Sfmbt2 10th intron-hosted miR-466(a/e)-3p are important epigenetic regulators of Nfat5 signaling, osmoregulation and urine concentration in mice

Biochim Biophys Acta. 2014 Feb;1839(2):97-106. doi: 10.1016/j.bbagrm.2013.12.005. Epub 2014 Jan 3.

Abstract

Sfmbt2-hosted miR-466a-3p and its close relatives are often among the most significantly up-regulated or down-regulated miRNAs in responses to numerous deleterious environmental stimuli. The exact roles of these miRNAs in cellular stress responses, however, are not clear. Here we showed that many Sfmbt2-hosted miRNAs were highly hypertonic stress responsive in vitro and in vivo. In renal medulla, water deprivation induced alterations in the expression of miR-466(a/b/c/e/p)-3p in a pattern similar to that of miR-200b-3p, a known regulator of osmoresponsive transcription factor Nfat5. Remarkably, exposure of mIMCD3 cells to an arginine vasopressin analog time-dependently down-regulated the expression of miR-466(a/b/c/e/p)-3p and miR-200b-3p, which provides a novel regulatory mechanism for these osmoresponsive miRNAs. In cultured mIMCD3 cells we further demonstrated that miR-466a-3p and miR-466g were capable of targeting Nfat5 by interacting with its 3'UTR. In transgenic mice overexpressing miR-466a-3p, significant down-regulation of Nfat5 and many other osmoregulation-related genes was observed in both the renal cortex and medulla. Moreover, sustained transgenic over-expression of miR-466a-3p was found to be associated with polydipsia, polyuria and disturbed ion homeostasis and kidney morphology. Since the mature sequence of miR-466a-3p is completely equivalent to that of miR-466e-3p and that the seed sequence of miR-466a-3p is completely equivalent to that of miR-297(a/b/c)-3p, miR-466d-3p, miR-467g and miR-669d-3p, and that miR-466a-3p differs from miR-466(b/c/p)-3p only in a 5' nucleotide, we propose that miR-466a-3p and many of its close relatives are important epigenetic regulators of renal Nfat5 signaling, osmoregulation and urine concentration in mice.

Keywords: Nfat5/OREBP/TonEBP; Osmoregulation; Sfmbt2 10th intron-hosted miRNA cluster (C2MC); Urine concentration; Vasopressin; miR-466a-3p.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions / genetics
  • Animals
  • Arginine Vasopressin / analogs & derivatives
  • Arginine Vasopressin / pharmacology
  • Base Sequence
  • Blotting, Western
  • Cell Line
  • Creatine / blood
  • Creatine / urine
  • Epigenesis, Genetic
  • Gene Expression / drug effects
  • Introns / genetics*
  • Kidney Concentrating Ability / genetics*
  • Kidney Cortex / metabolism
  • Kidney Medulla / metabolism
  • Mice
  • Mice, Transgenic
  • MicroRNAs / genetics*
  • NFATC Transcription Factors / genetics*
  • NFATC Transcription Factors / metabolism
  • Osmoregulation / genetics*
  • Potassium / blood
  • Potassium / urine
  • Repressor Proteins
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Homology, Nucleic Acid
  • Signal Transduction / genetics
  • Sodium / blood
  • Sodium / urine
  • Transcription Factors / genetics*
  • Urea / blood
  • Urea / urine

Substances

  • 3' Untranslated Regions
  • MicroRNAs
  • Mirn466 microRNA, mouse
  • NFATC Transcription Factors
  • Repressor Proteins
  • Sfmbt2 protein, mouse
  • Transcription Factors
  • Arginine Vasopressin
  • Urea
  • Sodium
  • Creatine
  • Potassium