  • Antigens, Differentiation, B-Lymphocyte / metabolism
  • Apoptosis / drug effects
  • Eosinophils / drug effects
  • Eosinophils / metabolism
  • Female
  • Humans
  • Inflammation / metabolism
  • Keratan Sulfate / chemistry*
  • Keratan Sulfate / metabolism
  • Keratan Sulfate / pharmacology
  • Lectins / chemistry*
  • Lectins / isolation & purification
  • Lectins / metabolism
  • Ligands
  • Male
  • Middle Aged
  • Proteoglycans / chemistry*
  • Proteoglycans / metabolism
  • Proteoglycans / pharmacology
  • Sialic Acids / chemistry*
  • Sialic Acids / metabolism
  • Sialic Acids / pharmacology
  • Trachea / chemistry*
  • Trachea / metabolism

Substances

  • Antigens, CD
  • Antigens, Differentiation, B-Lymphocyte
  • Lectins
  • Ligands
  • Proteoglycans
  • SIGLEC8 protein, human
  • Sialic Acids
  • Keratan Sulfate