Excluding Oct4 from Yamanaka Cocktail Unleashes the Developmental Potential of iPSCs

Cell Stem Cell. 2019 Dec 5;25(6):737-753.e4. doi: 10.1016/j.stem.2019.10.002. Epub 2019 Nov 7.

Abstract

Oct4 is widely considered the most important among the four Yamanaka reprogramming factors. Here, we show that the combination of Sox2, Klf4, and cMyc (SKM) suffices for reprogramming mouse somatic cells to induced pluripotent stem cells (iPSCs). Simultaneous induction of Sox2 and cMyc in fibroblasts triggers immediate retroviral silencing, which explains the discrepancy with previous studies that attempted but failed to generate iPSCs without Oct4 using retroviral vectors. SKM induction could partially activate the pluripotency network, even in Oct4-knockout fibroblasts. Importantly, reprogramming in the absence of exogenous Oct4 results in greatly improved developmental potential of iPSCs, determined by their ability to give rise to all-iPSC mice in the tetraploid complementation assay. Our data suggest that overexpression of Oct4 during reprogramming leads to off-target gene activation during reprogramming and epigenetic aberrations in resulting iPSCs and thereby bear major implications for further development and application of iPSC technology.

Keywords: Klf4; Myc; Oct4; Sox2; Yamanaka cocktail; developmental potential; induced pluripotent stem cells; reprogramming; retroviral silencing; seesaw model of pluripotency; tetraploid complementation; transcription factor.

MeSH terms

  • Animals
  • Cellular Reprogramming / genetics
  • Cellular Reprogramming / physiology
  • HEK293 Cells
  • Humans
  • Induced Pluripotent Stem Cells / cytology*
  • Induced Pluripotent Stem Cells / metabolism*
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism
  • Mice
  • Mice, Knockout
  • Octamer Transcription Factor-3 / genetics
  • Octamer Transcription Factor-3 / metabolism*
  • Polymerase Chain Reaction
  • SOXB1 Transcription Factors / genetics
  • SOXB1 Transcription Factors / metabolism
  • Sequence Analysis, RNA
  • Tetraploidy
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • KLF4 protein, human
  • Klf4 protein, mouse
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors
  • Octamer Transcription Factor-3
  • Pou5f1 protein, mouse
  • SOXB1 Transcription Factors
  • Sox2 protein, mouse
  • Transcription Factors