H3K4 Methylation-Dependent Memory of Somatic Cell Identity Inhibits Reprogramming and Development of Nuclear Transfer Embryos

Cell Stem Cell

Volumn 21, Issue 1, 2017, Pages 135-143.e6

  Hörmanseder, Eva ^a   Simeone, Angela ^a   Allen, George E ^a   Bradshaw, Charles R ^a   Figlmüller, Magdalena ^a   Gurdon, John ^a,b   Jullien, Jerome ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

cell fate stability; endoderm; epigenetic memory; H3K4me3; Kdm5b; nuclear transfer; reprogramming

Indexed keywords

HISTONE H3; HISTONE H3K4; UNCLASSIFIED DRUG; HISTONE; XENOPUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS TRANSPLANTATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO TRANSFER; EPIGENETICS; GENE EXPRESSION; HISTONE METHYLATION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; SOMATIC CELL; TRANSCRIPTION REGULATION; XENOPUS LAEVIS; ANIMAL; FEMALE; GENETIC EPIGENESIS; GENETICS; MALE; METABOLISM; METHYLATION; MOUSE;

ANIMALS; CELLULAR REPROGRAMMING; EPIGENESIS, GENETIC; FEMALE; HISTONES; MALE; METHYLATION; MICE; NUCLEAR TRANSFER TECHNIQUES; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 85016459583     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2017.03.003     Document Type: Article

References (39)

1. Alexa, A., Rahnenführer, J., Lengauer, T., Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22 (2006), 1600–1607.
2. Benayoun, B.A., Pollina, E.A., Ucar, D., Mahmoudi, S., Karra, K., Wong, E.D., Devarajan, K., Daugherty, A.C., Kundaje, A.B., Mancini, E., et al. H3K4me3 breadth is linked to cell identity and transcriptional consistency. Cell 158 (2014), 673–688.
3. Blau, H.M., Chiu, C.P., Webster, C., Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell 32 (1983), 1171–1180.
4. Blelloch, R., Wang, Z., Meissner, A., Pollard, S., Smith, A., Jaenisch, R., Reprogramming efficiency following somatic cell nuclear transfer is influenced by the differentiation and methylation state of the donor nucleus. Stem Cells 24 (2006), 2007–2013.
5. Boiani, M., Eckardt, S., Schöler, H.R., McLaughlin, K.J., Oct4 distribution and level in mouse clones: consequences for pluripotency. Genes Dev. 16 (2002), 1209–1219.
6. Chung, Y.G., Matoba, S., Liu, Y., Eum, J.H., Lu, F., Jiang, W., Lee, J.E., Sepilian, V., Cha, K.Y., Lee, D.R., Zhang, Y., Histone demethylase expression enhances human somatic cell nuclear transfer efficiency and promotes derivation of pluripotent stem cells. Cell Stem Cell 17 (2015), 758–766.
7. Clouaire, T., Webb, S., Skene, P., Illingworth, R., Kerr, A., Andrews, R., Lee, J.H., Skalnik, D., Bird, A., Cfp1 integrates both CpG content and gene activity for accurate H3K4me3 deposition in embryonic stem cells. Genes Dev. 26 (2012), 1714–1728.
8. Consortium, E.P., ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489 (2012), 57–74.
9. Dahl, J.A., Jung, I., Aanes, H., Greggains, G.D., Manaf, A., Lerdrup, M., Li, G., Kuan, S., Li, B., Lee, A.Y., et al. Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature 537 (2016), 548–552.
10. Enright, B.P., Kubota, C., Yang, X., Tian, X.C., Epigenetic characteristics and development of embryos cloned from donor cells treated by trichostatin A or 5-aza-2′-deoxycytidine. Biol. Reprod. 69 (2003), 896–901.
11. Firas, J., Liu, X., Polo, J.M., Epigenetic memory in somatic cell nuclear transfer and induced pluripotency: evidence and implications. Differentiation 88 (2014), 29–32.
12. Gao, S., Chung, Y.G., Williams, J.W., Riley, J., Moley, K., Latham, K.E., Somatic cell-like features of cloned mouse embryos prepared with cultured myoblast nuclei. Biol. Reprod. 69 (2003), 48–56.
13. Gentsch, G.E., Smith, J.C., Investigating physical chromatin associations across the Xenopus genome by chromatin immunoprecipitation. Cold Spring Harb. Protoc., 2014, 2014, 2014.
14. Gurdon, J.B., The developmental capacity of nuclei taken from differentiating endoderm cells of Xenopus laevis. J. Embryol. Exp. Morphol. 8 (1960), 505–526.
15. Gurdon, J.B., Elsdale, T.R., Fischberg, M., Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 182 (1958), 64–65.
16. Hirasawa, R., Matoba, S., Inoue, K., Ogura, A., Somatic donor cell type correlates with embryonic, but not extra-embryonic, gene expression in postimplantation cloned embryos. PLoS ONE, 8, 2013, e76422.
17. Hörmanseder, E., Tischer, T., Mayer, T.U., Modulation of cell cycle control during oocyte-to-embryo transitions. EMBO J. 32 (2013), 2191–2203.
18. Kim, K., Zhao, R., Doi, A., Ng, K., Unternaehrer, J., Cahan, P., Huo, H., Loh, Y.H., Aryee, M.J., Lensch, M.W., et al. Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells. Nat. Biotechnol. 29 (2011), 1117–1119.
19. Kishigami, S., Mizutani, E., Ohta, H., Hikichi, T., Thuan, N.V., Wakayama, S., Bui, H.T., Wakayama, T., Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem. Biophys. Res. Commun. 340 (2006), 183–189.
20. Lewis, P.W., Müller, M.M., Koletsky, M.S., Cordero, F., Lin, S., Banaszynski, L.A., Garcia, B.A., Muir, T.W., Becher, O.J., Allis, C.D., Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 340 (2013), 857–861.
21. Li, H., Durbin, R., Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 (2009), 1754–1760.
22. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 1000 Genome Project Data Processing Subgroup. The sequence alignment/map format and SAMtools. Bioinformatics 25 (2009), 2078–2079.
23. Liu, W., Liu, X., Wang, C., Gao, Y., Gao, R., Kou, X., Zhao, Y., Li, J., Wu, Y., Xiu, W., et al. Identification of key factors conquering developmental arrest of somatic cell cloned embryos by combining embryo biopsy and single-cell sequencing. Cell Discov., 2, 2016, 16010.
24. Martin, M., Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. 17 (2011), 10–12.
25. Matoba, S., Liu, Y., Lu, F., Iwabuchi, K.A., Shen, L., Inoue, A., Zhang, Y., Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell 159 (2014), 884–895.
26. Meissner, A., Jaenisch, R., Mammalian nuclear transfer. Dev. Dyn. 235 (2006), 2460–2469.
27. Muramoto, T., Müller, I., Thomas, G., Melvin, A., Chubb, J.R., Methylation of H3K4 is required for inheritance of active transcriptional states. Curr. Biol. 20 (2010), 397–406.
28. Ng, R.K., Gurdon, J.B., Epigenetic memory of active gene transcription is inherited through somatic cell nuclear transfer. Proc. Natl. Acad. Sci. USA 102 (2005), 1957–1962.
29. Nieuwkoop, P.D., Faber, J., Normal Table of Xenopus laevis (Daudin): A Systematical and Chronological Survey of the Development from the Fertilized Egg till the End of Metamorphosis. 1994, Garland Pub.
30. Polo, J.M., Liu, S., Figueroa, M.E., Kulalert, W., Eminli, S., Tan, K.Y., Apostolou, E., Stadtfeld, M., Li, Y., Shioda, T., et al. Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat. Biotechnol. 28 (2010), 848–855.
31. Probst, A.V., Dunleavy, E., Almouzni, G., Epigenetic inheritance during the cell cycle. Nat. Rev. Mol. Cell Biol. 10 (2009), 192–206.
32. Quinlan, A.R., Hall, I.M., BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26 (2010), 841–842.
33. Robinson, M.D., McCarthy, D.J., Smyth, G.K., edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 (2010), 139–140.
34. Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., Mesirov, J.P., Integrative genomics viewer. Nat. Biotechnol. 29 (2011), 24–26.
35. Santos-Rosa, H., Schneider, R., Bannister, A.J., Sherriff, J., Bernstein, B.E., Emre, N.C., Schreiber, S.L., Mellor, J., Kouzarides, T., Active genes are tri-methylated at K4 of histone H3. Nature 419 (2002), 407–411.
36. Takahashi, K., Yamanaka, S., Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126 (2006), 663–676.
37. Teperek, M., Simeone, A., Gaggioli, V., Miyamoto, K., Allen, G.E., Erkek, S., Kwon, T., Marcotte, E.M., Zegerman, P., Bradshaw, C.R., et al. Sperm is epigenetically programmed to regulate gene transcription in embryos. Genome Res. 26 (2016), 1034–1046.
38. Thorvaldsdóttir, H., Robinson, J.T., Mesirov, J.P., Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14 (2013), 178–192.
39. Trapnell, C., Pachter, L., Salzberg, S.L., TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 (2009), 1105–1111.