Developmentally Programmed Tankyrase Activity Upregulates β-Catenin and Licenses Progression of Embryonic Genome Activation

Dev Cell. 2020 Jun 8;53(5):545-560.e7. doi: 10.1016/j.devcel.2020.04.018. Epub 2020 May 21.

Abstract

Embryonic genome activation (EGA) is orchestrated by an intrinsic developmental program initiated during oocyte maturation with translation of stored maternal mRNAs. Here, we show that tankyrase, a poly(ADP-ribosyl) polymerase that regulates β-catenin levels, undergoes programmed translation during oocyte maturation and serves an essential role in mouse EGA. Newly translated TNKS triggers proteasomal degradation of axin, reducing targeted destruction of β-catenin and promoting β-catenin-mediated transcription of target genes, including Myc. MYC mediates ribosomal RNA transcription in 2-cell embryos, supporting global protein synthesis. Suppression of tankyrase activity using knockdown or chemical inhibition causes loss of nuclear β-catenin and global reductions in transcription and histone H3 acetylation. Chromatin and transcriptional profiling indicate that development arrests prior to the mid-2-cell stage, mediated in part by reductions in β-catenin and MYC. These findings indicate that post-transcriptional regulation of tankyrase serves as a ligand-independent developmental mechanism for post-translational β-catenin activation and is required to complete EGA.

Keywords: ATAC-seq; WNT signaling pathway; axin; embryonic genome activation; mouse; post-transcriptional regulation; preimplantation embryo; tankyrase; β-catenin.

Publication types

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

MeSH terms

  • Animals
  • Blastocyst / cytology
  • Blastocyst / metabolism*
  • Gene Expression Regulation, Developmental*
  • Histones / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mouse Embryonic Stem Cells / cytology
  • Mouse Embryonic Stem Cells / metabolism
  • Oocytes / cytology
  • Oocytes / metabolism
  • Proto-Oncogene Proteins c-myc / metabolism
  • RNA, Ribosomal / genetics
  • RNA, Ribosomal / metabolism
  • Tankyrases / genetics
  • Tankyrases / metabolism*
  • Up-Regulation
  • beta Catenin / genetics*
  • beta Catenin / metabolism

Substances

  • Histones
  • Myc protein, mouse
  • Proto-Oncogene Proteins c-myc
  • RNA, Ribosomal
  • beta Catenin
  • Tankyrases
  • Tnks protein, mouse
  • tankyrase-2, mouse