A hidden threshold in motor neuron gene networks revealed by modulation of miR-218 dose

Neuron. 2021 Oct 20;109(20):3252-3267.e6. doi: 10.1016/j.neuron.2021.07.028. Epub 2021 Aug 26.

Abstract

Disruption of homeostatic microRNA (miRNA) expression levels is known to cause human neuropathology. However, the gene regulatory and phenotypic effects of altering a miRNA's in vivo abundance (rather than its binary gain or loss) are not well understood. By genetic combination, we generated an allelic series of mice expressing varying levels of miR-218, a motor neuron-selective gene regulator associated with motor neuron disease. Titration of miR-218 cellular dose unexpectedly revealed complex, non-ratiometric target mRNA dose responses and distinct gene network outputs. A non-linearly responsive regulon exhibited a steep miR-218 dose-dependent threshold in repression that, when crossed, resulted in severe motor neuron synaptic failure and death. This work demonstrates that a miRNA can govern distinct gene network outputs at different expression levels and that miRNA-dependent phenotypes emerge at particular dose ranges because of hidden regulatory inflection points of their underlying gene networks.

Keywords: amyotrophic lateral sclerosis; gene dosage; gene networks; haploinsufficiency; microRNA-218; motoneuron; neurodevelopment; neuromuscular junction; neuropathology; single cell RNA sequencing.

Publication types

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

MeSH terms

  • Animals
  • Gene Dosage*
  • Gene Regulatory Networks / genetics*
  • Mice
  • Mice, Knockout
  • MicroRNAs / genetics*
  • Motor Neuron Disease / genetics*
  • Motor Neurons / metabolism*
  • Sequence Analysis, RNA
  • Single-Cell Analysis

Substances

  • MIRN218 microRNA, mouse
  • MicroRNAs