Intracellular Ca2+ Homeostasis and Nuclear Export Mediate Exit from Naive Pluripotency

Cell Stem Cell. 2019 Aug 1;25(2):210-224.e6. doi: 10.1016/j.stem.2019.04.015. Epub 2019 May 16.

Abstract

Progression through states of pluripotency is required for cells in early mammalian embryos to transition away from heightened self-renewal and toward competency for lineage specification. Here, we use a CRISPR mutagenesis screen in mouse embryonic stem cells (ESCs) to identify unexpected roles for nuclear export and intracellular Ca2+ homeostasis during the exit out of the naive state of pluripotency. Mutation of a plasma membrane Ca2+ pump encoded by Atp2b1 increased intracellular Ca2+ such that it overcame effects of intracellular Ca2+ reduction, which is required for naive exit. Persistent self-renewal of ESCs was supported both in Atp2b1-/-Tcf7l1-/- double-knockout ESCs passaged in defined media alone (no LIF or inhibitors) and in wild-type cells passaged in media containing only calcitonin and a GSK3 inhibitor. These new findings suggest a central role for intracellular Ca2+ in safeguarding naive pluripotency.

Keywords: Atp2b1; CRISPR; Ranbp3; Tcf7l1; calcitonin; calcium; embryonic stem cell; nuclear export; pluripotency; self-renewal.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus
  • Animals
  • Calcium Signaling / physiology*
  • Cell Differentiation
  • Cell Lineage
  • Cell Self Renewal / genetics
  • Clustered Regularly Interspaced Short Palindromic Repeats
  • Glycogen Synthase Kinase 3 / metabolism
  • Homeostasis
  • Intracellular Space / metabolism*
  • Mice
  • Mice, Knockout
  • Mouse Embryonic Stem Cells / physiology*
  • Nuclear Proteins / metabolism
  • Plasma Membrane Calcium-Transporting ATPases / genetics
  • Plasma Membrane Calcium-Transporting ATPases / metabolism*
  • Pluripotent Stem Cells / physiology*
  • Transcription Factor 7-Like 1 Protein / genetics
  • Transcription Factor 7-Like 1 Protein / metabolism*

Substances

  • Nuclear Proteins
  • Tcf7l1 protein, mouse
  • Transcription Factor 7-Like 1 Protein
  • ran-binding protein 1
  • Glycogen Synthase Kinase 3
  • Plasma Membrane Calcium-Transporting ATPases
  • Atp2b1 protein, mouse