Context-Dependent Functions of NANOG Phosphorylation in Pluripotency and Reprogramming

Stem Cell Reports. 2017 May 9;8(5):1115-1123. doi: 10.1016/j.stemcr.2017.03.023. Epub 2017 Apr 27.

Abstract

The core pluripotency transcription factor NANOG is critical for embryonic stem cell (ESC) self-renewal and somatic cell reprogramming. Although NANOG is phosphorylated at multiple residues, the role of NANOG phosphorylation in ESC self-renewal is incompletely understood, and no information exists regarding its functions during reprogramming. Here we report our findings that NANOG phosphorylation is beneficial, although nonessential, for ESC self-renewal, and that loss of phosphorylation enhances NANOG activity in reprogramming. Mutation of serine 65 in NANOG to alanine (S65A) alone has the most significant impact on increasing NANOG reprogramming capacity. Mechanistically, we find that pluripotency regulators (ESRRB, OCT4, SALL4, DAX1, and TET1) are transcriptionally primed and preferentially associated with NANOG S65A at the protein level due to presumed structural alterations in the N-terminal domain of NANOG. These results demonstrate that a single phosphorylation site serves as a critical interface for controlling context-dependent NANOG functions in pluripotency and reprogramming.

Keywords: iPSC; phospho-NANOG; pluripotency; post-translational modification; reprogramming; self-renewal; serine to alanine mutation.

Publication types

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

MeSH terms

  • Animals
  • Cell Line
  • Cells, Cultured
  • Cellular Reprogramming*
  • DAX-1 Orphan Nuclear Receptor / metabolism
  • DNA-Binding Proteins / metabolism
  • Embryonic Stem Cells / cytology*
  • Embryonic Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / cytology*
  • Induced Pluripotent Stem Cells / metabolism
  • Mice
  • Mutation, Missense*
  • Nanog Homeobox Protein / chemistry
  • Nanog Homeobox Protein / genetics
  • Nanog Homeobox Protein / metabolism*
  • Octamer Transcription Factor-3 / metabolism
  • Phosphorylation
  • Protein Domains
  • Protein Processing, Post-Translational*
  • Proto-Oncogene Proteins / metabolism
  • Receptors, Estrogen / metabolism
  • Transcription Factors / metabolism

Substances

  • DAX-1 Orphan Nuclear Receptor
  • DNA-Binding Proteins
  • Esrrb protein, mouse
  • Nanog Homeobox Protein
  • Nanog protein, mouse
  • Nr0b1 protein, mouse
  • Octamer Transcription Factor-3
  • Pou5f1 protein, mouse
  • Proto-Oncogene Proteins
  • Receptors, Estrogen
  • Sall4 protein, mouse
  • TET1 protein, mouse
  • Transcription Factors