Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-18T17:48:55.041Z Has data issue: false hasContentIssue false

Exchanges of histone methylation and variants during mouse zygotic genome activation

Published online by Cambridge University Press:  20 November 2019

Mingtian Deng
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China
Baobao Chen
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
Zifei Liu
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China
Yu Cai
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China
Yongjie Wan
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China
Jianguo Zhou
Affiliation:
National Experimental Teaching Demonstration Center of Animal Science, Nanjing Agricultural University, Nanjing 210095, China
Feng Wang*
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China
*
Author for correspondence: Feng Wang, Jiangsu Livestock Embryo Engineering Laboratory, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China. Tel.: +86 025 84395381. Fax: +86 025 84395314. E-mail: [email protected]

Summary

Minor and major zygotic genome activation (ZGA) are crucial for preimplantation development. During this process, histone variants and methylation influence chromatin accessibility and consequently regulated the expression of zygotic genes. However, the detailed exchanges of these modifications during ZGA remain to be determined. In the present study, the epigenetic modifications of histone 3 on lysine 9 (H3K9), 27 (H3K27) and 36 (H3K36), as well as four histone variants were determined during minor and major ZGA and in post-ZGA stages of mouse embryos. Firstly, microH2A1, H3K27me3 and H3K36me3 were asymmetrically stained in the female pronucleus during minor ZGA but lost staining in major ZGA. Secondly, H3K9me2 and H3K9me3 were strongly stained in the female pronucleus, but weakly stained in the male pronucleus and disappeared after ZGA. Thirdly, H2A.Z and H3.3 were symmetrically stained in male and female pronuclei during minor ZGA. Moreover, H3K27me2 was not statistically changed during mouse early development, while H3K36me2 was only detected in 2- and 4-cell embryos. In conclusion, our data revealed dynamics of histone methylation and variants during mice ZGA and provided details of their exchange in mice embryogenesis. Moreover, we further inferred that macroH2A1, H2A.Z, H3K9me2/3 and H3K27me2/3 may play crucial roles during mouse ZGA.

Type
Research Article
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abe, KI, Funaya, S, Tsukioka, D, Kawamura, M, Suzuki, Y, Suzuki, MG, Schultz, RM and Aoki, F (2018) Minor zygotic gene activation is essential for mouse preimplantation development. Proc Natl Acad Sci USA 115, E67808.CrossRefGoogle ScholarPubMed
Adenot, PG, Mercier, Y, Renard, JP and Thompson, EM (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, 4615–25.Google ScholarPubMed
Bošković, A, Bender, A, Gall, L, Ziegler-Birling, C, Beaujean, N and Torres-Padilla, M-E (2012) Analysis of active chromatin modifications in early mammalian embryos reveals uncoupling of H2A.Z acetylation and H3K36 trimethylation from embryonic genome activation. Epigenetics 7, 747–57.CrossRefGoogle ScholarPubMed
Cao, Z, Li, Y, Chen, Z, Wang, H, Zhang, M, Zhou, N, Wu, R, Ling, Y, Fang, F, Li, N and Zhang, Y (2015) Genome-wide dynamic profiling of histone methylation during nuclear transfer-mediated porcine somatic cell reprogramming. PLoS One 10, e0144897.CrossRefGoogle ScholarPubMed
Chang, CC, Ma, Y, Jacobs, S, Tian, XC, Yang, X and Rasmussen, TP (2005) A maternal store of macroH2A is removed from pronuclei prior to onset of somatic macroH2A expression in preimplantation embryos. Dev Biol 278, 367–80.CrossRefGoogle ScholarPubMed
Chung, N, Bogliotti, YS, Ding, W, Vilarino, M, Takahashi, K, Chitwood, JL, Schultz, RM and Ross, PJ (2017) Active H3K27me3 demethylation by KDM6B is required for normal development of bovine preimplantation embryos. Epigenetics 12, 1048–56.CrossRefGoogle ScholarPubMed
Dahl, JA, Jung, I, Aanes, H, Greggains, GD, Manaf, A, Lerdrup, M, Li, G, Kuan, S, Li, B, Lee, AY, Preissl, S, Jermstad, I, Haugen, MH, Suganthan, R, Bjørås, M, Hansen, K, Dalen, KT, Fedorcsak, P, Ren, B and Klungland, A (2016) Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature 537, 548.CrossRefGoogle ScholarPubMed
Deng, M, Liu, Z, Ren, C, Zhang, G, Pang, J, Zhang, Y, Wang, F and Wan, Y (2018) Long noncoding RNAs exchange during zygotic genome activation in goat. Biol Reprod 99, 707–17.CrossRefGoogle ScholarPubMed
Eckersley-Maslin, MA, Alda-Catalinas, C and Reik, W (2018) Dynamics of the epigenetic landscape during the maternal-to-zygotic transition. Nat Rev Mol Cell Biol 19, 436–50.CrossRefGoogle ScholarPubMed
Faast, R, Thonglairoam, V, Schulz, TC, Beall, J, Wells, JR, Taylor, H, Matthaei, K, Rathjen, PD, Tremethick, DJ and Lyons, I (2001) Histone variant H2A.Z is required for early mammalian development. Curr Biol 11, 1183–7.CrossRefGoogle ScholarPubMed
Hanna, CW, Demond, H and Kelsey, G (2018) Epigenetic regulation in development: is the mouse a good model for the human? Hum Reprod Update 24, 556–76.CrossRefGoogle Scholar
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 Dev Biol 8, 60.CrossRefGoogle ScholarPubMed
Huang, XJ, Wang, X, Ma, X, Sun, SC, Zhou, X, Zhu, C and Liu, H (2014) EZH2 is essential for development of mouse preimplantation embryos. Reprod Fertil Dev 26, 1166–75.CrossRefGoogle ScholarPubMed
Latham, KE, Garrels, JI, Chang, C and Solter, D (1991) Quantitative analysis of protein synthesis in mouse embryos. I. Extensive reprogramming at the one- and two-cell stages. Development 112, 921–32.Google ScholarPubMed
Lee, MT, Bonneau, AR and Giraldez, AJ (2014) Zygotic genome activation during the maternal-to-zygotic transition. Annu Rev Cell Dev Biol 30, 581613.CrossRefGoogle ScholarPubMed
Lepikhov, K and Walter, J (2004) Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote. BMC Dev Biol 4, 12.CrossRefGoogle ScholarPubMed
Lepikhov, K, Yang, F, Wrenzycki, C, Zakhartchenko, V, Niemann, H, Wolf, E and Walter, J (2005) Dynamics of histone H3 methylation at positions K4 and K9 in mouse, rabbit and bovine preimplantation embryos. Reprod Fertil Dev 18, 174.CrossRefGoogle Scholar
Lepikhov, K, Zakhartchenko, V, Hao, R, Yang, F, Wrenzycki, C, Niemann, H, Wolf, E and Walter, J (2008) Evidence for conserved DNA and histone H3 methylation reprogramming in mouse, bovine and rabbit zygotes. Epigenetics Chromatin 1, 111.CrossRefGoogle ScholarPubMed
Lin, CJ, Conti, M and Ramalho-Santos, M (2013) Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development. Development 140, 3624–34.CrossRefGoogle ScholarPubMed
Lindeman, Leif C, Andersen, Ingrid S, Reiner, Andrew H, Li, N, Aanes, H, Østrup, O, Winata, C, Mathavan, S, Müller, F, Aleström, P and Collas, P (2011) Prepatterning of developmental gene expression by modified histones before zygotic genome activation. Dev Cell 21, 9931004.CrossRefGoogle ScholarPubMed
Liu, X, Wang, Y, Gao, Y, Su, J, Zhang, J, Xing, X, Zhou, C, Yao, K, An, Q and Zhang, Y (2018) H3K9 demethylase KDM4E is an epigenetic regulator for bovine embryonic development and a defective factor for nuclear reprogramming. Development 145, dev158261.CrossRefGoogle Scholar
Nashun, B, Yukawa, M, Liu, H, Akiyama, T and Aoki, F (2010) Changes in the nuclear deposition of histone H2A variants during preimplantation development in mice. Development 137, 3785–94.CrossRefGoogle Scholar
Park, JS, Jeong, YS, Shin, ST, Lee, K-K and Kang, Y-K (2007) Dynamic DNA methylation reprogramming: Active demethylation and immediate remethylation in the male pronucleus of bovine zygotes. Dev Dynam 236, 25232533.CrossRefGoogle ScholarPubMed
Qiu, JJ, Zhang, WW, Wu, ZL, Wang, YH, Qian, M and Li, YP (2003) Delay of ZGA initiation occurred in 2-cell blocked mouse embryos. Cell Research 13, 179.CrossRefGoogle ScholarPubMed
Rangasamy, D, Berven, L, Ridgway, P and Tremethick, DJ (2003) Pericentric heterochromatin becomes enriched with H2A.Z during early mammalian development. EMBO J 22, 1599–607.CrossRefGoogle ScholarPubMed
Schultz, RM, Stein, P and Svoboda, P (2018) The oocyte-to-embryo transition in mouse: past, present and future. Biol Reprod 99, 160–74.CrossRefGoogle Scholar
Schulz, KN and Harrison, MM (2019) Mechanisms regulating zygotic genome activation. Nat Rev Genet 20, 221–34.CrossRefGoogle ScholarPubMed
Svoboda, P (2017) Mammalian zygotic genome activation. Semin Cell Dev Biol 84, 118–26.CrossRefGoogle ScholarPubMed
Vastenhouw, NL, Zhang, Y, Woods, IG, Imam, F, Regev, A, Liu, XS, Rinn, J and Schier, AF (2010) Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464, 922.CrossRefGoogle ScholarPubMed
Wang, C, Liu, X, Gao, Y, Yang, L, Li, C, Liu, W, Chen, C, Kou, X, Zhao, Y, Chen, J, Wang, Y, Le, R, Wang, H, Duan, T, Zhang, Y and Gao, S (2018) Reprogramming of H3K9me3-dependent heterochromatin during mammalian embryo development. Nat Cell Biol 20, 620–31.CrossRefGoogle ScholarPubMed
Warner, CM and Versteegh, LR (1974) In vivo and in vitro effect of alpha-amanitin on preimplantation mouse embryo RNA polymerase. Nature 248, 678–80.CrossRefGoogle ScholarPubMed
Wen, D, Banaszynski, LA, Liu, Y, Geng, F, Noh, KM, Xiang, J, Elemento, O, Rosenwaks, Z, Allis, CD and Rafii, S (2014) Histone variant H3.3 is an essential maternal factor for oocyte reprogramming. Proc Natl Acad Sci USA 111, 7325–30.CrossRefGoogle ScholarPubMed
Wu, J, Xu, J, Liu, B, Yao, G, Wang, P, Lin, Z, Huang, B, Wang, X, Li, T, Shi, S, Zhang, N, Duan, F, Ming, J, Zhang, X, Niu, W, Song, W, Jin, H, Guo, Y, Dai, S, Hu, L, Fang, L, Wang, Q, Li, Y, Li, W, Na, J, Xie, W and Sun, Y (2018) Chromatin analysis in human early development reveals epigenetic transition during ZGA. Nature 557, 256–60.CrossRefGoogle ScholarPubMed
Zheng, H, Huang, B, Zhang, B, Xiang, Y, Du, Z, Xu, Q, Li, Y, Wang, Q, Ma, J, Peng, X, Xu, F and Xie, W (2016) Resetting epigenetic memory by reprogramming of histone modifications in mammals. Mol Cell 63, 1066–79.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 J 33, 4638–52.CrossRefGoogle ScholarPubMed
Supplementary material: File

Deng et al. Supplementary material

Supplementary references

Download Deng et al. Supplementary material(File)
File 4.4 MB