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The Histone Codes for Meiosis

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The Histone Codes for Meiosis REPRODUCTIONREVIEW The histone codes for meiosis Lina Wang1,2,*, Zhiliang Xu1,3,*, Muhammad Babar Khawar4, Chao Liu1 and Wei Li1 1State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, People’s Republic of China, 2University of Chinese Academy of Sciences, Beijing, People’s Republic of China, 3Key Laboratory for Major Obstetric Diseases of Guangdong Province, Key Laboratory of Reproduction and Genetics of Guangdong Higher Education Institutes, The Third Affiliated Hospital of Guangzhou Medical University, Guangzhou, People’s Republic of China and 4Department of Zoology, University of the Punjab, Lahore, Pakistan Correspondence should be addressed to W Li or C Liu; Email: [email protected] or [email protected] *(L Wang and Z Xu contributed equally to this work) Abstract Meiosis is a specialized process that produces haploid gametes from diploid cells by a single round of DNA replication followed by two successive cell divisions. It contains many special events, such as programmed DNA double-strand break (DSB) formation, homologous recombination, crossover formation and resolution. These events are associated with dynamically regulated chromosomal structures, the dynamic transcriptional regulation and chromatin remodeling are mainly modulated by histone modifications, termed ‘histone codes’. The purpose of this review is to summarize the histone codes that are required for meiosis during spermatogenesis and oogenesis, involving meiosis resumption, meiotic asymmetric division and other cellular processes. We not only systematically review the functional roles of histone codes in meiosis but also discuss future trends and perspectives in this field. Reproduction (2017) 154 R65–R79 Introduction becoming shorter and thicker. During the diplotene stage, the chromosomes start to be decondensed, and the Sexual reproduction is an essential way for higher tetrad structures can be observed clearly. Chromosomes eukaryotes to produce offspring, which aims to keep continue to condense during the diakinesis stage, the genome stable and variable. It is achieved by the nucleolus disappears and chromosomes are evenly production of haploid gametes and the fusion of these distributed in the nucleus (Keeney et al. 1997, Zickler gametes. The gametes contain half of the chromosomal & Kleckner 1999, Borner et al. 2004, Strom et al. 2007, number in somatic cell because they are produced by Lange et al. 2016). a specialized cell division with a single round of DNA Different from most of the other meiotic processes, replication, followed by two successive divisions, meiotic process of the female mammals undergoes known as meiosis. Meiosis occurs in almost all sexually two of phases arrest during oocytes maturation. First, reproducing creatures and is highly conserved from the developing oocytes arrest at diplotene stage with a single-cell eukaryotes, such as yeast, to multicellular germinal vesicle (GV) in their nucleus, and this state is eukaryotes, such as insects, fish, birds and mammals maintained until meiosis resumption at puberty or even (Clancy 1998, Yamamoto et al. 1999, Hawley 2002, later. Meiosis resumption is marked by GV breakdown Smith et al. 2008). In contrast to mitosis, meiosis starts (GVBD), which indicates the completion of prophase I from a long premeiotic DNA replication process, and the transition to meiosis I (MI). After that, the oocytes followed by prophase I. According to the chromosomal will be arrested for the second time at metaphase II (MII), configurations, meiosis prophase I can be divided into which will be activated by the fertilization with sperms leptotene, zygotene, pachytene, diplotene and diakinesis (Downs 1996). stages. At the leptotene stage, when the DNA replication Chromosomes are constituted by nucleosomes, has been completed, chromatin starts to fold and condense which are the fundamental unit of chromatin and are to form the fibrous chromosomes. When entering into the composed of DNA and various histones. Two copies zygotene stage, the chromosomes approximately line up of the four histones (H2A, H2B, H3 and H4) constitute with their homologous chromosomes, which are equal the core particle of the nucleosome by forming an in length and position. Following that is the pachytene octamer, and H1 is a linker histone for packing the stage, in which chromosomes condense further, nucleosome into higher-order structures. Histone tails © 2017 Society for Reproduction and Fertility DOI: 10.1530/REP-17-0153 ISSN 1470–1626 (paper) 1741–7899 (online) Online version via www.reproduction-online.org Downloaded from Bioscientifica.com at 10/03/2021 12:59:21AM via free access 10.1530/REP-17-0153 R66 L Wang, Z Xu and others can be substituted by their variants or modified by Table 1 Histone modifications and variants in the meiosis. various modifiers, such as acetylation, ubiquitination, Modifications/variants Function Species/cells types Reference methylation and phosphorylation, to regulate the Acetylation chromatin status (Thompson et al. 2013, Watanabe et al. H3K9ac, H3K18ac, H3K23ac Meiotic cell division Mouse/primary spermatocytes Song et al. (2011) 2013, Hiragami-Hamada et al. 2016, Kadoch et al. H3K9ac Gene transcription Primary spermatocytes Li et al. (2017) 2016), which plays essential roles in DNA replication H3K9ac Meiotic recombination Yeast Yamada et al. (2013) (Franke et al. 2016), gene transcription (Yang et al. 2016), hotspots homologous recombination (Yoon et al. 2016), DSB H3K9ac, H3K14ac, H4K5ac, Open chromatin for the Mouse/oocytes Akiyama et al. (2004), Sarmento et al. repair (Lange et al. 2016) and chromatin stability. These H4K8ac, H4K12ac, gene expression in GV (2004), Kageyama et al. (2007), H4K16ac oocytes Nagashima et al. (2007), Gu et al. (2010) histone variants and post-translational modifications H4K5ac, H4K8ac, H4K12ac Transcription in leptotene Mouse/spermatocytes Shirakata et al. (2014) (PTMs) constitute the so-called ‘histone codes’ (Fig.1; and zygotene Tang et al. 2015, Wolfe et al. 2008). More than 50 H4K8ac Chromatin remodeling in Mouse/oocytes Kim et al. (2003) histone PTMs have been identified, and this number meiosis of oocytes is growing rapidly (Grunstein 1997, Jenuwein & Allis H4K16ac Meiotic recombination Yeast Cavero et al. (2016) checkpoint 2001, Eberharter & Becker 2002, Iizuka & Smith 2003, H4K44ac Facilitates homologous Yeast Hu et al. (2015) Zentner & Henikoff 2013). Histone codes have been recombination found to participate and play important roles in meiosis Methylation (Fig. 2, Table 1 and Box 1, 2, 3 and 4) (Maleki & Keeney H3K4me1/me2/me3 Chromatin reorganization Mouse/spermatocytes Godmann et al. (2007) 2004, Hu et al. 2015, Luense et al. 2016, Xu et al. H3K4me3 Programmed DSB hotspots Yeast/mouse spermatocyte/oocytes Borde et al. (2009), Buard et al. (2009), and meiotic Brick et al. (2012), Acquaviva et al. 2016), and the functions of these histone codes during recombination initiation (2013), Sommermeyer et al. (2013) meiosis will be summarized in the following sections of H3K9me1/me2 Synapsis and genes Mouse/spermatocyte/oocytes Tachibana et al. (2007) this review. transcription H3K9me3 Synapsis and pericentric Mouse/spermatocyte Peters et al. (2001), Kato et al. (2015) The histone codes of H1in meiosis heterochromatin modification Histone H1 is the linker histone in nucleosomes, and H3K27me3 Transcriptional silencing Mouse/spermatocyte Song et al. (2011) it is important for higher-order chromatin formation H3K27me3 Transcription activation Mouse/oocytes Xu et al. (2016) Figure 1 The histone codes. The genetic information is stored in the and compaction (Izzo & Schneider 2016). The H3K36me3 Meiotic recombination Mouse/spermatocytes Powers et al. (2016) nucleus and is divided into different chromosomes. The basic units of H3K79me2 Transcriptional reactivation Mouse/spermatocytes Ontoso et al. (2014) the chromosomes are nucleosomes, which contain double-stranded histone H1 family is heterogeneous, and multiple H3K79me3 Transcription repression on Mouse/spermatocytes Ontoso et al. (2014) DNA and a histone octamer connected by a linker histone H1. H1 variants are expressed in different organisms. For centromeric regions and Various histone modifications are located at histone –NH2 or –COOH example, in humans, the histone H1 family includes the sex body tails and some histone variants form the complex histone codes. 11 different members with 7 somatic subtypes, Ubiquitination H2Aub Transcriptional silencing Mouse/spermatocyte/oocytes Baarends et al. (2005), An et al. (2010), Hasegawa et al. (2015), Luo et al. (2015) H2BK123ub Meiosis initiation and DSB Yeast Robzyk et al. (2000), Yamashita et al. (2004) formation H2BK120ub Chromatin relaxation and Mouse/spermatocyte Xu et al. (2016) homologous recombination Phosphorylation H2AT119ph Disassembly of the Drosophila/oocyte Ivanovska et al. (2005) synaptonemal complex H2AXS139ph (γH2AX) Marker of programmed Mouse/spermatocyte/oocyte Turner et al. (2005), Blanco-Rodriguez DSB and promote DSB (2012) repair in meiosis H2AS121 ph Shugoshin localization and Yeast Watanabe et al. (2012) centromeric cohesion protection in meiosis I H3S10ph Chromosome condensation Worm/tetrahymena/yeast/mammals Wei et al. (1998, 1999), Song et al. (2011) and cell division Variants H1T, TH2B, H2AX, H2AZ, Meiotic divisions and Mouse/spermatocyte Govin and Khochbin (2013), H3.3 global histone removal Montellier et al. (2013) Figure 2 Various histone modifications H3T Spermatogonial differentia-
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