Roles of histone H3K9 methyltransferases during Drosophila spermatogenesis

Ushijima, Yuta; Inoué, Yoshihiro; Konishi, Takahiro; Kitazawa, Daishi; Yoshida, Hideki; Shimaji, Kouhei; Kimurâ, Hiroshi; Yamaguchi, Masamitsu

doi:10.1007/s10577-012-9276-1

Cited by 18 publications

(18 citation statements)

References 22 publications

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“…Our study reveals that the different histone modifications, as detected by highly specific antibodies, display a complex pattern during the development of the spermatid nucleus. Recently, a study of the enzymes involved in H3K9 methylation has been published by Ushijima et al [28]. The conclusions presented seem in part to deviate from our observations but the cytology displayed by these authors is difficult to interpret and does not permit to relate to our observations.…”

Section: Introductioncontrasting

confidence: 93%

Histone modifications in the male germ line of Drosophilaa

Hennig

Weyrich

2013

BMC Dev Biol

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BackgroundIn the male germ line of Drosophila chromatin remains decondensed and highly transcribed during meiotic prophase until it is rapidly compacted. A large proportion of the cell cycle-regulated histone H3.1 is replaced by H3.3, a histone variant encoded outside the histone repeat cluster and not subject to cell cycle controlled expression.ResultsWe investigated histone modification patterns in testes of D. melanogaster and D. hydei. In somatic cells of the testis envelope and in germ cells these modification patterns differ from those typically seen in eu- and heterochromatin of other somatic cells. During the meiotic prophase some modifications expected in active chromatin are not found or are found at low level. The absence of H4K16ac suggests that dosage compensation does not take place. Certain histone modifications correspond to either the cell cycle-regulated histone H3.1 or to the testis-specific variant H3.3. In spermatogonia we found H3K9 methylation in cytoplasmic histones, most likely corresponding to the H3.3 histone variant. Most histone modifications persist throughout the meiotic divisions. The majority of modifications persist until the early spermatid nuclei, and only a minority further persist until the final chromatin compaction stages before individualization of the spermatozoa.ConclusionHistone modification patterns in the male germ line differ from expected patterns. They are consistent with an absence of dosage compensation of the X chromosome during the male meiotic prophase. The cell cycle-regulated histone variant H3.1 and H3.3, expressed throughout the cell cycle, also vary in their modification patterns. Postmeiotically, we observed a highly complex pattern of the histone modifications until late spermatid nuclear elongation stages. This may be in part due to postmeiotic transcription and in part to differential histone replacement during chromatin condensation.

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Section: Introductioncontrasting

confidence: 93%

Histone modifications in the male germ line of Drosophilaa

Hennig

Weyrich

2013

BMC Dev Biol

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“…As histone H3 is highly conserved between mammals and Drosophila , the antibody also reacts with H3K9me2 in Drosophila as demonstrated in the Drosophila testis (Ushijima et al . ).…”

Section: Resultsmentioning

confidence: 97%

Genomewide identification of target genes of histone methyltransferase dG9a during Drosophila embryogenesis

et al. 2015

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Post-translational modification of the histone plays important roles in epigenetic regulation of various biological processes. Among the identified histone methyltransferases (HMTases), G9a is a histone H3 Lys 9 (H3K9)-specific example active in euchromatic regions. Drosophila G9a (dG9a) has been reported to feature H3K9 dimethylation activity in vivo. Here, we show that the time required for hatching of a homozygous dG9a null mutant and heteroallelic combination of dG9a null mutants is delayed, suggesting that dG9a is at least partially responsible for progression of embryogenesis. Immunocytochemical analyses of the wild-type and the dG9a null mutant flies indicated that dG9a localizes in cytoplasm up to nuclear division cycle 7 where it is likely responsible for di-methylation of nucleosome-free H3K9. From cycles 8-11, dG9a moves into the nucleus and is responsible for di-methylating H3K9 in nucleosomes. RNA-sequence analysis utilizing early wild-type and dG9a mutant embryos showed that dG9a down-regulates expression of genes responsible for embryogenesis. RNA fluorescent in situ hybridization analysis further showed temporal and spatial expression patterns of these mRNAs did not significantly change in the dG9a mutant. These results indicate that dG9a controls transcription levels of some zygotic genes without changing temporal and spatial expression patterns of the transcripts of these genes.

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“…Among them, the methylation of H3K4 and plus acetylation might help to achieve a more-open chromatin configuration, whereas H3K9 and H3K27 methylation are known to be associated with a more-repressed chromatin configuration (Rathke et al, 2014), indicating a balance of “opened” and “closed” chromatin regions during the histone-to-protamine transition. As some histone methyltransferases and demethylases are detectable during spermiogenesis (Godmann et al, 2007; Liu et al, 2010; Ushijima et al, 2012), the histone methylation may be dynamically regulated in testis. Although few mouse models exist that allow precise detection of methylation activity that directly regulates histone replacement during spermiogenesis, some studies have revealed that histone methylation may modulate the histone-to-protamine transition through some other ways.…”

Section: Methylationmentioning

confidence: 99%

Essential Role of Histone Replacement and Modifications in Male Fertility

et al. 2019

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Spermiogenesis is a complex cellular differentiation process that the germ cells undergo a distinct morphological change, and the protamines replace the core histones to facilitate chromatin compaction in the sperm head. Recent studies show the essential roles of epigenetic events during the histone-to-protamine transition. Defects in either the replacement or the modification of histones might cause male infertility with azoospermia, oligospermia or teratozoospermia. Here, we summarize recent advances in our knowledge of how epigenetic regulators, such as histone variants, histone modification and their related chromatin remodelers, facilitate the histone-to-protamine transition during spermiogenesis. Understanding the molecular mechanism underlying the modification and replacement of histones during spermiogenesis will enable the identification of epigenetic biomarkers of male infertility, and shed light on potential therapies for these patients in the future.

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Roles of histone H3K9 methyltransferases during Drosophila spermatogenesis

Cited by 18 publications

References 22 publications

Histone modifications in the male germ line of Drosophilaa

Histone modifications in the male germ line of Drosophilaa

Genomewide identification of target genes of histone methyltransferase dG9a during Drosophila embryogenesis

Essential Role of Histone Replacement and Modifications in Male Fertility

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