Blockade of CXCR3 receptor:ligand interactions reduces leukocyte recruitment to the lung and the severity of experimental idiopathic pneumonia syndrome

J Immunol. 2004 Aug 1;173(3):2050-9. doi: 10.4049/jimmunol.173.3.2050.

Abstract

Idiopathic pneumonia syndrome (IPS) is a frequently fatal complication after allogeneic stem cell transplantation (allo-SCT) that responds poorly to standard immunosuppressive therapy. The pathophysiology of IPS involves the secretion of inflammatory cytokines including IFN-gamma and TNF-alpha along with the recruitment of donor T cells to the lung. CXCR3 is a chemokine receptor that is expressed on activated Th1/Tc1 T cell subsets and the expression of its ligands CXCL9 (monokine induced by IFN-gamma (Mig)) and CXCL10 (IFN-gamma-inducible protein 10 (IP-10)) can be induced in a variety of cell types by IFN-gamma alone or in combination with TNF-alpha. We used a lethally irradiated murine SCT model (B6 --> bm1) to evaluate the role of CXCR3 receptor:ligand interactions in the development of IPS. We found that Mig and IP-10 protein levels were significantly elevated in the bronchoalveolar lavage fluid of allo-SCT recipients compared with syngeneic controls and correlated with the infiltration of IFN-gamma-secreting CXCR3(+) donor T cells into the lung. The in vivo neutralization of either Mig or IP-10 significantly reduced the severity of IPS compared with control-treated animals, and an additive effect was observed when both ligands were blocked simultaneously. Complementary experiments using CXCR3(-/-) mice as SCT donors also resulted in a significant decrease in IPS. These data demonstrate that interactions involving CXCR3 and its primary ligands Mig and IP-10 significantly contribute to donor T cell recruitment to the lung after allo-SCT. Therefore, approaches focusing on the abrogation of these interactions may prove successful in preventing or treating lung injury that occurs in this setting.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Bone Marrow Cells
  • Bronchoalveolar Lavage Fluid / cytology
  • Cells, Cultured / immunology
  • Chemokine CXCL10
  • Chemokine CXCL9
  • Chemokines, CXC / antagonists & inhibitors
  • Chemokines, CXC / physiology*
  • Chemotaxis, Leukocyte / drug effects*
  • Crosses, Genetic
  • Female
  • Hematopoietic Stem Cell Transplantation / adverse effects*
  • Interferon-gamma / biosynthesis
  • Interferon-gamma / blood
  • Ligands
  • Lung / pathology*
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Pneumonia / etiology
  • Pneumonia / immunology
  • Pneumonia / pathology
  • Pneumonia / prevention & control*
  • Receptors, CCR5 / deficiency
  • Receptors, CCR5 / genetics
  • Receptors, CXCR3
  • Receptors, Chemokine / antagonists & inhibitors
  • Receptors, Chemokine / deficiency
  • Receptors, Chemokine / genetics
  • Receptors, Chemokine / physiology*
  • Spleen / cytology
  • T-Lymphocytes, Cytotoxic / immunology
  • T-Lymphocytes, Cytotoxic / metabolism
  • Transplantation, Homologous / adverse effects*
  • Tumor Necrosis Factor-alpha / analysis

Substances

  • Chemokine CXCL10
  • Chemokine CXCL9
  • Chemokines, CXC
  • Cxcl9 protein, mouse
  • Cxcr3 protein, mouse
  • Ligands
  • Receptors, CCR5
  • Receptors, CXCR3
  • Receptors, Chemokine
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma