Imprinted Maternally Expressed microRNAs Antagonize Paternally Driven Gene Programs in Neurons

Mol Cell. 2020 Apr 2;78(1):85-95.e8. doi: 10.1016/j.molcel.2020.01.020. Epub 2020 Feb 6.

Abstract

Imprinted genes with parental-biased allelic expression are frequently co-regulated and enriched in common biological pathways. Here, we functionally characterize a large cluster of microRNAs (miRNAs) expressed from the maternally inherited allele ("maternally expressed") to explore the molecular and cellular consequences of imprinted miRNA activity. Using an induced neuron (iN) culture system, we show that maternally expressed miRNAs from the miR-379/410 cluster direct the RNA-induced silencing complex (RISC) to transcriptional and developmental regulators, including paternally expressed transcripts like Plagl1. Maternal deletion of this imprinted miRNA cluster resulted in increased protein levels of several targets and upregulation of a broader transcriptional program regulating synaptic transmission and neuronal function. A subset of the transcriptional changes resulting from miR-379/410 deletion can be attributed to de-repression of Plagl1. These data suggest maternally expressed miRNAs antagonize paternally driven gene programs in neurons.

Keywords: genomic imprinting; induced neuron; miR-379/410; microRNA; neuron differentiation; non-coding RNA.

Publication types

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

MeSH terms

  • Animals
  • Argonaute Proteins / metabolism
  • Cell Line
  • Cells, Cultured
  • Embryonic Stem Cells / metabolism
  • Excitatory Postsynaptic Potentials
  • Gene Deletion
  • Genomic Imprinting*
  • Mice
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Neurogenesis / genetics
  • Neurons / metabolism*
  • Neurons / physiology
  • RNA-Induced Silencing Complex / metabolism
  • Synaptic Transmission / genetics
  • Transcription, Genetic

Substances

  • Ago2 protein, mouse
  • Argonaute Proteins
  • MIRN379 microRNA, mouse
  • MIRN410 microRNA, mouse
  • MicroRNAs
  • RNA-Induced Silencing Complex