Zfp296 negatively regulates H3K9 methylation in embryonic development as a component of heterochromatin

Sci Rep. 2017 Sep 29;7(1):12462. doi: 10.1038/s41598-017-12772-y.

Abstract

The Cys2/His2-type zinc finger protein Zfp296 has been implicated in stem cell pluripotency and tumor pathogenesis. However, its mechanisms remain elusive. Here, we demonstrated that a Zfp296 deficiency in mice impairs germ-cell development and embryonic growth. Zfp296 was intracellularly localized to heterochromatin in embryos. A GST-Zfp296 pull-down experiment using ES cell nuclear extract followed by LC-MS/MS showed that Zfp296 interacts with component proteins of heterochromatin (such as HP1, Dnmt1, Dnmt3b, and ATRX) and the NuRD complex. We focused on H3K9 methylation as a hallmark of heterochromatin, and found that Zfp296 overexpression in cultured cells reduces the Suv39h1-mediated H3K9 methylation. Consistent with this finding, in Zfp296 -/- mouse embryos, we observed a global increase in H3K9 methylation in a developmental stage-dependent manner, and showed, by ChIP-qPCR, that the H3K9me3 levels at major satellite repeats were elevated in Zfp296 -/- embryos. Our results demonstrate that Zfp296 is a component of heterochromatin that affects embryonic development by negatively regulating H3K9 methylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation
  • Chromobox Protein Homolog 5
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism
  • DNA (Cytosine-5-)-Methyltransferase 1 / genetics
  • DNA (Cytosine-5-)-Methyltransferase 1 / metabolism
  • DNA (Cytosine-5-)-Methyltransferases / genetics
  • DNA (Cytosine-5-)-Methyltransferases / metabolism
  • DNA Methyltransferase 3B
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics*
  • Embryo, Mammalian
  • Embryonic Development / genetics*
  • Female
  • Gene Expression Regulation, Developmental
  • Heterochromatin / chemistry
  • Heterochromatin / metabolism*
  • Histones / genetics
  • Histones / metabolism*
  • Male
  • Methylation
  • Methyltransferases / genetics
  • Methyltransferases / metabolism
  • Mice
  • Mice, Knockout
  • Mouse Embryonic Stem Cells / cytology
  • Mouse Embryonic Stem Cells / metabolism*
  • Ovary / abnormalities
  • Ovary / growth & development
  • Ovary / metabolism
  • Primary Cell Culture
  • Protein Processing, Post-Translational*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Testis / abnormalities
  • Testis / growth & development
  • Testis / metabolism
  • X-linked Nuclear Protein / genetics
  • X-linked Nuclear Protein / metabolism

Substances

  • Chromosomal Proteins, Non-Histone
  • DNA-Binding Proteins
  • Heterochromatin
  • Histones
  • RNA, Messenger
  • Repressor Proteins
  • zinc finger protein 296, mouse
  • Chromobox Protein Homolog 5
  • Suv39h1 protein, mouse
  • Methyltransferases
  • DNA (Cytosine-5-)-Methyltransferase 1
  • DNA (Cytosine-5-)-Methyltransferases
  • Dnmt1 protein, mouse
  • Atrx protein, mouse
  • X-linked Nuclear Protein