PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos.
In eukaryotes, Suv39h H3K9 trimethyltransferases are required for pericentric heterochromatin formation and function. In early mouse preimplantation embryos, however, paternal pericentric heterochromatin lacks Suv39h-mediated H3K9me3 and downstream marks. Here we demonstrate Ezh2-independent targeting of maternally provided polycomb repressive complex 1 (PRC1) components to paternal heterochromatin. In Suv39h2 maternally deficient zygotes, PRC1 also associates with maternal heterochromatin lacking H3K9me3, thereby revealing hierarchy between repressive pathways. In Rnf2 maternally deficient zygotes, the PRC1 complex is disrupted, and levels of pericentric major satellite transcripts are increased at the paternal but not the maternal genome. We conclude that in early embryos, Suv39h-mediated H3K9me3 constitutes the dominant maternal transgenerational signal for pericentric heterochromatin formation. In absence of this signal, PRC1 functions as the default repressive back-up mechanism. Parental epigenetic asymmetry, also observed along cleavage chromosomes, is resolved by the end of the 8-cell stage--concurrent with blastomere polarization--marking the end of the maternal-to-embryonic transition.
Puschendorf
Mareike
M
Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058 Basel, Switzerland.
Terranova
Rémi
R
Boutsma
Erwin
E
Mao
Xiaohong
X
Isono
Kyo-ichi
K
Brykczynska
Urszula
U
Kolb
Carolin
C
Otte
Arie P
AP
Koseki
Haruhiko
H
Orkin
Stuart H
SH
van Lohuizen
Maarten
M
Peters
Antoine H F M
AH
D000818:Animals; D017209:Apoptosis / Q000502:physiology; D001757:Blastomeres / Q000378:metabolism; D004268:DNA-Binding Proteins / Q000235:genetics / Q000502:physiology; D004622:Embryo, Mammalian / Q000378:metabolism* / Q000648:ultrastructure; D047108:Embryonic Development / Q000502:physiology*; D000071221:Enhancer of Zeste Homolog 2 Protein; D005260:Female; D005455:Fluorescent Antibody Technique; D018392:Genomic Imprinting; D006570:Heterochromatin / Q000502:physiology* / Q000648:ultrastructure; D011495:Histone-Lysine N-Methyltransferase / Q000235:genetics / Q000502:physiology; D019426:Integrases / Q000378:metabolism; D008297:Male; D008780:Methyltransferases / Q000502:physiology*; D051379:Mice / Q000196:embryology*; D008810:Mice, Inbred C57BL; D018345:Mice, Knockout; D009865:Oocytes / Q000378:metabolism; D063150:Polycomb Repressive Complex 1; D063151:Polycomb Repressive Complex 2; D063146:Polycomb-Group Proteins; D011506:Proteins / Q000235:genetics / Q000502:physiology; D012097:Repressor Proteins / Q000502:physiology*; D020133:Reverse Transcriptase Polymerase Chain Reaction; D014158:Transcription, Genetic; D019076:Transgenes / Q000502:physiology; D044767:Ubiquitin-Protein Ligases
D004268:DNA-Binding Proteins; D006570:Heterochromatin; D063146:Polycomb-Group Proteins; D011506:Proteins; D012097:Repressor Proteins; C498700:Suv39h1 protein, mouse; D008780:Methyltransferases; D000071221:Enhancer of Zeste Homolog 2 Protein; C498410:Ezh2 protein, mouse; D011495:Histone-Lysine N-Methyltransferase; D063151:Polycomb Repressive Complex 2; D063150:Polycomb Repressive Complex 1; C489842:Rnf2 protein, mouse; D044767:Ubiquitin-Protein Ligases; C045073:Cre recombinase; D019426:Integrases