Abstract
Epigenetic marks, such as DNA methylation and posttranslational modifications of core histones, are the key regulators of gene expression. In the mouse, many of these marks are erased during gamete formation and must be introduced de novo after fertilization. Some of them appear synchronously, but the others are deposited asynchronously and/or remain differently distributed on maternal and paternal chromatin. Although the mechanisms regulating these processes are not entirely understandable, it is commonly accepted that epigenetic reprogramming occurring during the first cell cycle of a mouse embryo is crucial for its further development. This chapter focuses on selected epigenetic modifications, such as DNA methylation, the introduction of histone variants, histones acetylation, phosphorylation, and methylation. Properly depositing these marks on maternal and paternal chromatin is crucial for normal embryonic development.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abe K, Funaya S, Tsukioka D, Kawamura M, Suzuki Y, Suzuki MG, Schultz RM, Aoki F (2018) Minor zygotic gene activation is essential for mouse preimplantation development. PNAS 115:6780–6788
Adams RR, Maiato H, Earnshaw WC, Carmena M (2001) Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction and chromosome segregation. J Cell Biol 153:865–880
Adenot PG, Szollosi MS, Geze M, Renard JP, Debey P (1991) Dynamics of paternal chromatin changes in live one-cell mouse embryo after natural fertilization. Mol Reprod Dev. 28:23–34
Adenot PG, Mercier Y, Renard JP, 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 124:4615–4625
Ajiro K, Yasuda H, Tsuji H (1996) Vanadate triggers the transition from chromosome condensation to decondensation in a mitotic mutant (tsTM13) inactivation of p34cdc2/H1 kinase and dephosphorylation of mitosis-specific histone H3. Eur J Biochem 241:923–930
Akiyama T, Suzuki O, Matsuda J, Aoki F (2011) Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos. PLoS Genet 7(10):e1002279
Amor DJ, Kalitsis P, Sumer H, Choo KHA (2004) Building the centromere: from foundation proteins to 3D organization. Trends Cell Biol 14:359–368
Arney KL, Siqin B, Bannister AJ, Kouzarides T, Surani MA (2002) Histone methylation defines epigenetic asymmetry in the mouse zygote. Int J Dev Biol 46:317–320
Arpanahi A, Brinkworth M, Iles D, Krawetz SA, Paradowska A, Platts AE, Saida M, Steger K, Tedder P, Miller D (2009) Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res 19:1338–1349
Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas EJ 3rd, Gingeras TR et al (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120:169–181
Bošković A, Bender A, Gall L, Ziegler-Birling C, Beaujean N, Torres-Padilla ME (2012) Analysis of active chromatin modifications in early mammalian embryos reveals uncoupling of H2A.Z acetylation and H3K36 trimethylation from embryonic genome activation. Epigenetics 7:747–757
Bouniol-Baly C, Nguyen E, Besombes D, Debey P (1997) Dynamic organization of DNA replication in one-cell mouse embryos: Relationship to transcriptional activation. Exp Cell Res 236:201–211
Boyarchuk E, Montes de Oca R, Almouzni G (2011) Cell cycle dynamics of histone variants at the centromere, a model for chromosomal landmarks. Curr Opin Cell Biol 23:266–276
Brunner AM, Nanni P, Mansuy IM (2014) Epigenetic marking of sperm by post-translational modification of histones and protamines. Epigenetics Chromatin 7:2
Burton A, Brochard V, Galan C, Ruiz-Morales ER, Rovira Q et al (2021) Heterochromatin establishment during early mammalian development is regulated by pericentromeric RNA and characterized by non-repressive H3K9me3. Nat Cell Biol 22:767–778
Carone BR, Hung J-H, Hainer SJ, Chou M-T, Carone DM, Weng Z, Fazzio TG, Rando OJ (2014) High-resolution mapping of chromatin packaging in mouse embryonic stem cells and sperm. Dev Cell 30:11–22
Creyghton MP, Markoulaki S, Levine SS, Hanna J, Lodato MA, Sha K, Young RA, Jaenish R, Boyer LA (2008) H2A.Z is enriched at polycomb complex target genes in ES cells and is necessary for lineage commitment. Cell 135:649–661
Demond H, Kelsey G. (2020) The enigma of DNA methylation in the mammalian oocyte [version 1; peer review]. F1000Res 9:F1000 Faculty Rev 146. https://doi.org/10.12688/f1000research.21513.1
Erkek S, Hisano M, Liang CY, Gill M, Murr R, Dieker J, Schubeler D, van der Vlag J, Stadler MB, Peters AH (2013) Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa. Nat Struct Mol Biol 20:868–875
Faast R, Thonglairoam V, Schulz TC, Beall J, Wells JR, Taylor H, Matthaei K, Rathjen PD, Tremethick DJ, Lyons I (2001) Histone variant H2A.Z is required for early mammalian development. Curr Biol 11:1183–1187
Giet R, Glover DM (2001) Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Biol 152:669–682
Guenatri M, Bailly D, Maison C, Almouzni G (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166:493–505
Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77–88
Guo F, Li X, Liang D, Li T, Zhu P, Guo H, Wu X, Wen L, Gu T-P, Hu B, Walsh CP, Li J, Tang F, Xu G-L (2014) Active and passive demethylation of male and female pronuclear DNA in mammalian zygote. Cell Press 15:447–458
Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR (2009) Distinctive chromatin in human sperm packages genes for embryo development. Nature 460:473–478
Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R et al (2003) The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol 161:281–294
Hendzel MJ, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones D, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily with pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360
Howlett SK, Bolton VN (1985) Sequence and regulation of morphological and molecular events during the first cell cycle of mouse embryogenesis. J Embryol Exp Morphol 87:175–206
Jeong YS, Cho S, Park JS, Ko Y, Kang Y-K (2010) Phosphorylation of serine 10 of histone H3 shields modified lysine-9 selectively during mitosis. Genes Cells 15:181–192
Kawamura M, Funaya S, Sugie K, Suzuki MG, Aoki F (2021) Asymmetrical deposition and modification of histone variants are essential for zygote development. Life Sci Alliance 4(8):e202101102
Kim JM, Liu H, Tazaki M, Nagata M, Aoki F (2003) Changes in histone acetylation during mouse oocyte meiosis. J Cell Biol 162:37–46
Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, Yayoi O, Sato S, Nakabayashi K, Hata K, Sotomaru Y, Suzuki Y, Kono T (2012) Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet 8:1–14
Kouzarides T (2007) Chromatin modification and their function. Cell 128:693–705
Lan J, Lepikhov K, Giehr P, Walter J (2017) Histone and DNA methylation control by H3 serine/threonine 11 phosphorylation in the mouse zygote. Epigenetics Chromatin 10:5
Lin C-J, Conti M, Ramalho-Santos M (2013) Histone variant H3.3 maintains decondensed chromatin state essential for mouse preimplantation development. Development 140:3624–3634
Liu H, Kim J-M, Aoki F (2004) Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos. Development 131:2269–2280
Loyola A, Almouzni G (2007) Marking histone H3 variants: how, when and why? Trends Biochem Sci 32:425–433
Luense LJ, Wang X, Schon SB, Weller AH, Shiao EL, Bryant JM, Bartolomei MS, Coutifaris C, Garcia BA, Berger SL (2016) Comprehensive analysis of histone post-translational modifications in mouse and human male germ cells. Epigenetics Chromatin 9:24
Ma P, Schultz R (2008) Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Dev Biol 319:110–120
Ma X-S, Chao S-B, Huang X-J, Lin Q, Wang X-G et al (2015) The dynamics and regulatory mechanism of pronuclear H3k9me2 asymmetry in mouse zygotes. Sci Rep 5:17924
Maison C, Bailly D, Peters AHFM, Quivy J-P, Roche D, Taddei A, Lachner M, Jenuwein T, Almouzni G (2002) Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet 30:329–334
Margueron R, Reinberg D (2011) The polycomb complex PRC2 and its mark in life. Nature 469:343–349
Martens JHA, O’Sullivan RJ, Braunschweig U, Opravil S, Radolf M, Steilein P, Junwein T (2005) The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J 24:800–812
Martin C, Beaujean N, Brochard V, Audouard C, Zink D, Debey P (2006) Genome restructuring in mouse embryos during reprogramming and early development. Dev Biol 292:317–332
Mayer T, Niveleau A, Walter J, Fundele R, Haaf T (2000) Demethylation of the zygotic paternal genome. Nature 403:501–502
Meglicki M, Zientarski M, Borsuk E (2008) Constitutive heterochromatin during mouse oogenesis: the pattern of histone H3 modifications and localization of HP1a and HP1b proteins. Mol Reprod Dev 75:414–428
Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H, Sekimoto T, Ikawa M, Yoneda Y, Okabe M et al (2007) PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol 9:64–71
Nakamura T, Liu Y-J, Nakashima H et al (2012) PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 486:415–419
Nashun B, Yukawa M, Liu H, Akiyama T, Aoki F (2010) Changes in the nuclear deposition of histone H2A variants during pre-implantation development in mice. Development 137:3785–3794
Nowak SJ, Corces VG (2000) Phosphorylation of histone H3 correlates with transcriptionally active loci. Genes Dev 14:3003–3013
Pérez-CadahÃa B, Drobic B, Davie JR (2009) H3 phosphorylation: dual role in mitosis and interphase. Biochem Cell Biol 87:695–709
Peters AH, O’Carroll D, Scherthan H, Mechtler K, Sauer S, Schöfer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A et al (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323–337
Prigent C, Dimitrov S (2003) Phosphorylation of serine 10 in histone H3, what for? J Cell Sci 116:3677–3685
Ribeiro-Mason K, Boulesteix C, Fleurot R, Aguirre-Lavin T, Adenot P, Gall L, Debey P, Beaujean N (2012) H3S10 phosphorylation marks constitutive heterochromatin during interphase in early mouse embryos until the 4-cell stage. J Reprod Dev 58:467–475
Rice JC, Briggs SD, Ueberheide B, Barber CM, Shabanowitz J, Hunt DF, Shinkai Y, Allis CD (2003) Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 12:1591–1598
Simon JA, Kingston RE (2009) Mechanisms of Polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10(10):697–708
Steger K (1999) Transcriptional and translational regulation of gene expression in haploid spermatids. Anat Embryol (Berl) 199:471–487
Sullivan BA, Karpen GH (2004) Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat Struct Mol Biol 11:1076–1083
Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H, Shinkai Y (2002) G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 16:1779–1791
Tachibana M, Ueda J, Fukuda M, Takeda N, Ohta T, Iwanari H, Sakihama T, Kodama T, Hamakubo T, Shinkai Y (2005) Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at h3-K9. Genes Dev 19:815–826
Tachibana M, Nozaki M, Takeda N, Shinkai Y (2007) Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO J 26:3346–3359
Teperek-Tkacz M, Meglicki M, Pasternak M, Kubiak JZ, Borsuk E (2010) Phosphorylation of histone H3 serine 10 in early mouse embryos. Active phosphorylation at lates S phase and differential effects of ZM447439 on first two embryonic mitoses. Cell Cycle 9:1–14
van der Heijden GW, Dieker JW, Derijck AA et al (2005) Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech Dev 122:1008–1022
Wagschal A, Sutherland HG, Woodfine K, Henckel A, Chebli K, Schulz R, Oakey RJ, Bickmore WA, Feil R (2008) G9a histone methyltransferase contributes to imprinting in the mouse placenta. Mol Cell Biol 28:1104–1113
Wang Q, Wang C-M, Ai J-S, Xiong B, Yin S, Hou Y, Chen D-Y, Schatten H, Sun Q-Y (2006) Histone phosphorylation and pericentromeric histone modifications in oocyte meiosis. Cell Cycle 5:1974–1198
Wee G, Koo DB, Song BS et al (2006) Inheritable histone H4 acetylation of somatic chromatins in cloned embryos. J Biol Chem 281:6048–6057
Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD (1998) Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc Natl Acad Sci USA 95:7480–7484
Wu BJ, Dong FL, Ma XS, Wang XG, Lin F, Liu HL (2014) Localization and expression of histone H2A variants during mouse oogenesis and preimplantation embryo development. Genet Mol Res 13:5929–5939
Yeo S, Lee K-K, Han Y-M, Kang Y-K (2005) Methylation changes of lysine 9 of histone H3 during preimplantation mouse development. Mol Cells 20:423–428
Yeung WKA, Amor JB, Hatano Y, Yamagata K, Feil R, Lorincz M, Tachibana M, Shinkai Y, Sasaki H (2019) Histone H3K9 methyltransferase G9a in oocytes is essential for preimplantation development but dispensable for CG methylation protection. Cell Rep 27:282–293
Zatsepina O, Baly C, Chebrout M, Debey P (2003) The step-wise assembly of a functional nucleolus in preimplantation mouse embryos involves the cajal (coiled) body. Dev. Biol. 253:66–83
Zeng F, Schultz RM (2005) RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Dev Biol 283:40–57
Zippo A, Serafini R, Rocchigiani M, Pennacchini S, Krepelova A, Oliviero S (2009) Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138:1122–1136
Zylicz JJ, Dietmann S, Gunesdogan U, Hackett JA, Cougot D, Lee C, Surani MA (2015) Chromatin dynamics and the role of G9a in gene regulation and enhancer silencing during early mouse development. eLife 4:e09571
Zylicz JJ, Borensztein M, Wong FCK, Huang Y, Lee C, Surani A (2018) G9a regulates temporal preimplanation developmental program and lineage segregation in blastocyst. Elife 7:e33361
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Borsuk, E., Michalkiewicz, J., Kubiak, J.Z., Kloc, M. (2022). Histone Modifications in Mouse Pronuclei and Consequences for Embryo Development. In: Kloc, M., Kubiak, J.Z. (eds) Nuclear, Chromosomal, and Genomic Architecture in Biology and Medicine. Results and Problems in Cell Differentiation, vol 70. Springer, Cham. https://doi.org/10.1007/978-3-031-06573-6_14
Download citation
DOI: https://doi.org/10.1007/978-3-031-06573-6_14
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-06572-9
Online ISBN: 978-3-031-06573-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)