Disruption of the TWEAK/Fn14 pathway prevents 5-fluorouracil-induced diarrhea in mice

World J Gastroenterol. 2017 Apr 7;23(13):2294-2307. doi: 10.3748/wjg.v23.i13.2294.

Abstract

Aim: To clarify the roles of TWEAK and its receptor Fn14 in 5-fluorouracil (5-FU)-induced diarrhea.

Methods: Diarrhea was induced in wild-type (WT), Fn14 knockout (KO), and IL-13 receptor (IL-13R)α1 KO BALB/c mice using a single injection of 5-FU. Histological analysis, cytokine analysis, and flow cytometry was performed on ileal tissues and cells. Murine colon carcinoma-bearing mice were co-treated with an anti-TWEAK antibody and 5-FU. Embryonic fibroblast response to cytokines was also analyzed.

Results: 5-FU induced high Fn14 expression in epithelial cells. The severity of 5-FU-induced diarrhea was lower in Fn14 KO mice compared with WT mice. Administration of anti-TWEAK antibody reduced 5-FU-induced diarrhea without affecting the antitumor effects of 5-FU in vivo. 5-FU-induced expression of IL-13, IL-17A, TNF-α, and IFN-γ in the ileum was Fn14 dependent. The severity of 5-FU-induced diarrhea was lower in IL-13Rα1 KO mice, indicating major role for IL-13 signaling via IL-13Rα1 in pathogenesis. We found that IL-13Rα2, an IL-13 neutralizing/cell protective receptor, was strongly induced by IL-33 in vitro and in vivo. IL-13Rα2 was upregulated in the ileum of 5-FU-treated Fn14 KO mice. Thus, the deletion of Fn14 upregulated IL-13Rα2 expression, which reduced IL-13 expression and activity.

Conclusion: Disruption of the TWEAK/Fn14 pathway affects several interconnected pathways, including those associated with IL-13, IL-33, and IL-13Rα2, to attenuate 5-FU-induced intestinal side effects.

Keywords: Cancer chemotherapy; Interleukin-13; Interleukin-13 receptor α2; Interleukin-33.

MeSH terms

  • Animals
  • Antimetabolites, Antineoplastic / adverse effects*
  • Cell Line, Tumor
  • Cytokine TWEAK / antagonists & inhibitors
  • Cytokine TWEAK / metabolism*
  • Diarrhea / chemically induced*
  • Diarrhea / metabolism
  • Diarrhea / prevention & control
  • Fluorouracil / adverse effects*
  • Interleukin-13 / metabolism
  • Interleukin-13 Receptor alpha2 Subunit / metabolism
  • Interleukin-33 / metabolism
  • Male
  • Mice, Inbred BALB C
  • Mice, Knockout
  • TWEAK Receptor / antagonists & inhibitors
  • TWEAK Receptor / metabolism*

Substances

  • Antimetabolites, Antineoplastic
  • Cytokine TWEAK
  • Il33 protein, mouse
  • Interleukin-13
  • Interleukin-13 Receptor alpha2 Subunit
  • Interleukin-33
  • TWEAK Receptor
  • Tnfrsf12a protein, mouse
  • Tnfsf12 protein, mouse
  • Fluorouracil