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Dynamic and aberrant patterns of H3K4me3, H3K9me3, and H3K27me3 during early zygotic genome activation in cloned mouse embryos

Published online by Cambridge University Press:  15 September 2022

Zhihui Liu ,
Jing Cui ,
Weiguo Wang ,
Mingyang Li ,
Zhisong Wang ,
Giorgio Antonio Presicce ,
Xiuchun (Cindy) Tian ,
Liyou An  and
Fuliang Du Open the ORCID record for Fuliang Du [Opens in a new window]
Zhihui Liu
Affiliation:
Jiangsu Key Laboratory for Molecular and Medical Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing210046, China
Jing Cui
Affiliation:
Jiangsu Key Laboratory for Molecular and Medical Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing210046, China
Weiguo Wang
Affiliation:
Jiangsu Key Laboratory for Molecular and Medical Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing210046, China
Mingyang Li
Affiliation:
Jiangsu Key Laboratory for Molecular and Medical Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing210046, China
Zhisong Wang
Affiliation:
Jiangsu Key Laboratory for Molecular and Medical Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing210046, China
Giorgio Antonio Presicce
Affiliation:
ARSIAL, Rome00162, Italy
Xiuchun (Cindy) Tian
Affiliation:
Centre for Regenerative Biology/Department of Animal Science, University of Connecticut, Storrs, CT, USA
Liyou An*
Affiliation:
Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi830046, China
Fuliang Du*
Affiliation:
Jiangsu Key Laboratory for Molecular and Medical Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing210046, China
*
Author for correspondence: Fuliang Du’ Jiangsu Key Laboratory for Molecular and Medical Biotechnology, College of Life Sciences, Nanjing Normal University, #1 Wenyuan Rd, Nanjing210046, P R China, Email: fuliangd@njnu.edu.cn. Liyou An. Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi830046, China. Email: anliyou@aliyun.com
Author for correspondence: Fuliang Du’ Jiangsu Key Laboratory for Molecular and Medical Biotechnology, College of Life Sciences, Nanjing Normal University, #1 Wenyuan Rd, Nanjing210046, P R China, Email: fuliangd@njnu.edu.cn. Liyou An. Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi830046, China. Email: anliyou@aliyun.com
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Summary

Somatic cell nuclear transfer (NT) is associated with aberrant changes in epigenetic reprogramming that impede the development of embryos, particularly during zygotic genome activation. Here, we characterized epigenetic patterns of H3K4me3, H3K9me3, and H3K27me3 in mouse NT embryos up to the second cell cycle (i.e. four-celled stage) during zygotic genome activation. In vivo fertilized and parthenogenetically activated (PA) embryos served as controls. In fertilized embryos, maternal and paternal pronuclei exhibited asymmetric H3K4me3, H3K9me3, and H3K27me3 modifications, with the paternal pronucleus showing delayed epigenetic modifications. Higher levels of H3K4me3 and H3K9me3 were observed in NT and PA embryos than in fertilized embryos. However, NT embryos exhibited a lower level of H3K27me3 than PA and fertilized embryos from pronuclear stage 3 to the four-celled stage. Our finding that NT embryos exhibited aberrant H3K4me3, H3K9me3, and H3K27me3 modifications in comparison with fertilized embryos during early zygotic genome activation help to unravel the epigenetic mechanisms of methylation changes in early NT reprogramming and provide an insight into the role of histone H3 in the regulation of cell plasticity during natural reproduction and somatic cell NT.

Keywords

Epigenetic modificationMouseNuclear reprogrammingNuclear transfer
Type
Research Article
Information
Zygote , Volume 30 , Issue 6 , December 2022 , pp. 903 - 909
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this study.

References

Adenot, P. G., Mercier, Y., Renard, J. P. and Thompson, E. M. (1997). Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development, 124(22), 4615–4625. doi: 10.1242/dev.124.22.4615 CrossRefGoogle ScholarPubMed
Bai, G. Y., Song, S. H., Zhang, Y. W., Huang, X., Huang, X. W., Sun, R. Z. and Lei, L. (2018). Kdm6a overexpression improves the development of cloned mouse embryos. Zygote, 26(1), 24–32. doi: 10.1017/S0967199417000673 CrossRefGoogle ScholarPubMed
Balakrishnan, L. and Milavetz, B. (2010). Decoding the histone H4 lysine 20 methylation mark. Critical Reviews in Biochemistry and Molecular Biology, 45(5), 440–452. doi: 10.3109/10409238.2010.504700 CrossRefGoogle ScholarPubMed
Bao, S., Miyoshi, N., Okamoto, I., Jenuwein, T., Heard, E. and Azim Surani, M. (2005). Initiation of epigenetic reprogramming of the X chromosome in somatic nuclei transplanted to a mouse oocyte. EMBO Reports, 6(8), 748–754. doi: 10.1038/sj.embor.7400461 CrossRefGoogle ScholarPubMed
Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I. and Zhao, K. (2007). High-resolution profiling of histone methylations in the human genome. Cell, 129(4), 823–837. doi: 10.1016/j.cell.2007.05.009 CrossRefGoogle ScholarPubMed
Biterge, B. and Schneider, R. (2014). Histone variants: Key players of chromatin. Cell and Tissue Research, 356(3), 457–466. doi: 10.1007/s00441-014-1862-4 CrossRefGoogle ScholarPubMed
Campbell, K. H., McWhir, J., Ritchie, W. A. and Wilmut, I. (1996). Sheep cloned by nuclear transfer from a cultured cell line. Nature, 380(6569), 64–66. doi: 10.1038/380064a0 CrossRefGoogle ScholarPubMed
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. and Zhang, Y. (2015). Histone demethylase expression enhances human somatic cell nuclear transfer efficiency and promotes derivation of pluripotent stem cells. Cell Stem Cell, 17(6), 758–766. doi: 10.1016/j.stem.2015.10.001 CrossRefGoogle ScholarPubMed
Deng, M., Chen, B., Liu, Z., Cai, Y., Wan, Y., Zhou, J. and Wang, F. (2020). Exchanges of histone methylation and variants during mouse zygotic genome activation. Zygote, 28(3), 250–254. doi: 10.1017/S0967199420000076 CrossRefGoogle ScholarPubMed
Gao, R., Wang, C., Gao, Y., Xiu, W., Chen, J., Kou, X., Zhao, Y., Liao, Y., Bai, D., Qiao, Z., Yang, L., Wang, M., Zang, R., Liu, X., Jia, Y., Li, Y., Zhang, Y., Yin, J., Wang, H., Wan, X., Zhang, Y. and Gao, S. (2018). Inhibition of aberrant DNA re-methylation improves post-implantation development of somatic cell nuclear transfer embryos. Cell Stem Cell, 23(3), 426–435.e5. doi: 10.1016/j.stem.2018.07.017 CrossRefGoogle ScholarPubMed
Gou, L. T., Lim, D. H., Ma, W., Aubol, B. E., Hao, Y., Wang, X., Zhao, J., Liang, Z., Shao, C., Zhang, X., Meng, F., Li, H., Zhang, X., Xu, R., Li, D., Rosenfeld, M. G., Mellon, P. L., Adams, J. A., Liu, M. F. and Fu, X. D. (2020). Initiation of parental genome reprogramming in fertilized oocyte by splicing kinase SRPK1-catalyzed protamine phosphorylation. Cell, 180(6), 1212–1227.e14. doi: 10.1016/j.cell.2020.02.020 CrossRefGoogle ScholarPubMed
Gurdon, J. B. (1962). The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. Journal of Embryology and Experimental Morphology, 10, 622–640. doi: 10.1242/dev.10.4.622 Google ScholarPubMed
Ho, N. T. K., Nguyen, T. V. T., Nguyen, T. V. and Bui, H. T. (2019). Epigenetic impairments in development of parthenogenetic preimplantation mouse embryos. Journal of Reproduction and Development, 65(1), 83–90. doi: 10.1262/jrd.2018-028 CrossRefGoogle ScholarPubMed
Hörmanseder, E., Simeone, A., Allen, G. E., Bradshaw, C. R., Figlmüller, M., Gurdon, J. and Jullien, J. (2017). H3K4 methylation-dependent memory of somatic cell identity inhibits reprogramming and development of nuclear transfer embryos. Cell Stem Cell, 21(1), 135–143.e6. doi: 10.1016/j.stem.2017.03.003 CrossRefGoogle ScholarPubMed
Hou, J., Liu, L., Zhang, J., Cui, X. H., Yan, F. X., Guan, H., Chen, Y. F. and An, X. R. (2008). Epigenetic modification of histone 3 at lysine 9 in sheep zygotes and its relationship with DNA methylation. BMC Developmental Biology, 8, 60. doi: 10.1186/1471-213X-8-60 CrossRefGoogle ScholarPubMed
Inoue, K., Kohda, T., Sugimoto, M., Sado, T., Ogonuki, N., Matoba, S., Shiura, H., Ikeda, R., Mochida, K., Fujii, T., Sawai, K., Otte, A. P., Tian, X. C., Yang, X., Ishino, F., Abe, K. and Ogura, A. (2010). Impeding Xist expression from the active X chromosome improves mouse somatic cell nuclear transfer. Science, 330(6003), 496–499. doi: 10.1126/science.1194174 CrossRefGoogle ScholarPubMed
Lachner, M. and Jenuwein, T. (2002). The many faces of histone lysine methylation. Current Opinion in Cell Biology, 14(3), 286–298. doi: 10.1016/s0955-0674(02)00335-6 CrossRefGoogle ScholarPubMed
Lee, M. T., Bonneau, A. R. and Giraldez, A. J. (2014). Zygotic genome activation during the maternal-to-zygotic transition. Annual Review of Cell and Developmental Biology, 30, 581–613. doi: 10.1146/annurev-cellbio-100913-013027 CrossRefGoogle ScholarPubMed
Lepikhov, K., Wossidlo, M., Arand, J. and Walter, J. (2010). DNA methylation reprogramming and DNA repair in the mouse zygote. International Journal of Developmental Biology, 54(11–12), 1565–1574. doi: 10.1387/ijdb.103206kl CrossRefGoogle ScholarPubMed
Liu, W., Yin, J., Kou, X., Jiang, Y., Gao, H., Zhao, Y., Huang, B., He, W., Wang, H., Han, Z. and Gao, S. (2014). Asymmetric reprogramming capacity of parental pronuclei in mouse zygotes. Cell Reports, 6(6), 1008–1016. doi: 10.1016/j.celrep.2014.02.018 CrossRefGoogle ScholarPubMed
Liu, W., Liu, X., Wang, C., Gao, Y., Gao, R., Kou, X., Zhao, Y., Li, J., Wu, Y., Xiu, W., Wang, S., Yin, J., Liu, W., Cai, T., Wang, H., Zhang, Y. and Gao, S. (2016). Identification of key factors conquering developmental arrest of somatic cell cloned embryos by combining embryo biopsy and single-cell sequencing. Cell Discovery, 2, 16010. doi: 10.1038/celldisc.2016.10 CrossRefGoogle ScholarPubMed
Liu, X., Luo, C., Deng, K., Wu, Z., Wei, Y., Jiang, J., Lu, F. and Shi, D. (2018a). Cytoplasmic volume of recipient oocytes affects the nucleus reprogramming and the developmental competence of HMC buffalo (Bubalus bubalis) embryos. Journal of Veterinary Medical Science, 80(8), 1291–1300. doi: 10.1292/jvms.18-0043 CrossRefGoogle ScholarPubMed
Liu, X., Wang, Y., Gao, Y., Su, J., Zhang, J., Xing, X., Zhou, C., Yao, K., An, Q. and Zhang, Y. (2018b). H3K9 demethylase KDM4E is an epigenetic regulator for bovine embryonic development and a defective factor for nuclear reprogramming. Development, 145(4), dev158261. doi: 10.1242/dev.158261 CrossRefGoogle Scholar
Liu, X., Chen, L., Wang, T., Zhou, J., Li, Z., Bu, G., Zhang, J., Yin, S., Wu, D., Dou, C., Xu, T., He, H., Zhu, W., Yu, L., Liu, Z., Zhang, X., Chen, Z. X. and Miao, Y. L. (2021). TDG is a pig-specific epigenetic regulator with insensitivity to H3K9 and H3K27 demethylation in nuclear transfer embryos. Stem Cell Reports, 16(11), 2674–2689. doi: 10.1016/j.stemcr.2021.09.012 CrossRefGoogle ScholarPubMed
Markoulaki, S., Meissner, A. and Jaenisch, R. (2008). Somatic cell nuclear transfer and derivation of embryonic stem cells in the mouse. Methods, 45(2), 101–114. doi: 10.1016/j.ymeth.2008.04.002 CrossRefGoogle ScholarPubMed
Matoba, S. and Zhang, Y. (2018). Somatic cell nuclear transfer reprogramming: Mechanisms and applications. Cell Stem Cell, 23(4), 471–485. doi: 10.1016/j.stem.2018.06.018 CrossRefGoogle ScholarPubMed
Matoba, S., Liu, Y., Lu, F., Iwabuchi, K. A., Shen, L., Inoue, A. and Zhang, Y. (2014). Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell, 159, 884–895. doi: 10.1016/j.cell.2014.09.055 CrossRefGoogle ScholarPubMed
Matoba, S., Wang, H., Jiang, L., Lu, F., Iwabuchi, K. A., Wu, X., Inoue, K., Yang, L., Press, W., Lee, J. T., Ogura, A., Shen, L. and Zhang, Y. (2018). Loss of H3K27me3 imprinting in somatic cell nuclear transfer embryos disrupts post-implantation development. Cell Stem Cell, 23(3), 343–354.e5. doi: 10.1016/j.stem.2018.06.008 CrossRefGoogle ScholarPubMed
Panda, S. K., George, A., Saha, A. P., Sharma, R., Manik, R. S., Chauhan, M. S., Palta, P. and Singla, S. K. (2011). Effect of cytoplasmic volume on developmental competence of buffalo (Bubalus bubalis) embryos produced through hand-made cloning. Cell Reprogram, 13(3), 257–262. doi: 10.1089/cell.2010.0096 CrossRefGoogle ScholarPubMed
Santos, F., Peters, A. H., Otte, A. P., Reik, W. and Dean, W. (2005). Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Developmental Biology, 280(1), 225–236. doi: 10.1016/j.ydbio.2005.01.025 CrossRefGoogle ScholarPubMed
Schultz, R. M., Stein, P. and Svoboda, P. (2018). The oocyte-to-embryo transition in mouse: Past, present, and future. Biology of Reproduction, 99(1), 160–174. doi: 10.1093/biolre/ioy013 CrossRefGoogle ScholarPubMed
Svoboda, P. (2018). Mammalian zygotic genome activation. Seminars in Cell and Developmental Biology, 84, 118–126. doi: 10.1016/j.semcdb.2017.12.006 CrossRefGoogle ScholarPubMed
Tadros, W. and Lipshitz, H. D. (2009). The maternal-to-zygotic transition: A play in two acts. Development, 136(18), 3033–3042. doi: 10.1242/dev.033183 CrossRefGoogle ScholarPubMed
Tardat, M., Albert, M., Kunzmann, R., Liu, Z., Kaustov, L., Thierry, R., Duan, S., Brykczynska, U., Arrowsmith, C. H. and Peters, A. H. (2015). Cbx2 targets PRC1 to constitutive heterochromatin in mouse zygotes in a parent-of-origin-dependent manner. Molecular Cell, 58(1), 157–171. doi: 10.1016/j.molcel.2015.02.013 CrossRefGoogle Scholar
Van Thuan, N. V., Kishigami, S. and Wakayama, T. (2010). How to improve the success rate of mouse cloning technology. Journal of Reproduction and Development, 56(1), 20–30. doi: 10.1262/jrd.09-221a CrossRefGoogle Scholar
Wakayama, S., Kishigami, S. and Wakayama, T. (2019). Improvement of mouse cloning from any type of cell by nuclear injection. Methods in Molecular Biology, 1874, 211–228. doi: 10.1007/978-1-4939-8831-0_12 CrossRefGoogle ScholarPubMed
Wang, F., Kou, Z., Zhang, Y. and Gao, S. (2007). Dynamic reprogramming of histone acetylation and methylation in the first cell cycle of cloned mouse embryos. Biology of Reproduction, 77(6), 1007–1016. doi: 10.1095/biolreprod.107.063149 CrossRefGoogle ScholarPubMed
Weng, X. G., Cai, M. M., Zhang, Y. T., Liu, Y., Liu, C. and Liu, Z. H. (2020). Improvement in the in vitro development of cloned pig embryos after kdm4a overexpression and an H3K9me3 methyltransferase inhibitor treatment. Theriogenology, 146, 162–170. doi: 10.1016/j.theriogenology.2019.11.027 CrossRefGoogle Scholar
Xue, Z., Huang, K., Cai, C., Cai, L., Jiang, C. Y., Feng, Y., Liu, Z., Zeng, Q., Cheng, L., Sun, Y. E., Liu, J. Y., Horvath, S. and Fan, G. (2013). Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature, 500(7464), 593–597. doi: 10.1038/nature12364 CrossRefGoogle ScholarPubMed
Yang, L., Song, L., Liu, X., Bai, L. and Li, G. (2018). KDM6A and KDM6B play contrasting roles in nuclear transfer embryos revealed by MERVL reporter system. EMBO Reports, 19(12), e46240. doi: 10.15252/embr.201846240 CrossRefGoogle ScholarPubMed
Zhang, M., Wang, F., Kou, Z., Zhang, Y. and Gao, S. (2009). Defective chromatin structure in somatic cell cloned mouse embryos. Journal of Biological Chemistry, 284(37), 24981–24987. doi: 10.1074/jbc.M109.011973 CrossRefGoogle ScholarPubMed
Zhang, B., Zheng, H., Huang, B., Li, W., Xiang, Y., Peng, X., Ming, J., Wu, X., Zhang, Y., Xu, Q., Liu, W., Kou, X., Zhao, Y., He, W., Li, C., Chen, B., Li, Y., Wang, Q., Ma, J., Yin, Q., Kee, K., Meng, A., Gao, S., Xu, F., Na, J. and Xie, W. (2016). Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature, 537(7621), 553–557. doi: 10.1038/nature19361 CrossRefGoogle ScholarPubMed
Zhou, C., Wang, Y., Zhang, J., Su, J., An, Q., Liu, X., Zhang, M., Wang, Y., Liu, J. and Zhang, Y. (2019). H3K27me3 is an epigenetic barrier while KDM6A overexpression improves nuclear reprogramming efficiency. FASEB Journal, 33(3), 4638–4652. doi: 10.1096/fj.201801887R CrossRefGoogle ScholarPubMed
Zhou, C., Zhang, J., Zhang, M., Wang, D., Ma, Y., Wang, Y., Wang, Y., Huang, Y. and Zhang, Y. (2020). Transcriptional memory inherited from donor cells is a developmental defect of bovine cloned embryos. FASEB Journal, 34(1), 1637–1651. doi: 10.1096/fj.201900578RR CrossRefGoogle ScholarPubMed