Opposing roles of miR-294 and MBNL1/2 in shaping the gene regulatory network of embryonic stem cells

EMBO Rep. 2018 Jun;19(6):e45657. doi: 10.15252/embr.201745657. Epub 2018 May 7.

Abstract

Alternative pre-mRNA splicing plays important roles in regulating self-renewal and differentiation of embryonic stem cells (ESCs). However, how specific alternative splicing programs are established in ESCs remains elusive. Here, we show that a subset of alternative splicing events in ESCs is dependent on miR-294 expression. Remarkably, roughly 60% of these splicing events are affected by the depletion of Muscleblind-Like Splicing Regulator 1 and 2 (Mbnl1/2). Distinct from canonical miRNA function, miR-294 represses Mbnl1/2 through both posttranscriptional and epigenetic mechanisms. Furthermore, we uncover non-canonical functions of MBNL proteins that bind and promote the expression of miR-294 targets, including Cdkn1a and Tgfbr2, thereby opposing the role of miR-294 in regulating cell proliferation, apoptosis, and epithelial-mesenchymal transition (EMT). Our study reveals extensive interactions between miRNAs and splicing factors, highlighting their roles in regulating cell type-specific alternative splicing and defining gene expression programs during development and cellular differentiation.

Keywords: alternative splicing; embryonic stem cells; miR‐290; muscleblind‐like proteins; posttranscriptional regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing
  • Animals
  • Apoptosis / genetics
  • Cell Line
  • Cell Proliferation / genetics
  • DNA-Binding Proteins / physiology*
  • Embryonic Stem Cells / physiology*
  • Epithelial-Mesenchymal Transition / genetics
  • Gene Expression Regulation, Developmental
  • Gene Regulatory Networks
  • MicroRNAs / genetics
  • MicroRNAs / physiology*
  • RNA-Binding Proteins / physiology*

Substances

  • DNA-Binding Proteins
  • MIRN294 microRNA, mouse
  • Mbnl1 protein, mouse
  • Mbnl2 protein, mouse
  • MicroRNAs
  • RNA-Binding Proteins