Transforming growth factor β1 alters the 3'-UTR of mRNA to promote lung fibrosis

J Biol Chem. 2019 Oct 25;294(43):15781-15794. doi: 10.1074/jbc.RA119.009148. Epub 2019 Sep 5.

Abstract

Idiopathic pulmonary fibrosis (IPF) is a chronic disease characterized by the pathological remodeling of air sacs as a result of excessive accumulation of extracellular matrix (ECM) proteins, but the mechanism governing the robust protein expression is poorly understood. Our recent findings demonstrate that alternative polyadenylation (APA) caused by NUDT21 reduction is important for the increased expression of fibrotic mediators and ECM proteins in lung fibroblasts by shortening the 3'-untranslated regions (3'-UTRs) of mRNAs and stabilizing their transcripts, therefore activating pathological signaling pathways. Despite the importance of NUDT21 reduction in the regulation of fibrosis, the underlying mechanisms for the depletion are unknown. We demonstrate here that NUDT21 is depleted by TGFβ1. We found that miR203, which is increased in IPF, was induced by TGFβ1 to target the NUDT21 3'-UTR, thus depleting NUDT21 in human and mouse lung fibroblasts. TGFβ1-mediated NUDT21 reduction was attenuated by the miR203 inhibitor antagomiR203 in fibroblasts. TGFβ1 transgenic mice revealed that TGFβ1 down-regulates NUDT21 in fibroblasts in vivo Furthermore, TGFβ1 promoted differential APA of fibrotic genes, including FGF14, RICTOR, TMOD2, and UCP5, in association with increased protein expression. This unique differential APA signature was also observed in IPF fibroblasts. Altogether, our results identified TGFβ1 as an APA regulator through NUDT21 depletion amplifying pulmonary fibrosis.

Keywords: APA; NUDT21; alternative polyadenylation; mRNA; miR203; polyadenylation; post-transcriptional regulation; pulmonary fibrosis; transforming growth factor β (TGFβ).

Publication types

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

MeSH terms

  • 3' Untranslated Regions / genetics*
  • Animals
  • Cells, Cultured
  • Cleavage And Polyadenylation Specificity Factor / genetics
  • Cleavage And Polyadenylation Specificity Factor / metabolism
  • Down-Regulation / genetics
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Fibrosis
  • Humans
  • Lung / pathology*
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Models, Biological
  • Polyadenylation / genetics
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Transforming Growth Factor beta1 / metabolism*

Substances

  • 3' Untranslated Regions
  • Cleavage And Polyadenylation Specificity Factor
  • MIRN203 microRNA, human
  • MicroRNAs
  • Nudt21 protein, human
  • Nudt21 protein, mouse
  • RNA, Messenger
  • Transforming Growth Factor beta1