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Genome-Wide Analysis of DNA Methylation Dynamics during Early Human Development


DNA methylation reprogramming after fertilization is critical for normal mammalian development. Early embryos are sensitive to environmental stresses and a number of reports have pointed out the increased risk of DNA methylation errors associated with assisted reproduction technologies. Therefore, it is very important to understand normal DNA methylation patterns during early human development. Recent reduced representation bisulfite sequencing studies reported partial methylomes of human gametes and early embryos. To provide a more comprehensive view of DNA methylation dynamics during early human development, we report on whole genome bisulfite sequencing of human gametes and blastocysts. We show that the paternal genome is globally demethylated in blastocysts whereas the maternal genome is demethylated to a much lesser extent. We also reveal unique regulation of imprinted differentially methylated regions, gene bodies and repeat sequences during early human development. Our high-resolution methylome maps are essential to understand epigenetic reprogramming by human oocytes and will aid in the preimplantation epigenetic diagnosis of human embryos.


Vyšlo v časopise: Genome-Wide Analysis of DNA Methylation Dynamics during Early Human Development. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004868
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004868

Souhrn

DNA methylation reprogramming after fertilization is critical for normal mammalian development. Early embryos are sensitive to environmental stresses and a number of reports have pointed out the increased risk of DNA methylation errors associated with assisted reproduction technologies. Therefore, it is very important to understand normal DNA methylation patterns during early human development. Recent reduced representation bisulfite sequencing studies reported partial methylomes of human gametes and early embryos. To provide a more comprehensive view of DNA methylation dynamics during early human development, we report on whole genome bisulfite sequencing of human gametes and blastocysts. We show that the paternal genome is globally demethylated in blastocysts whereas the maternal genome is demethylated to a much lesser extent. We also reveal unique regulation of imprinted differentially methylated regions, gene bodies and repeat sequences during early human development. Our high-resolution methylome maps are essential to understand epigenetic reprogramming by human oocytes and will aid in the preimplantation epigenetic diagnosis of human embryos.


Zdroje

1. MesserschmidtDM, KnowlesBB, SolterD (2014) DNA methylation dynamics during epigenetic reprogramming in the germline and preimplantation embryos. Genes Dev 28: 812–828.

2. SmithZD, MeissnerA (2013) DNA methylation: roles in mammalian development. Nat Rev Genet 14: 204–220.

3. SaitouM, KagiwadaS, KurimotoK (2012) Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 139: 15–31.

4. SmallwoodSA, TomizawaS, KruegerF, RufN, CarliN, et al. (2011) Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet 43: 811–814.

5. KobayashiH, SakuraiT, ImaiM, TakahashiN, FukudaA, et al. (2012) Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet 8: e1002440.

6. KohliRM, ZhangY (2013) TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502: 472–479.

7. GuoH, ZhuP, YanL, LiR, HuB, et al. (2014) The DNA methylation landscape of human early embryos. Nature 511: 606–610.

8. BeaujeanN, HartshorneG, CavillaJ, TaylorJ, GardnerJ, et al. (2004) Non-conservation of mammalian preimplantation methylation dynamics. Curr Biol 14: R266–267.

9. SmithZD, ChanMM, HummKC, KarnikR, MekhoubadS, et al. (2014) DNA methylation dynamics of the human preimplantation embryo. Nature 511: 611–615.

10. MiuraF, EnomotoY, DairikiR, ItoT (2012) Amplification-free whole-genome bisulfite sequencing by post-bisulfite adaptor tagging. Nucleic Acids Res 40: e136.

11. ShiraneK, TohH, KobayashiH, MiuraF, ChibaH, et al. (2013) Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoS Genet 9: e1003439.

12. WangL, ZhangJ, DuanJ, GaoX, ZhuW, et al. (2014) Programming and inheritance of parental DNA methylomes in mammals. Cell 157: 979–991.

13. MolaroA, HodgesE, FangF, SongQ, McCombieWR, et al. (2011) Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 146: 1029–1041.

14. Al-KhtibM, BlachereT, GuerinJF, LefevreA (2012) Methylation profile of the promoters of Nanog and Oct4 in ICSI human embryos. Hum Reprod 27: 2948–2954.

15. DenommeMM, MannMR (2012) Genomic imprints as a model for the analysis of epigenetic stability during assisted reproductive technologies. Reproduction 144: 393–409.

16. Ferguson-SmithAC (2011) Genomic imprinting: the emergence of an epigenetic paradigm. Nat Rev Genet 12: 565–575.

17. CourtF, TayamaC, RomanelliV, Martin-TrujilloA, Iglesias-PlatasI, et al. (2014) Genome-wide parent-of-origin DNA methylation analysis reveals the intricacies of human imprinting and suggests a germline methylation-independent mechanism of establishment. Genome Res 24: 554–569.

18. LiX, ItoM, ZhouF, YoungsonN, ZuoX, et al. (2008) A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev Cell 15: 547–557.

19. Bourc'hisD, XuGL, LinCS, BollmanB, BestorTH (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294: 2536–2539.

20. HuntrissJ, HinkinsM, OliverB, HarrisSE, BeazleyJC, et al. (2004) Expression of mRNAs for DNA methyltransferases and methyl-CpG-binding proteins in the human female germ line, preimplantation embryos, and embryonic stem cells. Mol Reprod Dev 67: 323–336.

21. SmithZD, ChanMM, MikkelsenTS, GuH, GnirkeA, et al. (2012) A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484: 339–344.

22. WangH, XingJ, GroverD, HedgesDJ, HanK, et al. (2005) SVA elements: a hominid-specific retroposon family. J Mol Biol 354: 994–1007.

23. LaniaL, Di CristofanoA, StrazzulloM, PengueG, MajelloB, et al. (1992) Structural and functional organization of the human endogenous retroviral ERV9 sequences. Virology 191: 464–468.

24. SchuelerMG, SullivanBA (2006) Structural and functional dynamics of human centromeric chromatin. Annu Rev Genomics Hum Genet 7: 301–313.

25. GopalakrishnanS, SullivanBA, TrazziS, Della ValleG, RobertsonKD (2009) DNMT3B interacts with constitutive centromere protein CENP-C to modulate DNA methylation and the histone code at centromeric regions. Hum Mol Genet 18: 3178–3193.

26. XueZ, HuangK, CaiC, CaiL, JiangCY, et al. (2013) Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500: 593–597.

27. KobayashiH, YanagisawaE, SakashitaA, SugawaraN, KumakuraS, et al. (2013) Epigenetic and transcriptional features of the novel human imprinted lncRNA GPR1AS suggest it is a functional ortholog to mouse Zdbf2linc. Epigenetics 8: 635–645.

28. ProudhonC, DuffieR, AjjanS, CowleyM, IranzoJ, et al. (2012) Protection against de novo methylation is instrumental in maintaining parent-of-origin methylation inherited from the gametes. Mol Cell 47: 909–920.

29. HirasawaR, ChibaH, KanedaM, TajimaS, LiE, et al. (2008) Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev 22: 1607–1616.

30. YamagataK, YamazakiT, MikiH, OgonukiN, InoueK, et al. (2007) Centromeric DNA hypomethylation as an epigenetic signature discriminates between germ and somatic cell lineages. Dev Biol 312: 419–426.

31. UedaY, OkanoM, WilliamsC, ChenT, GeorgopoulosK, et al. (2006) Roles for Dnmt3b in mammalian development: a mouse model for the ICF syndrome. Development 133: 1183–1192.

32. HancksDC, KazazianHHJr (2010) SVA retrotransposons: Evolution and genetic instability. Semin Cancer Biol 20: 234–245.

33. ChandlerVL (2010) Paramutation's properties and puzzles. Science 330: 628–629.

34. van MontfoortAP, HanssenLL, de SutterP, VivilleS, GeraedtsJP, et al. (2012) Assisted reproduction treatment and epigenetic inheritance. Hum Reprod Update 18: 171–197.

35. HiuraH, OkaeH, MiyauchiN, SatoF, SatoA, et al. (2012) Characterization of DNA methylation errors in patients with imprinting disorders conceived by assisted reproduction technologies. Hum Reprod 27: 2541–2548.

36. HardyK, HandysideAH, WinstonRM (1989) The human blastocyst: cell number, death and allocation during late preimplantation development in vitro. Development 107: 597–604.

37. UshijimaC, KumasakoY, KihailePE, HirotsuruK, UtsunomiyaT (2000) Analysis of chromosomal abnormalities in human spermatozoa using multi-colour fluorescence in-situ hybridization. Hum Reprod 15: 1107–1111.

38. BahnakBR, WuQY, CoulombelL, DrouetL, Kerbiriou-NabiasD, et al. (1988) A simple and efficient method for isolating high molecular weight DNA from mammalian sperm. Nucleic Acids Res 16: 1208.

39. KruegerF, AndrewsSR (2011) Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27: 1571–1572.

40. Huang daW, ShermanBT, LempickiRA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57.

41. BensonG (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573–580.

42. BaileyTL (2011) DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics 27: 1653–1659.

43. YanL, YangM, GuoH, YangL, WuJ, et al. (2013) Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol 20: 1131–1139.

44. FangF, HodgesE, MolaroA, DeanM, HannonGJ, et al. (2012) Genomic landscape of human allele-specific DNA methylation. Proc Natl Acad Sci U S A 109: 7332–7337.

45. DasR, LeeYK, StrogantsevR, JinS, LimYC, et al. (2013) DNMT1 and AIM1 Imprinting in human placenta revealed through a genome-wide screen for allele-specific DNA methylation. BMC Genomics 14: 685.

Štítky
Genetika Reprodukčná medicína

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PLOS Genetics


2014 Číslo 12
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