GlcNAc6ST-1-mediated decoration of MAdCAM-1 protein with L-selectin ligand carbohydrates directs disease activity of ulcerative colitis

Inflamm Bowel Dis. 2009 May;15(5):697-706. doi: 10.1002/ibd.20827.

Abstract

Background: A diffuse lymphocyte infiltrate is 1 of the characteristic features of ulcerative colitis (UC). Such lymphocyte recruitment requires lymphocyte rolling mediated by L-selectin ligand carbohydrates (6-sulfo sialyl Lewis X-capped O-glycans) and/or mucosal addressin cell adhesion molecule 1 (MAdCAM-1) expressed on high endothelial venule (HEV)-like vessels. The present study was undertaken to elucidate the role of MAdCAM-1 posttranslationally modified ("decorated") with L-selectin ligand carbohydrates in UC pathogenesis and consequent clinical outcomes.

Methods: Biopsy specimens composed of active and remission phases of UC as well as normal colonic mucosa were immunostained for CD34, MAdCAM-1, and MECA-79, and the immunostained sections were quantitatively analyzed. Reverse-transcriptase polymerase chain reaction (RT-PCR) was carried out to evaluate transcripts of MAdCAM-1 and N-acetylglucosamine-6-O-sulfotransferases (GlcNAc6STs). CHO and Lec2 cells transfected with CD34 and MAdCAM-1 together with enzymes involved in L-selectin ligand carbohydrate biosynthesis were analyzed by immunofluorescence, FACS, and Western blotting to characterize the biochemical properties of GlcNAc6STs.

Results: The number of MAdCAM-1(+) vessels was increased in UC, with no significant difference between active and remission phases. An increased ratio of MECA-79(+) to MAdCAM-1(+) vessels with preferential GlcNAc6ST-1 transcripts was observed in the active phase of UC compared to the remission phase. MAdCAM-1 protein was colocalized with L-selectin ligand carbohydrates at the luminal surface of HEV-like vessels in situ. GlcNAc6ST-1 preferentially utilizes MAdCAM-1 as a scaffold protein for GlcNAc-6-O-sulfation in L-selectin ligand carbohydrate biosynthesis.

Conclusions: UC disease activity is not regulated by expression of MAdCAM-1 protein itself, but rather by GlcNAc6ST-1-mediated decoration of MAdCAM-1 protein with L-selectin ligand carbohydrates.

Publication types

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

MeSH terms

  • Animals
  • Antigens, Surface / genetics
  • Antigens, Surface / metabolism
  • Blotting, Western
  • CHO Cells
  • Carbohydrate Sulfotransferases
  • Case-Control Studies
  • Cell Adhesion Molecules
  • Colitis, Ulcerative / metabolism*
  • Colitis, Ulcerative / pathology*
  • Cricetinae
  • Cricetulus
  • Fluorescent Antibody Technique
  • Humans
  • Immunoenzyme Techniques
  • Immunoglobulins / genetics
  • Immunoglobulins / metabolism*
  • L-Selectin / metabolism*
  • Ligands
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mucoproteins / genetics
  • Mucoproteins / metabolism*
  • Oligosaccharides / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sialyl Lewis X Antigen
  • Sulfotransferases / genetics
  • Sulfotransferases / metabolism*

Substances

  • Antigens, Surface
  • Cell Adhesion Molecules
  • Immunoglobulins
  • L-selectin counter-receptors
  • Ligands
  • MADCAM1 protein, human
  • Membrane Proteins
  • Mucoproteins
  • Oligosaccharides
  • RNA, Messenger
  • Sialyl Lewis X Antigen
  • L-Selectin
  • Sulfotransferases