Transforming growth factor β regulates P-body formation through induction of the mRNA decay factor tristetraprolin

Mol Cell Biol. 2014 Jan;34(2):180-95. doi: 10.1128/MCB.01020-13. Epub 2013 Nov 4.

Abstract

Transforming growth factor β (TGF-β) is a potent growth regulator and tumor suppressor in normal intestinal epithelium. Likewise, epithelial cell growth is controlled by rapid decay of growth-related mRNAs mediated through 3' untranslated region (UTR) AU-rich element (ARE) motifs. We demonstrate that treatment of nontransformed intestinal epithelial cells with TGF-β inhibited ARE-mRNA expression. This effect of TGF-β was promoted through increased assembly of cytoplasmic RNA processing (P) bodies where ARE-mRNA localization was observed. P-body formation was dependent on TGF-β/Smad signaling, as Smad3 deletion abrogated P-body formation. In concert with increased P-body formation, TGF-β induced expression of the ARE-binding protein tristetraprolin (TTP), which colocalized to P bodies. TTP expression was necessary for TGF-β-dependent P-body formation and promoted growth inhibition by TGF-β. The significance of this was observed in vivo, where colonic epithelium deficient in TGF-β/Smad signaling or TTP expression showed attenuated P-body levels. These results provide new insight into TGF-β's antiproliferative properties and identify TGF-β as a novel mRNA stability regulator in intestinal epithelium through its ability to promote TTP expression and subsequent P-body formation.

Publication types

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

MeSH terms

  • 3' Untranslated Regions
  • AU Rich Elements
  • Animals
  • Binding Sites
  • Cell Line
  • Cell Proliferation
  • Cellular Senescence
  • Colon / cytology
  • Cytoplasmic Structures / metabolism
  • Intestinal Mucosa / cytology
  • Mice
  • Mice, Knockout
  • Promoter Regions, Genetic
  • RNA Processing, Post-Transcriptional
  • RNA Stability
  • RNA, Messenger / genetics*
  • RNA, Messenger / metabolism
  • Rats
  • Signal Transduction
  • Smad3 Protein / metabolism
  • Transcriptional Activation*
  • Transforming Growth Factor beta / physiology*
  • Tristetraprolin / genetics
  • Tristetraprolin / metabolism*

Substances

  • 3' Untranslated Regions
  • RNA, Messenger
  • Smad3 Protein
  • Smad3 protein, rat
  • Transforming Growth Factor beta
  • Tristetraprolin