The role of maternal-specific H3K9me3 modification in establishing imprinted X-chromosome inactivation and embryogenesis in mice

Nature Communications

Volumn 5, Issue , 2014, Pages

  Fukuda, Atsushi ^a   Tomikawa, Junko ^a   Miura, Takumi ^a   Hata, Kenichiro ^a   Nakabayashi, Kazuhiko ^a   Eggan, Kevin ^b,c   Akutsu, Hidenori ^a   Umezawa, Akihiro ^a  

^a NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Harvard University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL DEVELOPMENT; CHROMOSOME; EMBRYO; GENE EXPRESSION; GERM CELL;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO DEVELOPMENT; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENOME IMPRINTING; HISTONE MODIFICATION; IMMUNOFLUORESCENCE; IN VITRO STUDY; MESSENGER RNA SYNTHESIS; MOUSE; NONHUMAN; PREIMPLANTATION EMBRYO; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; X CHROMOSOME INACTIVATION; ZYGOTE; ANIMAL; BLASTOCYST; CHROMATIN; MALE; METABOLISM; PHYSIOLOGY;

MUS;

CHROMATIN; HISTONE DEMETHYLASE; KDM3A PROTEIN, MOUSE; KDM4B PROTEIN, MOUSE; LONG UNTRANSLATED RNA; RLIM PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE; XIST NON-CODING RNA;

ANIMALS; BLASTOCYST; CHROMATIN; EMBRYONIC DEVELOPMENT; FEMALE; HISTONE DEMETHYLASES; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MALE; MICE; PROMOTER REGIONS, GENETIC; RNA, LONG NONCODING; UBIQUITIN-PROTEIN LIGASES; X CHROMOSOME INACTIVATION;

EID: 84923309363     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6464     Document Type: Article

References (40)

1. Augui, S., Nora, E. P. & Heard, E. Regulation of X-chromosome inactivation by the X-inactivation centre. Nat. Rev. Genet. 12, 429-442 (2011).
2. Lee, J. T. Gracefully ageing at 50, X-chromosome inactivation becomes a paradigm for RNA and chromatin control. Nat. Rev. Mol. Cell Biol. 12, 815-826 (2011).
3. Wutz, A. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat. Rev. Genet. 12, 542-553 (2011).
4. Takagi, N. & Sasaki, M. Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 256, 640-642 (1975).
5. Shin, J. et al. Maternal Rnf12/RLIM is required for imprinted X-chromosome inactivation in mice. Nature 467, 977-981 (2010).
6. Tada, T. et al. Imprint switching for non-random X-chromosome inactivation during mouse oocyte growth. Development 127, 3101-3105 (2000).
7. Chiba, H. et al. De novo DNA methylation independent establishment of maternal imprint on X chromosome in mouse oocytes. Genesis 46, 768-774 (2008).
8. Marahrens, Y., Panning, B., Dausman, J., Strauss, W. & Jaenisch, R. Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev. 11, 156-166 (1997).
9. Liu, N. et al. Genome-wide gene expression profiling reveals aberrant MAPK and Wnt signaling pathways associated with early parthenogenesis. J. Mol. Cell Biol. 2, 333-344 (2010).
10. Obata, Y. & Kono, T. Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J. Biol. Chem. 277, 5285-5289 (2002).
11. Kono, T. et al. Birth of parthenogenetic mice that can develop to adulthood. Nature 428, 860-864 (2004).
12. Kawahara, M. et al. High-frequency generation of viable mice from engineered bi-maternal embryos. Nat. Biotechnol. 25, 1045-1050 (2007).
13. Santos, F., Peters, A. H., Otte, A. P., Reik, W. & Dean, W. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 280, 225-236 (2005).
14. Cantone, I. & Fisher, A. G. Epigenetic programming and reprogramming during development. Nat. Struct. Mol. Biol. 20, 282-289 (2013).
15. 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).
16. Yuan, P. et al. Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev. 23, 2507-2520 (2009).
17. Fodor, B. D. et al. Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev. 20, 1557-1562 (2006).
18. Nakamura, T. et al. PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 486, 415-419 (2012).
19. Nesterova, T. B., Barton, S. C., Surani, M. A. & Brockdorff, N. Loss of Xist imprinting in diploid parthenogenetic preimplantation embryos. Dev. Biol. 235, 343-350 (2001).
20. Plath, K. et al. Role of histone H3 lysine 27 methylation in X inactivation. Science 300, 131-135 (2003).
21. Okamoto, I., Tan, S. & Takagi, N. X-chromosome inactivation in XX androgenetic mouse embryos surviving implantation. Development 127, 4137-4145 (2000).
22. Barakat, T. S. et al. RNF12 activates Xist and is essential for X chromosome inactivation. PLoS Genet. 7, e1002001 (2011).
23. Puschendorf, M. et al. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 40, 411-420 (2008).
24. Dahl, J. A. & Collas, P. A rapid micro chromatin immunoprecipitation assay (microChIP). Nat. Protoc. 3, 1032-1045 (2008).
25. Turner, B. in Mapping Protein/DNA Interactions by Cross-Linking (2001).
26. Hoki, Y. et al. A proximal conserved repeat in the Xist gene is essential as a genomic element for X-inactivation in mouse. Development 136, 139-146 (2009).
27. Fukuda, A. et al. Identification of inappropriately reprogrammed genes by large-scale transcriptome analysis of individual cloned mouse blastocysts. PLoS ONE 5, e11274 (2010).
28. Inoue, K. et al. Impeding Xist expression from the active X chromosome improves mouse somatic cell nuclear transfer. Science 330, 496-499 (2010).
29. Marks, H. et al. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149, 590-604 (2012).
30. Karimi, M. M. et al. DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8, 676-687 (2011).
31. Ono, Y. & Kono, T. Irreversible barrier to the reprogramming of donor cells in cloning with mouse embryos and embryonic stem cells. Biol. Reprod. 75, 210-216 (2006).
32. Dindot, S. V., Person, R., Strivens, M., Garcia, R. & Beaudet, A. L. Epigenetic profiling at mouse imprinted gene clusters reveals novel epigenetic and genetic features at differentially methylated regions. Genome Res. 19, 1374-1383 (2009).
33. Sasaki, H. & Matsui, Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat. Rev. Genet. 9, 129-140 (2008).
34. Sugimoto, M. & Abe, K. X chromosome reactivation initiates in nascent primordial germ cells in mice. PLoS Genet. 3, e116 (2007).
35. Duszczyk, M. M., Wutz, A., Rybin, V. & Sattler, M. The Xist RNA A-repeat comprises a novel AUCG tetraloop fold and a platform for multimerization. RNA 17, 1973-1982 (2011).
36. Gontan, C. et al. RNF12 initiates X-chromosome inactivation by targeting REX1 for degradation. Nature 485, 386-390 (2012).
37. Zhang, L. et al. RNF12 controls embryonic stem cell fate and morphogenesis in zebrafish embryos by targeting Smad7 for degradation. Mol. Cell 46, 650-661 (2012).
38. Shin, J. et al. RLIM is dispensable for X-chromosome inactivation in the mouse embryonic epiblast. Nature 511, 86-89 (2014).
39. Brykczynska, U. et al. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17, 679-687 (2010).
40. Hammoud, S. S. et al. Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473-478 (2009).