CCR7/CCL19 controls expression of EDG-1 in T cells

J Biol Chem. 2012 Apr 6;287(15):11656-64. doi: 10.1074/jbc.M111.310045. Epub 2012 Feb 13.

Abstract

T lymphocytes circulate between the blood, tissues, and lymph. These T cells carry out immune functions, using the C-C chemokine receptor 7 (CCR7) and its cognate ligands, CCL19 and CCL21, to enter and travel through the lymph nodes. Distinct roles for each ligand in regulating T lymphocyte trafficking have remained elusive. We report that in the human T cell line HuT78 and in primary murine T lymphocytes, signaling from CCR7/CCL19 leads to increased expression and phosphorylation of extracellular signal-regulated kinase 5 (ERK5) within eight hours of stimulation. Within 48-72 h we observed peak levels of endothelial differentiation gene 1 (EDG-1), which mediates the egress of T lymphocytes from lymph nodes. The increased expression of EDG-1 was preceded by up-regulation of its transcription factor, Krüppel-like factor 2 (KLF-2). To determine the cellular effect of disrupting ERK5 signaling from CCR7, we examined the migration of ERK5(flox/flox)/Lck-Cre murine T cells to EDG-1 ligands. While CCL19-stimulated ERK5(flox/flox) naïve T cells showed increased migration to EDG-1 ligands at 48 h, the migration of ERK5(flox/flox)/Lck-Cre T cells remained at a basal level. Accordingly, we define a novel signaling pathway that controls EDG-1 up-regulation following stimulation of T cells by CCR7/CCL19. This is the first report to link the two signaling events that control migration through the lymph nodes: CCR7 mediates entry into the lymph nodes and EDG-1 signaling controls their subsequent exit.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus
  • Animals
  • Cell Line
  • Chemokine CCL19 / genetics
  • Chemokine CCL19 / metabolism
  • Chemokine CCL19 / physiology*
  • Chemokine CCL21 / physiology
  • Chemotaxis
  • Dendritic Cells / metabolism
  • Gene Expression
  • Gene Expression Regulation*
  • Humans
  • Lysophospholipids / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Mitogen-Activated Protein Kinase 7 / genetics
  • Mitogen-Activated Protein Kinase 7 / metabolism
  • Phosphorylation
  • Receptors, CCR7 / metabolism
  • Receptors, CCR7 / physiology*
  • Receptors, Lysosphingolipid / genetics
  • Receptors, Lysosphingolipid / metabolism*
  • Signal Transduction
  • Sphingosine / analogs & derivatives
  • Sphingosine / physiology
  • Sphingosine-1-Phosphate Receptors
  • T-Lymphocytes / metabolism*
  • T-Lymphocytes / physiology

Substances

  • CCL19 protein, human
  • CCR7 protein, human
  • Chemokine CCL19
  • Chemokine CCL21
  • Lysophospholipids
  • Receptors, CCR7
  • Receptors, Lysosphingolipid
  • S1PR1 protein, human
  • Sphingosine-1-Phosphate Receptors
  • sphingosine 1-phosphate
  • MAPK1 protein, human
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinase 7
  • Sphingosine