Identification of L-selectin binding heparan sulfates attached to collagen type XVIII

J Biol Chem. 2005 Jul 22;280(29):26965-73. doi: 10.1074/jbc.M502188200. Epub 2005 May 24.

Abstract

L-selectin is a C-type lectin expressed on leukocytes that is involved in both lymphocyte homing to the lymph node and leukocyte extravasation during inflammation. Known L-selectin ligands include sulfated Lewis-type carbohydrates, glycolipids, and proteoglycans. Previously, we have shown that in situ detection of different types of L-selectin ligands is highly dependent on the tissue fixation protocol used. Here we use this knowledge to specifically examine the expression of L-selectin binding proteoglycans in normal mouse tissues. We show that L-selectin binding chondroitin/dermatan sulfate proteoglycans are present in cartilage, whereas L-selectin binding heparan sulfate proteoglycans are present in spleen and kidney. Furthermore, we show that L-selectin only binds a subset of renal heparan sulfates, attached to a collagen type XVIII protein backbone and predominantly present in medullary tubular and vascular basement membranes. As L-selectin does not bind other renal heparan sulfate proteoglycans such as perlecan, agrin, and syndecan-4, and not all collagen type XVIII expressed in the kidney binds L-selectin, this indicates that there is a specific L-selectin binding domain on heparan sulfate glycosaminoglycan chains. Using an in vitro L-selectin binding assay, we studied the contribution of N-sulfation, O-sulfation, C5-epimerization, unsubstituted glucosamine residues, and chain length in L-selectin binding to heparan sulfate/heparin glycosaminoglycan chains. Based on our results and the accepted model of heparan sulfate domain organization, we propose a model for the interaction of L-selectin with heparan sulfate glycosaminoglycan chains. Interestingly, this opens the possibility of active regulation of L-selectin binding to heparan sulfate proteoglycans, e.g. under inflammatory conditions.

MeSH terms

  • Animals
  • Collagen Type XVIII / metabolism*
  • Heparitin Sulfate / metabolism*
  • Humans
  • Kidney / chemistry
  • L-Selectin / metabolism*
  • Ligands
  • Mice
  • Mice, Inbred C57BL
  • Protein Binding
  • Proteoglycans / analysis
  • Proteoglycans / chemistry
  • Proteoglycans / metabolism
  • Selectins
  • Substrate Specificity
  • Tissue Distribution

Substances

  • Collagen Type XVIII
  • Ligands
  • Proteoglycans
  • Selectins
  • L-Selectin
  • Heparitin Sulfate