Interleukin-17 signaling in inflammatory, Kupffer cells, and hepatic stellate cells exacerbates liver fibrosis in mice

  • Fanli Meng
  • , Kai Wang
  • , Tomonori Aoyama
  • , Sergei I. Grivennikov
  • , Yonghan Paik
  • , David Scholten
  • , Min Cong
  • , Keiko Iwaisako
  • , Xiao Liu
  • , Mingjun Zhang
  • , Christoph H. Sterreicher
  • , Felix Stickel
  • , Klaus Ley
  • , David A. Brenner
  • , Tatiana Kisseleva

Research output: Contribution to journalArticlepeer-review

628 Scopus citations

Abstract

BACKGROUND & AIMS: Interleukin (IL)-17 signaling has been implicated in lung and skin fibrosis. We examined the role of IL-17 signaling in the pathogenesis of liver fibrosis in mice. METHODS: Using cholestatic and hepatotoxic models of liver injury, we compared the development of liver fibrosis in wild-type mice with that of IL-17RA-/- mice and of bone marrow chimeric mice devoid of IL-17 signaling in immune and Kupffer cells (IL-17RA-/- to wild-type and IL-17A-/- to wild-type mice) or liver resident cells (wild-type to IL-17RA-/- mice). RESULTS: In response to liver injury, levels of Il-17A and its receptor increased. IL-17A increased appeared to promote fibrosis by activating inflammatory and liver resident cells. IL-17 signaling facilitated production of IL-6, IL-1, and tumor necrosis factor-α by inflammatory cells and increased the expression of transforming growth factor-1, a fibrogenic cytokine. IL-17 directly induced production of collagen type I in hepatic stellate cells by activating the signal transducer and activator of transcription 3 (Stat3) signaling pathway. Mice devoid of Stat3 signaling in hepatic stellate cells (GFAPStat3-/- mice) were less susceptible to fibrosis. Furthermore, deletion of IL-23 from immune cells attenuated liver fibrosis, whereas deletion of IL-22 exacerbated fibrosis. Administration of IL-22 and IL-17E (IL-25, a negative regulator of IL-23) protected mice from bile duct ligation-induced liver fibrosis. CONCLUSIONS: IL-17 induces liver fibrosis through multiple mechanisms in mice. Reagents that block these pathways might be developed as therapeutics for patients with cirrhosis.

Original languageEnglish
Pages (from-to)765-776.e3
JournalGastroenterology
Volume143
Issue number3
DOIs
StatePublished - Sep 2012
Externally publishedYes

Keywords

  • Bone Marrow-Derived Macrophages
  • Immune Response
  • Mouse Model
  • Myofibroblast

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