Heparin-disaccharide affects T cells: inhibition of NF-kappaB activation, cell migration, and modulation of intracellular signaling

J Leukoc Biol. 2004 Jun;75(6):1139-46. doi: 10.1189/jlb.1203659. Epub 2004 Mar 12.

Abstract

We previously reported that disaccharides (DS), generated by enzymatic degradation of heparin or heparan sulfate, inhibit T cell-mediated immune reactions in rodents and regulate cytokine [tumor necrosis factor alpha (TNF-alpha), interleukin (IL)-8, and IL-1beta] secretion by T cells, macrophages, or intestinal epithelial cells. Here, we investigated the effects of a trisulfated heparin DS (3S-DS) on two aspects of T cell function: secretion of proinflammatory cytokines and migration to an inflamed site. 3S-DS down-regulated nuclear factor-kappaB activity and reduced the secretion of TNF-alpha and interferon-gamma (IFN-gamma) by anti-CD3-activated T cells. In addition, 3S-DS inhibited CXC chemokine ligand 12 (CXCL12; stromal cell-derived factor-1alpha)-dependent migration in vitro and in vivo and decreased CXCL12-induced T cell adhesion to the extracellular matrix glycoprotein, fibronectin (FN). This inhibition was accompanied by attenuation of CXCL12-induced Pyk2 phosphorylation but did not involve internalization of the CXCL12 receptor, CXCR4, or phosphorylation of extracellular-regulated kinase. Despite inhibiting CXCL12-induced adhesion, 3S-DS, on its own, induced T cell adhesion to FN, which was accompanied by phosphorylation of Pyk2. A monosulfated DS showed no effect. Taken together, these data provide evidence that 3S-DS can regulate inflammation by inducing and modulating T cell-signaling events, desensitizing CXCR4, and modulating T cell receptor-induced responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Bone Marrow / metabolism
  • Cell Adhesion / drug effects
  • Cell Movement / drug effects*
  • Chemokine CXCL12
  • Chemokines, CXC / metabolism
  • Chemotaxis
  • Disaccharides / pharmacology*
  • Fibronectins / metabolism
  • Focal Adhesion Kinase 2
  • Heparin / analogs & derivatives*
  • Heparin / pharmacology*
  • Heparitin Sulfate / pharmacology
  • Humans
  • Interferon-gamma / metabolism
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Mitogen-Activated Protein Kinases / metabolism
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / genetics
  • NF-kappa B / metabolism*
  • Phosphorylation
  • Protein-Tyrosine Kinases / metabolism
  • Receptors, Antigen, T-Cell / metabolism
  • Receptors, CXCR4 / metabolism
  • Signal Transduction*
  • T-Lymphocytes / drug effects*
  • T-Lymphocytes / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Antibodies, Monoclonal
  • CXCL12 protein, human
  • Chemokine CXCL12
  • Chemokines, CXC
  • Cxcl12 protein, mouse
  • Disaccharides
  • Fibronectins
  • NF-kappa B
  • Receptors, Antigen, T-Cell
  • Receptors, CXCR4
  • Tumor Necrosis Factor-alpha
  • heparin disaccharide
  • Interferon-gamma
  • Heparin
  • Heparitin Sulfate
  • Protein-Tyrosine Kinases
  • Focal Adhesion Kinase 2
  • Ptk2b protein, mouse
  • Mitogen-Activated Protein Kinases