miR-34a is a microRNA safeguard for Citrobacter-induced inflammatory colon oncogenesis

Elife. 2018 Dec 13:7:e39479. doi: 10.7554/eLife.39479.

Abstract

Inflammation often induces regeneration to repair the tissue damage. However, chronic inflammation can transform temporary hyperplasia into a fertile ground for tumorigenesis. Here, we demonstrate that the microRNA miR-34a acts as a central safeguard to protect the inflammatory stem cell niche and reparative regeneration. Although playing little role in regular homeostasis, miR-34a deficiency leads to colon tumorigenesis after Citrobacter rodentium infection. miR-34a targets both immune and epithelial cells to restrain inflammation-induced stem cell proliferation. miR-34a targets Interleukin six receptor (IL-6R) and Interleukin 23 receptor (IL-23R) to suppress T helper 17 (Th17) cell differentiation and expansion, targets chemokine CCL22 to hinder Th17 cell recruitment to the colon epithelium, and targets an orphan receptor Interleukin 17 receptor D (IL-17RD) to inhibit IL-17-induced stem cell proliferation. Our study highlights the importance of microRNAs in protecting the stem cell niche during inflammation despite their lack of function in regular tissue homeostasis.

Keywords: Citrobacter rodentium; Th17; cancer biology; colon cancer; inflammation; mouse; stem cell.

Publication types

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

MeSH terms

  • Animals
  • Cell Transformation, Neoplastic / genetics*
  • Cells, Cultured
  • Citrobacter rodentium / physiology
  • Colon / metabolism*
  • Colon / microbiology
  • Colon / pathology
  • Enterobacteriaceae Infections / genetics*
  • Enterobacteriaceae Infections / microbiology
  • Gene Expression Profiling*
  • Inflammation / genetics*
  • Inflammation / microbiology
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • MicroRNAs / genetics*
  • Neoplastic Stem Cells / metabolism
  • Receptors, Interleukin / genetics
  • Receptors, Interleukin / metabolism
  • Th17 Cells / metabolism

Substances

  • MIRN34a microRNA, mouse
  • MicroRNAs
  • Receptors, Interleukin