Maternal H3K27me3 controls DNA methylation-independent imprinting

Nature

Volumn 547, Issue 7664, 2017, Pages 419-424

  Inoue, Azusa ^a   Jiang, Lan ^a   Lu, Falong ^a,d   Suzuki, Tsukasa ^a   Zhang, Yi ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE H3; LYSINE; DEOXYRIBONUCLEASE I; HISTONE;

ALLELE; CELLS AND CELL COMPONENTS; DNA; EMBRYO; ENZYME; ENZYME ACTIVITY; GENE EXPRESSION; GENOME; METHYLATION; PROTEIN; SPERM;

ALLELE; ANIMAL CELL; ARTICLE; BLASTOCYST; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; FEMALE; GENE EXPRESSION; GENOME IMPRINTING; HISTONE METHYLATION; HUMAN; MOUSE; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROMOTER REGION; ANIMAL; CELL LINEAGE; CHEMISTRY; CHROMATIN; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; MALE; MAMMALIAN EMBRYO; METABOLISM; MORULA; OOCYTE; ZYGOTE;

MAMMALIA;

ALLELES; ANIMALS; BLASTOCYST; CELL LINEAGE; CHROMATIN; DEOXYRIBONUCLEASE I; DNA; DNA METHYLATION; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION; GENOMIC IMPRINTING; HISTONES; LYSINE; MALE; MICE; MORULA; OOCYTES; ZYGOTE;

EID: 85026357924     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature23262     Document Type: Article

References (52)

1. Burton, A. & Torres-Padilla, M. E. Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis. Nat. Rev. Mol. Cell Biol. 15, 723-735 (2014).
2. Inoue, A. & Zhang, Y. Nucleosome assembly is required for nuclear pore complex assembly in mouse zygotes. Nat. Struct. Mol. Biol. 21, 609-616 (2014).
3. Zhou, L. Q. & Dean, J. Reprogramming the genome to totipotency in mouse embryos. Trends Cell Biol. 25, 82-91 (2015).
4. Ferguson-Smith, A. C. Genomic imprinting: the emergence of an epigenetic paradigm. Nat. Rev. Genet. 12, 565-575 (2011).
5. Boyle, A. P. et al. High-resolution mapping and characterization of open chromatin across the genome. Cell 132, 311-322 (2008).
6. Stergachis, A. B. et al. Developmental fate and cellular maturity encoded in human regulatory DNA landscapes. Cell 154, 888-903 (2013).
7. Lu, F. et al. Establishing chromatin regulatory landscape during mouse preimplantation development. Cell 165, 1375-1388 (2016).
8. Wu, J. et al. The landscape of accessible chromatin in mammalian preimplantation embryos. Nature 534, 652-657 (2016).
9. Kobayashi, H. et al. Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 8, e1002440 (2012).
10. Deaton, A. M. & Bird, A. CpG islands and the regulation of transcription. Genes Dev. 25, 1010-1022 (2011).
11. Zheng, H. et al. Resetting epigenetic memory by reprogramming of histone modifications in mammals. Mol. Cell 63, 1066-1079 (2016).
12. Agger, K. et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449, 731-734 (2007).
13. Matoba, S. et al. Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell 159, 884-895 (2014).
14. Borensztein, M. et al. Xist-dependent imprinted X inactivation and the early developmental consequences of its failure. Nat. Struct. Mol. Biol. 24, 226-233 (2017).
15. Okae, H. et al. Re-investigation and RNA sequencing-based identification of genes with placenta-specific imprinted expression. Hum. Mol. Genet. 21, 548-558 (2012).
16. Okae, H. et al. RNA sequencing-based identification of aberrant imprinting in cloned mice. Hum. Mol. Genet. 23, 992-1001 (2014).
17. Varmuza, S. & Miri, K. What does genetics tell us about imprinting and the placenta connection? Cell. Mol. Life Sci. 72, 51-72 (2015).
18. Wang, X., Soloway, P. D. & Clark, A. G. A survey for novel imprinted genes in the mouse placenta by mRNA-seq. Genetics 189, 109-122 (2011).
19. Babak, T. et al. Genetic conflict reflected in tissue-specific maps of genomic imprinting in human and mouse. Nat. Genet. 47, 544-549 (2015).
20. Kuzmin, A. et al. The PcG gene Sfmbt2 is paternally expressed in extraembryonic tissues. Gene Expr. Patterns 8, 107-116 (2008).
21. Blakeley, P. et al. Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development 142, 3151-3165 (2015).
22. Bartolomei, M. S., Webber, A. L., Brunkow, M. E. & Tilghman, S. M. Epigenetic mechanisms underlying the imprinting of the mouse H19 gene. Genes Dev. 7, 1663-1673 (1993).
23. Ferguson-Smith, A. C., Sasaki, H., Cattanach, B. M. & Surani, M. A. Parentalorigin- specific epigenetic modification of the mouse H19 gene. Nature 362, 751-755 (1993).
24. Stöger, R. et al. Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell 73, 61-71 (1993).
25. Mager, J., Montgomery, N. D., de Villena, F. P.-M. & Magnuson, T. Genome imprinting regulated by the mouse Polycomb group protein Eed. Nat. Genet. 33, 502-507 (2003).
26. Lewis, A. et al. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat. Genet. 36, 1291-1295 (2004).
27. Umlauf, D. et al. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat. Genet. 36, 1296-1300 (2004).
28. Terranova, R. et al. Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos. Dev. Cell 15, 668-679 (2008).
29. Pandey, R. R. et al. Kcnq1ot1 antisense noncoding RNA mediates lineagespecific transcriptional silencing through chromatin-level regulation. Mol. Cell 32, 232-246 (2008).
30. Yamasaki-Ishizaki, Y. et al. Role of DNA methylation and histone H3 lysine 27 methylation in tissue-specific imprinting of mouse Grb10. Mol. Cell. Biol. 27, 732-742 (2007).
31. Sanz, L. A. et al. A mono-allelic bivalent chromatin domain controls tissuespecific imprinting at Grb10. EMBO J. 27, 2523-2532 (2008).
32. Duffié, R. et al. The Gpr1/Zdbf2 locus provides new paradigms for transient and dynamic genomic imprinting in mammals. Genes Dev. 28, 463-478 (2014).
33. Monk, D. et al. Comparative analysis of human chromosome 7q21 and mouse proximal chromosome 6 reveals a placental-specific imprinted gene, TFPI2/Tfpi2, which requires EHMT2 and EED for allelic-silencing. Genome Res. 18, 1270-1281 (2008).
34. Henckel, A. et al. Histone methylation is mechanistically linked to DNA methylation at imprinting control regions in mammals. Hum. Mol. Genet. 18, 3375-3383 (2009).
35. Kobayashi, H. et al. Imprinted DNA methylation reprogramming during early mouse embryogenesis at the Gpr1-Zdbf2 locus is linked to long cis-intergenic transcription. FEBS Lett. 586, 827-833 (2012).
36. Saitou, M., Kagiwada, S. & Kurimoto, K. Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 139, 15-31 (2012).
37. Pires, N. D. & Grossniklaus, U. Different yet similar: evolution of imprinting in flowering plants and mammals. F1000Prime Rep. 6, 63 (2014).
38. Moreno-Romero, J., Jiang, H., Santos-González, J. & Köhler, C. Parental epigenetic asymmetry of PRC2-mediated histone modifications in the Arabidopsis endosperm. EMBO J. 35, 1298-1311 (2016).
39. Inoue, A., Nakajima, R., Nagata, M. & Aoki, F. Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice. Hum. Reprod. 23, 1377-1384 (2008).
40. Ohnishi, Y. et al. Small RNA class transition from siRNA/piRNA to miRNA during pre-implantation mouse development. Nucleic Acids Res. 38, 5141-5151 (2010).
41. Inoue, A., Akiyama, T., Nagata, M. & Aoki, F. The perivitelline space-forming capacity of mouse oocytes is associated with meiotic competence. J. Reprod. Dev. 53, 1043-1052 (2007).
42. Sugimoto, M. et al. A simple and robust method for establishing homogeneous mouse epiblast stem cell lines by Wnt inhibition. Stem Cell Reports 4, 744-757 (2015).
43. Xiang, Y. et al. JMJD3 is a histone H3K27 demethylase. Cell Res. 17, 850-857 (2007).
44. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
45. John, S. et al. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat. Genet. 43, 264-268 (2011).
46. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
47. Ramírez, F. et al. deepTools2: a next generation web server for deepsequencing data analysis. Nucleic Acids Res. 44 (W1), W160-W165 (2016).
48. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
49. Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923-930 (2014).
50. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
51. Song, Q. et al. A reference methylome database and analysis pipeline to facilitate integrative and comparative epigenomics. PLoS ONE 8, e81148 (2013).
52. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).