Proinflammatory effects of TWEAK/Fn14 interactions in glomerular mesangial cells

J Immunol. 2006 Feb 1;176(3):1889-98. doi: 10.4049/jimmunol.176.3.1889.

Abstract

TNF-like weak inducer of apoptosis, or TWEAK, is a relatively new member of the TNF-ligand superfamily. Ligation of the TWEAK receptor Fn14 by TWEAK has proinflammatory effects on fibroblasts, synoviocytes, and endothelial cells. Several of the TWEAK-inducible cytokines are important in the pathogenesis of kidney diseases; however, whether TWEAK can induce a proinflammatory effect on kidney cells is not known. We found that murine mesangial cells express cell surface TWEAK receptor. TWEAK stimulation of mesangial cells led to a dose-dependent increase in CCL2/MCP-1, CCL5/RANTES, CXCL10/IFN-gamma-induced protein 10 kDa, and CXCL1/KC. The induced levels of chemokines were comparable to those found following mesangial cell exposure to potent proinflammatory stimuli such as TNF-alpha + IL-1beta. CXCL11/interferon-inducible T cell alpha chemoattractant, CXCR5, mucosal addressin cell adhesion molecule-1, and VCAM-1 were up-regulated by TWEAK as well. TWEAK stimulation of mesangial cells resulted in an increase in phosphorylated Ikappa-B, while pretreatment with an Ikappa-B phosphorylation inhibitor significantly blocked chemokine induction, implicating activation of the NF-kappaB signaling pathway in TWEAK-induced chemokine secretion. Importantly, the Fn14-mediated proinflammatory effects of TWEAK on kidney cells were confirmed using mesangial cells derived from Fn14-deficient mice and by injection in vivo of TWEAK into wild-type vs Fn14-deficient mice. Finally, TWEAK-induced chemokine secretion was prevented by treatment with novel murine anti-TWEAK Abs. We conclude that TWEAK induces mesangial cells to secrete proinflammatory chemokines, suggesting a prominent role for TWEAK in the pathogenesis of renal injury. Our results support Ab inhibition of TWEAK as a potential new approach for the treatment of chemokine-dependent inflammatory kidney diseases.

Publication types

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

MeSH terms

  • Animals
  • Antibodies, Monoclonal
  • Apoptosis / immunology
  • Cell Line, Transformed
  • Cells, Cultured
  • Chemokines / biosynthesis
  • Cytokine TWEAK
  • Glomerular Mesangium / metabolism*
  • I-kappa B Proteins / metabolism
  • Inflammation Mediators / metabolism
  • Inflammation Mediators / physiology*
  • Interferon-gamma / physiology
  • Interleukin-1 / physiology
  • Interleukin-6 / physiology
  • Mesangial Cells / metabolism*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • NF-KappaB Inhibitor alpha
  • Phosphorylation
  • Receptors, Tumor Necrosis Factor / genetics
  • Receptors, Tumor Necrosis Factor / physiology*
  • TWEAK Receptor
  • Tumor Necrosis Factor Inhibitors
  • Tumor Necrosis Factor-alpha / physiology
  • Tumor Necrosis Factors / immunology
  • Tumor Necrosis Factors / metabolism
  • Tumor Necrosis Factors / physiology*
  • Up-Regulation / physiology

Substances

  • Antibodies, Monoclonal
  • Chemokines
  • Cytokine TWEAK
  • I-kappa B Proteins
  • Inflammation Mediators
  • Interleukin-1
  • Interleukin-6
  • Nfkbia protein, mouse
  • Receptors, Tumor Necrosis Factor
  • TWEAK Receptor
  • Tnfrsf12a protein, mouse
  • Tnfsf12 protein, mouse
  • Tumor Necrosis Factor Inhibitors
  • Tumor Necrosis Factor-alpha
  • Tumor Necrosis Factors
  • NF-KappaB Inhibitor alpha
  • Interferon-gamma