Genome-wide, Single-Cell DNA Methylomics Reveals Increased Non-CpG Methylation during Human Oocyte Maturation

Stem Cell Reports

Volumn 9, Issue 1, 2017, Pages 397-407

  Yu, Bo ^a   Dong, Xiao ^b   Gravina, Silvia ^b   Kartal, Önder ^c   Schimmel, Timothy ^d   Cohen, Jacques ^d   Tortoriello, Drew ^e   Zody, Raifa ^e   Hawkins, R David ^a   Vijg, Jan ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d Reprogenetics LLC   (United States)

^e Sher Institutes for Reproductive Medicine   (United States)

Author keywords

DNA methylome; epigenome; human oocyte; in vitro maturation; non CpG methylation; oocyte maturation; single cell

Indexed keywords

CELL DNA; GONADORELIN AGONIST; GONADORELIN ANTAGONIST; LEUPRORELIN;

ADULT; ARTICLE; BIOINFORMATICS; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION COEFFICIENT; CPG ISLAND; DNA METHYLATION; FEMALE; GENOME-WIDE ASSOCIATION STUDY; GERMINAL VESICLE; HUMAN; HUMAN CELL; INTERMETHOD COMPARISON; METAPHASE; NUCLEOTIDE SEQUENCE; OOCYTE MATURATION; OOCYTE RETRIEVAL; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SINGLE CELL ANALYSIS; SINGLE CELL WHOLE GENOME BISULFITE SEQUENCING; ZONA PELLUCIDA; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; HUMAN GENOME; METABOLISM; OOCYTE; OOCYTE DEVELOPMENT;

ADULT; CELLS, CULTURED; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME, HUMAN; HUMANS; OOCYTES; OOGENESIS; SINGLE-CELL ANALYSIS;

EID: 85021120967     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2017.05.026     Document Type: Article

References (31)

1. Bogdanovic, O., Smits, A.H., de la Calle Mustienes, E., Tena, J.J., Ford, E., Williams, R., Senanayake, U., Schultz, M.D., Hontelez, S., van Kruijsbergen, I., et al. Active DNA demethylation at enhancers during the vertebrate phylotypic period. Nat. Genet. 48 (2016), 417–426.
2. Farlik, M., Sheffield, N.C., Nuzzo, A., Datlinger, P., Schonegger, A., Klughammer, J., Bock, C., Single-cell DNA methylome sequencing and bioinformatic inference of epigenomic cell-state dynamics. Cell Rep. 10 (2015), 1386–1397.
3. Gkountela, S., Zhang, K.X., Shafiq, T.A., Liao, W.W., Hargan-Calvopina, J., Chen, P.Y., Clark, A.T., DNA demethylation dynamics in the human prenatal germline. Cell 161 (2015), 1425–1436.
4. Gravina, S., Ganapathi, S., Vijg, J., Single-cell, locus-specific bisulfite sequencing (SLBS) for direct detection of epimutations in DNA methylation patterns. Nucleic Acids Res., 43, 2015, e93.
5. Gravina, S., Dong, X., Yu, B., Vijg, J., Single-cell genome-wide bisulfite sequencing uncovers extensive heterogeneity in the mouse liver methylome. Genome Biol., 17, 2016, 150.
6. Guo, J.U., Su, Y., Shin, J.H., Shin, J., Li, H., Xie, B., Zhong, C., Hu, S., Le, T., Fan, G., et al. Distribution, recognition and regulation of non-CpG methylation in the adult mammalian brain. Nat. Neurosci. 17 (2014), 215–222.
7. Guo, W., Chung, W.Y., Qian, M., Pellegrini, M., Zhang, M.Q., Characterizing the strand-specific distribution of non-CpG methylation in human pluripotent cells. Nucleic Acids Res. 42 (2014), 3009–3016.
8. Guo, F., Yan, L., Guo, H., Li, L., Hu, B., Zhao, Y., Yong, J., Hu, Y., Wang, X., Wei, Y., et al. The transcriptome and DNA methylome landscapes of human primordial germ cells. Cell 161 (2015), 1437–1452.
9. Hargan-Calvopina, J., Taylor, S., Cook, H., Hu, Z., Lee, S.A., Yen, M.R., Chiang, Y.S., Chen, P.Y., Clark, A.T., Stage-specific demethylation in primordial germ cells safeguards against precocious differentiation. Dev. Cell 39 (2016), 75–86.
10. Hon, G.C., Rajagopal, N., Shen, Y., McCleary, D.F., Yue, F., Dang, M.D., Ren, B., Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues. Nat. Genet. 45 (2013), 1198–1206.
11. Kocabas, A.M., Crosby, J., Ross, P.J., Otu, H.H., Beyhan, Z., Can, H., Tam, W.L., Rosa, G.J., Halgren, R.G., Lim, B., et al. The transcriptome of human oocytes. Proc. Natl. Acad. Sci. USA 103 (2006), 14027–14032.
12. Kuhtz, J., Romero, S., De Vos, M., Smitz, J., Haaf, T., Anckaert, E., Human in vitro oocyte maturation is not associated with increased imprinting error rates at LIT1, SNRPN, PEG3 and GTL2. Hum. Reprod. 29 (2014), 1995–2005.
13. Lister, R., Mukamel, E.A., Nery, J.R., Urich, M., Puddifoot, C.A., Johnson, N.D., Lucero, J., Huang, Y., Dwork, A.J., Schultz, M.D., et al. Global epigenomic reconfiguration during mammalian brain development. Science, 341, 2013, 1237905.
14. Okae, H., Chiba, H., Hiura, H., Hamada, H., Sato, A., Utsunomiya, T., Kikuchi, H., Yoshida, H., Tanaka, A., Suyama, M., et al. Genome-wide analysis of DNA methylation dynamics during early human development. PLoS Genet., 10, 2014, e1004868.
15. Schwartzman, O., Tanay, A., Single-cell epigenomics: techniques and emerging applications. Nat. Rev. Genet. 16 (2015), 716–726.
16. Shirane, K., Toh, H., Kobayashi, H., Miura, F., Chiba, H., Ito, T., Kono, T., Sasaki, H., Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoS Genet., 9, 2013, e1003439.
17. Smallwood, S.A., Kelsey, G., De novo DNA methylation: a germ cell perspective. Trends Genet. 28 (2012), 33–42.
18. Smallwood, S.A., Tomizawa, S., Krueger, F., Ruf, N., Carli, N., Segonds-Pichon, A., Sato, S., Hata, K., Andrews, S.R., Kelsey, G., Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat. Genet. 43 (2011), 811–814.
19. Smallwood, S.A., Lee, H.J., Angermueller, C., Krueger, F., Saadeh, H., Peat, J., Andrews, S.R., Stegle, O., Reik, W., Kelsey, G., Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat. Methods 11 (2014), 817–820.
20. Smith, Z.D., Chan, M.M., Humm, K.C., Karnik, R., Mekhoubad, S., Regev, A., Eggan, K., Meissner, A., DNA methylation dynamics of the human preimplantation embryo. Nature 511 (2014), 611–615.
21. Strimmer, K., fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24 (2008), 1461–1462.
22. Strimmer, K., A unified approach to false discovery rate estimation. BMC Bioinformatics, 9, 2008, 303.
23. Surani, M.A., Human germline: a new research frontier. Stem Cell Reports 4 (2015), 955–960.
24. Tang, W.W., Dietmann, S., Irie, N., Leitch, H.G., Floros, V.I., Bradshaw, C.R., Hackett, J.A., Chinnery, P.F., Surani, M.A., A unique gene regulatory network resets the human germline epigenome for development. Cell 161 (2015), 1453–1467.
25. Tomizawa, S., Kobayashi, H., Watanabe, T., Andrews, S., Hata, K., Kelsey, G., Sasaki, H., Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes. Development 138 (2011), 811–820.
26. Veselovska, L., Smallwood, S.A., Saadeh, H., Stewart, K.R., Krueger, F., Maupetit-Mehouas, S., Arnaud, P., Tomizawa, S., Andrews, S., Kelsey, G., Deep sequencing and de novo assembly of the mouse oocyte transcriptome define the contribution of transcription to the DNA methylation landscape. Genome Biol., 16, 2015, 209.
27. von Meyenn, F., Reik, W., Forget the parents: epigenetic reprogramming in human germ cells. Cell 161 (2015), 1248–1251.
28. Wallace, W.H., Kelsey, T.W., Human ovarian reserve from conception to the menopause. PLoS One, 5, 2010, e8772.
29. Yu, B., Russanova, V.R., Gravina, S., Hartley, S., Mullikin, J.C., Ignezweski, A., Graham, J., Segars, J.H., DeCherney, A.H., Howard, B.H., DNA methylome and transcriptome sequencing in human ovarian granulosa cells links age-related changes in gene expression to gene body methylation and 3′-end GC density. Oncotarget 6 (2015), 3627–3643.
30. Ziller, M.J., Muller, F., Liao, J., Zhang, Y., Gu, H., Bock, C., Boyle, P., Epstein, C.B., Bernstein, B.E., Lengauer, T., et al. Genomic distribution and inter-sample variation of non-CpG methylation across human cell types. PLoS Genet., 7, 2011, e1002389.
31. Ziller, M.J., Gu, H., Muller, F., Donaghey, J., Tsai, L.T., Kohlbacher, O., De Jager, P.L., Rosen, E.D., Bennett, D.A., Bernstein, B.E., et al. Charting a dynamic DNA methylation landscape of the human genome. Nature 500 (2013), 477–481.