Regnase-1 Maintains Iron Homeostasis via the Degradation of Transferrin Receptor 1 and Prolyl-Hydroxylase-Domain-Containing Protein 3 mRNAs

Cell Rep. 2017 May 23;19(8):1614-1630. doi: 10.1016/j.celrep.2017.05.009.

Abstract

Iron metabolism is regulated by transcriptional and post-transcriptional mechanisms. The mRNA of the iron-controlling gene, transferrin receptor 1 (TfR1), has long been believed to be negatively regulated by a yet-unidentified endonuclease. Here, we show that the endonuclease Regnase-1 is critical for the degradation of mRNAs involved in iron metabolism in vivo. First, we demonstrate that Regnase-1 promotes TfR1 mRNA decay. Next, we show that Regnase-1-/- mice suffer from severe iron deficiency anemia, although hepcidin expression is downregulated. The iron deficiency anemia is induced by a defect in duodenal iron uptake. We reveal that duodenal Regnase-1 controls the expression of PHD3, which impairs duodenal iron uptake via HIF2α suppression. Finally, we show that Regnase-1 is a HIF2α-inducible gene and thus provides a positive feedback loop for HIF2α activation via PHD3. Collectively, these results demonstrate that Regnase-1-mediated regulation of iron-related transcripts is essential for the maintenance of iron homeostasis.

Keywords: HIF2α; anemia; endonuclease; iron metabolism; mRNA degradation; transferrin receptor.

MeSH terms

  • Anemia / metabolism
  • Anemia / pathology
  • Animals
  • Antigens, CD / genetics
  • Antigens, CD / metabolism*
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Duodenum / metabolism
  • Ferritins / metabolism
  • Homeostasis*
  • Iron / metabolism*
  • Mice
  • Procollagen-Proline Dioxygenase / metabolism*
  • Promoter Regions, Genetic / genetics
  • RNA Stability*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, Transferrin / genetics
  • Receptors, Transferrin / metabolism*
  • Response Elements / genetics
  • Ribonucleases / deficiency
  • Ribonucleases / metabolism*
  • Transcription, Genetic

Substances

  • Antigens, CD
  • Basic Helix-Loop-Helix Transcription Factors
  • CD71 antigen
  • RNA, Messenger
  • Receptors, Transferrin
  • endothelial PAS domain-containing protein 1
  • Ferritins
  • Iron
  • PHD3 protein, mouse
  • Procollagen-Proline Dioxygenase
  • Ribonucleases
  • regnase-1, mouse