A High-Content Screen Identifies MicroRNAs That Regulate Liver Repopulation After Injury in Mice

Gastroenterology. 2020 Mar;158(4):1044-1057.e17. doi: 10.1053/j.gastro.2019.11.025. Epub 2019 Nov 20.

Abstract

Background & aims: Liver regeneration is impaired in mice with hepatocyte-specific deficiencies in microRNA (miRNA) processing, but it is not clear which miRNAs regulate this process. We developed a high-throughput screen to identify miRNAs that regulate hepatocyte repopulation after toxic liver injury using fumarylacetoacetate hydrolase-deficient mice.

Methods: We constructed plasmid pools encoding more than 30,000 tough decoy miRNA inhibitors (hairpin nucleic acids designed to specifically inhibit interactions between miRNAs and their targets) to target hepatocyte miRNAs in a pairwise manner. The plasmid libraries were delivered to hepatocytes in fumarylacetoacetate hydrolase-deficient mice at the time of liver injury via hydrodynamic tail-vein injection. Integrated transgene-containing transposons were quantified after liver repopulation via high-throughput sequencing. Changes in polysome-bound transcripts after miRNA inhibition were determined using translating ribosome affinity purification followed by high-throughput sequencing.

Results: Analyses of tough decoy abundance in hepatocyte genomic DNA and input plasmid pools identified several thousand miRNA inhibitors that were significantly depleted or increased after repopulation. We classified a subset of miRNA binding sites as those that have strong effects on liver repopulation, implicating the targeted hepatocyte miRNAs as regulators of this process. We then generated a high-content map of pairwise interactions between 171 miRNA-binding sites and identified synergistic and redundant effects.

Conclusions: We developed a screen to identify miRNAs that regulate liver repopulation after injury in live mice.

Keywords: Genetic Screen; Post-Transcriptional Regulation; Tough decoy; microRNA.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Chromosome Mapping
  • Hepatocytes / physiology
  • High-Throughput Nucleotide Sequencing / methods*
  • Hydrolases / deficiency
  • Liver / injuries*
  • Liver / physiopathology
  • Liver Regeneration / genetics*
  • Mice
  • MicroRNAs / analysis*
  • MicroRNAs / antagonists & inhibitors
  • Plasmids
  • RNA-Binding Proteins / analysis

Substances

  • MicroRNAs
  • RNA-Binding Proteins
  • Hydrolases
  • fumarylacetoacetase