DNA methylation and chromatin accessibility profiling of mouse and human fetal germ cells

Cell Research

Volumn 27, Issue 2, 2017, Pages 165-183

  Guo, Hongshan ^a   Hu, Boqiang ^a   Yan, Liying ^a,b,c   Yong, Jun ^a,b,c   Wu, Yan ^d   Gao, Yun ^a   Guo, Fan ^a   Hou, Yu ^a   Fan, Xiaoying ^a   Dong, Ji ^a,b,c   Wang, Xiaoye ^a,b,c   Zhu, Xiaohui ^a,b,c   Yan, Jie ^a,b,c   Wei, Yuan ^a,b,c   Jin, Hongyan ^a,b,c   Zhang, Wenxin ^a,b,c   Wen, Lu ^a,b   Tang, Fuchou ^a,b,e   Qiao, Jie ^a,b,c  

^a PEKING UNIVERSITY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c Beijing Key Laboratory of Reproductive Endocrinology and Assisted Reproductive Technology   (China)

^d NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^e Beijing Advanced Innovation Center for Imaging Technology   (China)

Author keywords

chromatin; development; epigenetics; stem cell biology; transcription

Indexed keywords

ANIMAL; ANTIBODY SPECIFICITY; CHROMATIN; CYTOLOGY; DNA METHYLATION; FETUS; GENETICS; GENOME IMPRINTING; GERM CELL; HUMAN; MALE; MAMMAL; METABOLISM; MOUSE; NUCLEAR REPROGRAMMING; NUCLEOSOME; NUCLEOTIDE REPEAT; PROMOTER REGION;

ANIMALS; CELLULAR REPROGRAMMING; CHROMATIN; DNA METHYLATION; FETUS; GENOMIC IMPRINTING; GERM CELLS; HUMANS; MALE; MAMMALS; MICE; NUCLEOSOMES; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC; REPETITIVE SEQUENCES, NUCLEIC ACID;

EID: 84994666754     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2016.128     Document Type: Article

References (57)

1. Lee HJ, Hore TA, Reik W. Reprogramming the methylome: erasing memory and creating diversity. Cell Stem Cell 2014; 14: 710-719
2. Saitou M, Kagiwada S, Kurimoto K. Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 2012; 139: 15-31
3. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002; 16: 6-21
4. Hackett JA, Surani MA. Beyond DNA: programming and inheritance of parental methylomes. Cell 2013; 153: 737-739
5. Guo F, Yan L, Guo H, et al. The transcriptome and DNA methylome landscapes of human primordial germ cells. Cell 2015; 161: 1437-1452
6. Gkountela S, Zhang KX, Shafiq TA, et al. DNA demethylation dynamics in the human prenatal germline. Cell 2015; 161: 1425-1436
7. Tang WW, Dietmann S, Irie N, et al. A unique gene regulatory network resets the human germline epigenome for development. Cell 2015; 161: 1453-1467
8. Lesch BJ, Dokshin GA, Young RA, McCarrey JR, Page DC. A set of genes critical to development is epigenetically poised in mouse germ cells from fetal stages through completion of meiosis. Proc Natl Acad Sci USA 2013; 110: 16061-16066
9. Sachs M, Onodera C, Blaschke K, Ebata KT, Song JS, Ramalho-Santos M. Bivalent chromatin marks developmental regulatory genes in the mouse embryonic germline in vivo. Cell Rep 2013; 3: 1777-1784
10. Ng JH, Kumar V, Muratani M, et al. In vivo epigenomic profiling of germ cells reveals germ cell molecular signatures. Dev Cell 2013; 24: 324-333
11. Saitou M, Miyauchi H. Gametogenesis from pluripotent stem cells. Cell Stem Cell 2016; 18: 721-735
12. Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 2012; 338: 971-975
13. Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 2011; 146: 519-532
14. Zhou Q, Wang M, Yuan Y, et al. Complete meiosis from embryonic stem cell-derived germ cells in vitro. Cell Stem Cell 2016; 18: 330-340
15. Nakaki F, Hayashi K, Ohta H, Kurimoto K, Yabuta Y, Saitou M. Induction of mouse germ-cell fate by transcription factors in vitro. Nature 2013; 501: 222-226
16. Kurimoto K, Yabuta Y, Hayashi K, et al. Quantitative dynamics of chromatin remodeling during germ cell specification from mouse embryonic stem cells. Cell Stem Cell 2015; 16: 517-532
17. Seki Y, Hayashi K, Itoh K, Mizugaki M, Saitou M, Matsui Y. Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev Biol 2005; 278: 440-458
18. Seki Y, Yamaji M, Yabuta Y, et al. Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 2007; 134: 2627-2638
19. Kelly TK, Liu Y, Lay FD, Liang G, Berman BP, Jones PA. Genome-wide mapping of nucleosome positioning and DNA methylation within individual DNA molecules. Genome Res 2012; 22: 2497-2506
20. Taberlay PC, Statham AL, Kelly TK, Clark SJ, Jones PA. Reconfiguration of nucleosome-depleted regions at distal regulatory elements accompanies DNA methylation of enhancers and insulators in cancer. Genome Res 2014; 24: 1421-1432
21. Kobayashi H, Sakurai T, Miura F, et al. High-resolution DNA methylome analysis of primordial germ cells identifies gender-specific reprogramming in mice. Genome Res 2013; 23: 616-627
22. Seisenberger S, Andrews S, Krueger F, et al. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 2012; 48: 849-862
23. Zhang Y, Vastenhouw NL, Feng J, et al. Canonical nucleosome organization at promoters forms during genome activation. Genome Res 2014; 24: 260-266
24. Beh LY, Muller MM, Muir TW, Kaplan N, Landweber LF. DNA-guided establishment of nucleosome patterns within coding regions of a eukaryotic genome. Genome Res 2015; 25: 1727-1738
25. Schones DE, Cui K, Cuddapah S, et al. Dynamic regulation of nucleosome positioning in the human genome. Cell 2008; 132: 887-898
26. Tsui K, Dubuis S, Gebbia M, et al. Evolution of nucleosome occupancy: conservation of global properties and divergence of gene-specific patterns. Mol Cell Biol 2011; 31: 4348-4355
27. Boyle AP, Davis S, Shulha HP, et al. High-resolution mapping and characterization of open chromatin across the genome. Cell 2008; 132: 311-322
28. Shen Y, Yue F, McCleary DF, et al. A map of the cis-regulatory sequences in the mouse genome. Nature 2012; 488: 116-120
29. Heintzman ND, Hon GC, Hawkins RD, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009; 459: 108-112
30. Murakami K, Gunesdogan U, Zylicz JJ, et al. NANOG alone induces germ cells in primed epiblast in vitro by activation of enhancers. Nature 2016; 529: 403-407
31. Irie N, Weinberger L, Tang WW, et al. SOX17 is a critical specifier of human primordial germ cell fate. Cell 2015; 160: 253-268
32. Perrett RM, Turnpenny L, Eckert JJ, et al. The early human germ cell lineage does not express SOX2 during in vivo development or upon in vitro culture. Biol Reprod 2008; 78: 852-858
33. Guo H, Zhu P, Yan L, et al. The DNA methylation landscape of human early embryos. Nature 2014; 511: 606-610
34. Smith ZD, Chan MM, Humm KC, et al. DNA methylation dynamics of the human preimplantation embryo. Nature 2014; 511: 611-615
35. Yan L, Guo H, Hu B, et al. Epigenomic landscape of human fetal brain, heart, and liver. J Biol Chem 2016; 291: 4386-4398
36. Chodavarapu RK, Feng S, Bernatavichute YV, et al. Relationship between nucleosome positioning and DNA methylation. Nature 2010; 466: 388-392
37. Portella G, Battistini F, Orozco M. Understanding the connection between epigenetic DNA methylation and nucleosome positioning from computer simulations. PLoS Comput Biol 2013; 9: e1003354
38. Valouev A, Johnson SM, Boyd SD, Smith CL, Fire AZ, Sidow A. Determinants of nucleosome organization in primary human cells. Nature 2011; 474: 516-520
39. Buenrostro JD, Wu B, Litzenburger UM, et al. Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 2015; 523: 486-490
40. Cusanovich DA, Daza R, Adey A, et al. Multiplex single cell profiling of chromatin accessibility by combinatorial cellular indexing. Science 2015; 348: 910-914
41. Jin W, Tang Q, Wan M, et al. Genome-wide detection of DNase I hypersensitive sites in single cells and FFPE tissue samples. Nature 2015; 528: 142-146
42. Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 2013; 10: 1213-1218
43. De Felici M, Barrios F. Seeking the origin of female germline stem cells in the mammalian ovary. Reproduction 2013; 146: R125-130
44. Guo H, Zhu P, Wu X, Li X, Wen L, Tang F. Single-cell methylome landscapes of mouse embryonic stem cells and early embryos analyzed using reduced representation bisulfite sequencing. Genome Res 2013; 23: 2126-2135
45. Robinson LL, Gaskell TL, Saunders PT, Anderson RA. Germ cell specific expression of c-kit in the human fetal gonad. Mol Hum Reprod 2001; 7: 845-852
46. Miura F, Enomoto Y, Dairiki R, Ito T. Amplification-free whole-genome bisulfite sequencing by post-bisulfite adaptor tagging. Nucleic Acids Res 2012; 40: e136
47. Smallwood SA, Lee HJ, Angermueller C, et al. Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat Methods 2014; 11: 817-820
48. Tang F, Barbacioru C, Wang Y, et al. mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods 2009; 6: 377-382
49. Tang F, Barbacioru C, Nordman E, et al. RNA-Seq analysis to capture the transcriptome landscape of a single cell. Nat Protoc 2010; 5: 516-535
50. Li H, Handsaker B, Wysoker A, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25: 2078-2079
51. Okae H, Chiba H, Hiura H, et al. Genome-wide analysis of DNA methylation dynamics during early human development. PLoS Genet 2014; 10: e1004868
52. Heinz S, Benner C, Spann N, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010; 38: 576-589
53. Huber W, Carey VJ, Gentleman R, et al. Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods 2015; 12: 115-121
54. Gentleman RC, Carey VJ, Bates DM, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5: R80
55. Falcon S, Gentleman R. Using GOstats to test gene lists for GO term association. Bioinformatics 2007; 23: 257-258
56. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10: R25
57. Trapnell C, Roberts A, Goff L, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012; 7: 562-578