Simultaneous mapping of active DNA demethylation and sister chromatid exchange in single cells

Genes and Development

Volumn 31, Issue 5, 2017, Pages 511-523

  Wu, Xiaoji ^a,b,c,d   Inoue, Azusa ^a,b,c,d   Suzuki, Tsukasa ^a,b,c,d   Zhang, Yi ^a,b,c,d  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

5 carboxylcytosine; 5 formylcytosine; Low input; Methylase assisted bisulfite sequencing; Single cell; Sister chromatid exchange

Indexed keywords

DNA;

ADULT; ANIMAL CELL; ARTICLE; CELL HETEROGENEITY; CONTROLLED STUDY; DEMETHYLATION; EMBRYO; FEMALE; GENE REARRANGEMENT; GENOME; MALE; MOUSE; NONHUMAN; OXIDATION; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SISTER CHROMATID; SISTER CHROMATID EXCHANGE; ANIMAL; BLASTOMA; CHROMOSOMAL MAPPING; DNA METHYLATION; DNA REPLICATION; GENOMICS; MAMMALIAN EMBRYO; METABOLISM; PROCEDURES; SINGLE CELL ANALYSIS;

ANIMALS; BLASTOMERES; CHROMOSOME MAPPING; DNA METHYLATION; DNA REPLICATION; EMBRYO, MAMMALIAN; GENOMICS; MICE; SINGLE-CELL ANALYSIS; SISTER CHROMATID EXCHANGE;

EID: 85017246672     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.294843.116     Document Type: Article

References (47)

1. Bachman M, Uribe-Lewis S, Yang X, Williams M, Murrell A, Balasubramanian S. 2014. 5-hydroxymethylcytosine is a predominantly stable DNA modification. Nat Chem 6: 1049–1055.
2. Booth MJ, Marsico G, Bachman M, Beraldi D, Balasubramanian S. 2014. Quantitative sequencing of 5-formylcytosine in DNA at single-base resolution. Nat Chem 6: 435–440.
3. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci 107: 21931–21936.
4. Falconer E, Hills M, Naumann U, Poon SS, Chavez EA, Sanders AD, Zhao Y, Hirst M, Lansdorp PM. 2012. DNA template strand sequencing of single-cells maps genomic rearrangements at high resolution. Nat Methods 9: 1107–1112.
5. Farlik M, Sheffield NC, Nuzzo A, Datlinger P, Schonegger A, Klughammer J, Bock C. 2015. Single-cell DNA methylome sequencing and bioinformatic inference of epigenomic cell-state dynamics. Cell Rep 10: 1386–1397.
6. Gu TP, Guo F, Yang H, Wu HP, Xu GF, Liu W, Xie ZG, Shi L, He X, Jin SG, et al. 2011. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477: 606–610.
7. Guo H, Zhu P, Wu X, Li X, Wen L, Tang F. 2013. Single-cell methylome landscapes of mouse embryonic stem cells and early embryos analyzed using reduced representation bisulfite sequencing. Genome Res 23: 2126–2135.
8. Guo F, Li X, Liang D, Li T, Zhu P, Guo H, Wu X, Wen L, Gu TP, Hu B, et al. 2014. Active and passive demethylation of male and female pronuclear DNA in the mammalian zygote. Cell Stem Cell 15: 447–458.
9. Han D, Lu X, Shih AH, Nie J, You Q, Xu MM, Melnick AM, Levine RL, He C. 2016. A highly sensitive and robust method for genome-wide 5hmC profiling of rare cell populations. Mol Cell 63: 711–719.
10. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L, et al. 2011. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333: 1303–1307.
11. Incarnato D, Krepelova A, Neri F. 2014. High-throughput single nucleotide variant discovery in E14 mouse embryonic stem cells provides a new reference genome assembly. Genomics 104: 121–127.
12. Inoue A, Zhang Y. 2011. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334: 194.
13. Inoue A, Shen L, Dai Q, He C, Zhang Y. 2011. Generation and replication-dependent dilution of 5fC and 5caC during mouse preimplantation development. Cell Res 21: 1670–1676.
14. Inoue A, Matoba S, Zhang Y. 2012. Transcriptional activation of transposable elements in mouse zygotes is independent of Tet3-mediated 5-methylcytosine oxidation. Cell Res 22: 1640–1649.
15. Iqbal K, Jin SG, Pfeifer GP, Szabo PE. 2011. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci 108: 3642–3647.
16. Ito S, D’Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. 2010. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466: 1129–1133.
17. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y. 2011. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333: 1300–1303.
18. Jones PA. 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13: 484–492.
19. Keane TM, Goodstadt L, Danecek P, White MA, Wong K, Yalcin B, Heger A, Agam A, Slater G, Goodson M, et al. 2011. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477: 289–294.
20. Krueger F, Andrews SR. 2011. Bismark: a flexible aligner and methylation caller for bisulfite-seq applications. Bioinformatics 27: 1571–1572.
21. Law JA, Jacobsen SE. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204–220.
22. Lu F, Liu Y, Jiang L, Yamaguchi S, Zhang Y. 2014. Role of Tet proteins in enhancer activity and telomere elongation. Genes Dev 28: 2103–2119.
23. Lu X, Han D, Zhao BS, Song CX, Zhang LS, Dore LC, He C. 2015. Base-resolution maps of 5-formylcytosine and 5-carboxylcytosine reveal genome-wide DNA demethylation dynamics. Cell Res 25: 386–389.
24. Lu F, Liu Y, Inoue A, Suzuki T, Zhao K, Zhang Y. 2016. Establishing chromatin regulatory landscape during mouse preimplantation development. Cell 165: 1375–1388.
25. Meissner A, Gnirke A, Bell GW, Ramsahoye B, Lander ES, Jaenisch R. 2005. Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res 33: 5868–5877.
26. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, et al. 2008. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454: 766–770.
27. Miura F, Enomoto Y, Dairiki R, Ito T. 2012. Amplification-free whole-genome bisulfite sequencing by post-bisulfite adaptor tagging. Nucleic Acids Res 40: e136.
28. Mooijman D, Dey SS, Boisset JC, Crosetto N, van Oudenaarden A. 2016. Single-cell 5hmC sequencing reveals chromosome-wide cell-to-cell variability and enables lineage reconstruction. Nat Biotechnol 34: 852–856.
29. O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, Rajput B, Robbertse B, Smith-White B, Ako-Adjei D, et al. 2016. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 44: D733–D745.
30. Raiber EA, Beraldi D, Ficz G, Burgess HE, Branco MR, Murat P, Oxley D, Booth MJ, Reik W, Balasubramanian S. 2012. Genome-wide distribution of 5-formylcytosine in embryonic stem cells is associated with transcription and depends on thymine DNA glycosylase. Genome Biol 13: R69.
31. Satija R, Farrell JA, Gennert D, Schier AF, Regev A. 2015. Spatial reconstruction of single-cell gene expression data. Nat Biotechnol 33: 495–502.
32. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, Wagner U, Dixon J, Lee L, Lobanenkov VV, et al. 2012. A map of the cis-regulatory sequences in the mouse genome. Nature 488: 116–120.
33. Shen L, Wu H, Diep D, Yamaguchi S, D’Alessio AC, Fung HL, Zhang K, Zhang Y. 2013. Genome-wide analysis reveals TET- and TDG-dependent 5-methylcytosine oxidation dynamics. Cell 153: 692–706.
34. Shen L, Inoue A, He J, Liu Y, Lu F, Zhang Y. 2014. Tet3 and DNA replication mediated emethylation of both the maternal and paternal genomes in mouse zygotes. Cell Stem Cell 15: 459–470.
35. Smallwood SA, Lee HJ, Angermueller C, Krueger F, Saadeh H, Peat J, Andrews SR, Stegle O, Reik W, Kelsey G. 2014. Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat Methods 11: 817–820.
36. Smith ZD, Meissner A. 2013. DNA methylation: roles in mammalian development. Nat Rev Genet 14: 204–220.
37. Song CX, Szulwach KE, Dai Q, Fu Y, Mao SQ, Lin L, Street C, Li Y, Poidevin M, Wu H, et al. 2013. Genome-wide profiling of 5-formylcytosine reveals its roles in epigenetic priming. Cell 153: 678–691.
38. Sun Z, Dai N, Borgaro JG, Quimby A, Sun D, Correa IR Jr, Zheng Y, Zhu Z, Guan S. 2015. A sensitive approach to map genome-wide 5-hydroxymethylcytosine and 5-formylcytosine at single-base resolution. Mol Cell 57: 750–761.
39. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, et al. 2009. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930–935.
40. Wang L, Zhang J, Duan J, Gao X, Zhu W, Lu X, Yang L, Zhang J, Li G, Ci W, et al. 2014. Programming and inheritance of parental DNA methylomes in mammals. Cell 157: 979–991.
41. Wilson DM 3rd, Thompson LH. 2007. Molecular mechanisms of sister-chromatid exchange. Mutat Res 616: 11–23.
42. Wossidlo M, Nakamura T, Lepikhov K, Marques CJ, Zakhartch-enko V, Boiani M, Arand J, Nakano T, Reik W, Walter J. 2011. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun 2: 241.
43. Wu H, Zhang Y. 2014. Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 156: 45–68.
44. Wu H, D’Alessio AC, Ito S, Wang Z, Cui K, Zhao K, Sun YE, Zhang Y. 2011. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev 25: 679–684.
45. Wu H, Wu X, Shen L, Zhang Y. 2014. Single-base resolution analysis of active DNA demethylation using methylase-assisted bisulfite sequencing. Nat Biotechnol 32: 1231–1240.
46. Wu H, Wu X, Zhang Y. 2016. Base-resolution profiling of active DNA demethylation using MAB-seq and caMAB-seq. Nat Protoc 11: 1081–1100.
47. Xia B, Han D, Lu X, Sun Z, Zhou A, Yin Q, Zeng H, Liu M, Jiang X, Xie W, et al. 2015. Bisulfite-free, base-resolution analysis of 5-formylcytosine at the genome scale. Nat Methods 12: 1047–1050.