Small RNA Sequencing Reveals Dlk1-Dio3 Locus-Embedded MicroRNAs as Major Drivers of Ground-State Pluripotency

Stem Cell Reports. 2017 Dec 12;9(6):2081-2096. doi: 10.1016/j.stemcr.2017.10.009. Epub 2017 Nov 9.

Abstract

Ground-state pluripotency is a cell state in which pluripotency is established and maintained through efficient repression of endogenous differentiation pathways. Self-renewal and pluripotency of embryonic stem cells (ESCs) are influenced by ESC-associated microRNAs (miRNAs). Here, we provide a comprehensive assessment of the "miRNome" of ESCs cultured under conditions favoring ground-state pluripotency. We found that ground-state ESCs express a distinct set of miRNAs compared with ESCs grown in serum. Interestingly, most "ground-state miRNAs" are encoded by an imprinted region on chromosome 12 within the Dlk1-Dio3 locus. Functional analysis revealed that ground-state miRNAs embedded in the Dlk1-Dio3 locus (miR-541-5p, miR-410-3p, and miR-381-3p) promoted pluripotency via inhibition of multi-lineage differentiation and stimulation of self-renewal. Overall, our results demonstrate that ground-state pluripotency is associated with a unique miRNA signature, which supports ground-state self-renewal by suppressing differentiation.

Keywords: Dlk1-Dio3 locus; Sfmbt2 locus; differentiation; ground-state pluripotency; microRNA; self-renewal; small RNA sequencing.

MeSH terms

  • Animals
  • Calcium-Binding Proteins
  • Cell Differentiation / genetics
  • Cell Lineage / genetics
  • Cell Self Renewal / genetics
  • Cells, Cultured
  • Embryonic Stem Cells / cytology
  • Embryonic Stem Cells / metabolism
  • Humans
  • Intercellular Signaling Peptides and Proteins / genetics*
  • Iodide Peroxidase / genetics*
  • Mice
  • MicroRNAs / genetics*
  • Pluripotent Stem Cells / cytology
  • Pluripotent Stem Cells / metabolism*
  • Repressor Proteins
  • Sequence Analysis, RNA
  • Transcription Factors

Substances

  • Calcium-Binding Proteins
  • Dlk1 protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • MicroRNAs
  • Repressor Proteins
  • Sfmbt2 protein, mouse
  • Transcription Factors
  • iodothyronine deiodinase type III
  • Iodide Peroxidase