Galectin-8 binds specific beta1 integrins and induces polarized spreading highlighted by asymmetric lamellipodia in Jurkat T cells

Exp Cell Res. 2006 Feb 15;312(4):374-86. doi: 10.1016/j.yexcr.2005.10.025.

Abstract

Integrin-mediated encounters of T cells with extracellular cues lead these cells to adhere to a variety of substrates and acquire a spread phenotype needed for their tissue incursions. We studied the effects of galectin-8 (Gal-8), a beta-galactoside binding lectin, on Jurkat T cells. Immobilized Gal-8 bound alpha1beta1, alpha3beta1 and alpha5beta1 but not alpha2beta1 and alpha4beta1 and adhered these cells with similar kinetics to immobilized fibronectin (FN). Function-blocking experiments with monoclonal anti-integrin antibodies suggested that alpha5beta1 is the main mediator of cell adhesion to this lectin. Gal-8, but not FN, induced extensive cell spreading frequently leading to a polarized phenotype characterized by an asymmetric lamellipodial protrusion. These morphological changes involved actin cytoskeletal rearrangements controlled by PI3K, Rac-1 and ERK1/2 activity. Gal-8-induced Rac-1 activation and binding to alpha1 and alpha5 integrins have not been described in any other cellular system. Strikingly, Gal-8 was also a strong stimulus on Jurkat cells in suspension, triggering ERK1/2 activation that in most adherent cells is instead dependent on cell attachment. In addition, we found that patients with systemic lupus erythematosus (SLE), a prototypic autoimmune disorder, produce Gal-8 autoantibodies that impede both its binding to integrins and cell adhesion. These are the first function-blocking autoantibodies reported for a member of the galectin family. These results indicate that Gal-8 constitutes a novel extracellular stimulus for T cells, able to bind specific beta1 integrins and to trigger signaling pathways conducive to cell spreading. Gal-8 could modulate a wide range of T cell-driven immune processes that eventually become altered in autoimmune disorders.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Androstadienes / pharmacology
  • Antibodies, Monoclonal / pharmacology
  • Autoantibodies / pharmacology
  • Cell Adhesion / drug effects
  • Cell Adhesion / physiology
  • Cell Shape / drug effects
  • Cell Surface Extensions / drug effects
  • Cell Surface Extensions / physiology
  • Cytochalasin D / pharmacology
  • Cytoskeleton / drug effects
  • Cytoskeleton / metabolism
  • Fibronectins / metabolism
  • Fibronectins / pharmacology
  • Flavonoids / pharmacology
  • Galectins / antagonists & inhibitors
  • Galectins / metabolism*
  • Galectins / pharmacology
  • Humans
  • Integrin beta1 / immunology
  • Integrin beta1 / metabolism*
  • Jurkat Cells
  • Leukemia, T-Cell / metabolism
  • Leukemia, T-Cell / pathology
  • Leukocytes, Mononuclear / cytology
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / metabolism
  • Lupus Erythematosus, Systemic / immunology
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Phosphoinositide-3 Kinase Inhibitors
  • Protein Binding / drug effects
  • Protein Kinase Inhibitors / pharmacology
  • Thiogalactosides / pharmacology
  • Transfection
  • Wortmannin
  • rac1 GTP-Binding Protein / genetics
  • rac1 GTP-Binding Protein / metabolism

Substances

  • Androstadienes
  • Antibodies, Monoclonal
  • Autoantibodies
  • Fibronectins
  • Flavonoids
  • Galectins
  • Integrin beta1
  • LGALS8 protein, human
  • Phosphoinositide-3 Kinase Inhibitors
  • Protein Kinase Inhibitors
  • RAC1 protein, human
  • Thiogalactosides
  • Cytochalasin D
  • thiodigalactoside
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • rac1 GTP-Binding Protein
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one
  • Wortmannin