Sperm-derived histones contribute to zygotic chromatin in humans

Heijden, Godfried W. van der; Ramos, Liliana; Baart, Esther B.; Berg, I. M. van den; Derijck, Alwin A.H.A.; Vlag, Johan van der; Martini, Elena; Boer, P. de

doi:10.1186/1471-213x-8-34

Cited by 163 publications

(106 citation statements)

References 33 publications

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“…Acquisition of totipotency is thought to be mediated by extensive epigenetic reprogramming of parental genomes, affecting DNA methylation and histone modifications, and possibly replication timing and transcriptional activity in parental specific manners [1][2][3][4] . It is currently unclear to what extent differential reprogramming of maternal and paternal genomes is due to differences in chromatin states inherited from the oocyte and spermatozoon [4][5][6][7][8][9][10][11] . Beyond DNA methylation 1,2,6,12 , it is unknown which types of parental chromatin states are maintained or reprogrammed in early embryos.…”

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confidence: 99%

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Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa

Erkek

Hisano

Liang

et al. 2013

Nat Struct Mol Biol

294

373

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In mammals, fusion of two morphologically distinct gametes, oocytes and spermatozoa, leads to the formation of totipotent embryos. Acquisition of totipotency is thought to be mediated by extensive epigenetic reprogramming of parental genomes, affecting DNA methylation and histone modifications, and possibly replication timing and transcriptional activity in parental specific manners [1][2][3][4] . It is currently unclear to what extent differential reprogramming of maternal and paternal genomes is due to differences in chromatin states inherited from the oocyte and spermatozoon [4][5][6][7][8][9][10][11] . Beyond DNA methylation 1,2,6,12 , it is unknown which types of parental chromatin states are maintained or reprogrammed in early embryos. If certain parental chromatin states did escape reprogramming in the early embryo, such information could constitute an "intrinsic intergenerational epigenetic program directing gene expression in the next generation 13 . If these chromatin states also escaped reprogramming during gametogenesis, the inheritance program would function transgenerationally 13 . An increasing number of studies point to inter-or transgenerational transmission of acquired phenotypic traits that are related to temporal exposure of (grand-)parents to alternative instructive environmental cues [14][15][16][17][18] . Mechanistically, such phenotypic changes may be related to (transient) alterations of an intrinsic inheritance program.A role of histones and associated posttranslational modifications in maternal and paternal transmission of intrinsic or acquired epigenetic information is largely unknown 13 . In many metazoans, male germ cells undergo during their final differentiation into sperm an extensive chromatin remodeling process during which 3 genomic DNA becomes newly packaged into a highly condensed configuration by sperm specific proteins. In mammals, removal of histones is generally not complete 10,11,[19][20][21][22][23][24] . Furthermore, remaining histones have been reported to stay associated with the paternal genome during de novo chromatin formation in the zygote following fertilization 9 .We and others recently showed that histones lasting in human sperm are to some extent enriched at regulatory sequences of genes 10,11 . We also demonstrated that H3K4me3-and H3K27me3-marked histones are retained at promoters of specific sets of genes in mouse spermatozoa 11. The extent of evolutionary conservation of nucleosome retention at gene regulatory sequences in spermatozoa and the mechanistic principles of such retention are, however, unknown.To address conservation and to dissect the molecular logic underlying nucleosome retention, we determined the genome-wide nucleosome occupancy in mouse spermatozoa that only contain 1% residual histones. We show here that combinatorial effects of sequence composition, histone variants and histone modifications uniquely determine the packaging of sperm DNA. Nucleosomes in sperm mainly localize to unmethylated CpG-rich sequences in a histone variant specif...

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confidence: 99%

“…In mammals, removal of histones is generally not complete 10,11,[19][20][21][22][23][24] . Furthermore, remaining histones have been reported to stay associated with the paternal genome during de novo chromatin formation in the zygote following fertilization 9 .…”

mentioning

confidence: 99%

Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa

Erkek

Hisano

Liang

et al. 2013

Nat Struct Mol Biol

294

373

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“…57 The fate of paternal histones and histone modifications after fertilization remains unknown, but some retained histones stay associated with the paternal genome in the zygote. 58,59 Whether those histones and their modifications could resist further reprogramming during cellular differentiation and directly influence gene expression in differentiated cells (such as liver cells) or could be propagated into subsequent generations remains a challenging topic of research.…”

Section: Discussionmentioning

confidence: 99%

Effect of high fat diet on paternal sperm histone distribution and male offspring liver gene expression

et al. 2015

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Several studies have described phenotypic changes in the offspring of mice exposed to a variety of environmental factors, including diet, toxins, and stress; however, the molecular pathways involved in these changes remain unclear. Using a high fat diet (HFD)-induced obesity mouse model, we examined liver gene expression in male offspring and analyzed chromatin of paternal spermatozoa. We found that the hepatic mRNA level of 7 genes (out of 20 evaluated) was significantly altered in HFD male offspring compared to control mice, suggesting that phenotypic changes in the offspring depend on parental diet. We examined 7 imprinted loci in spermatozoa DNA from HFD-treated and control fathers by bisulfite sequencing, but did not detect changes in DNA methylation associated with HFD. Using chromatin immunoprecipitation followed by high-throughput sequencing, we found differential histone H3-occupancy at genes involved in the regulation of embryogenesis and differential H3K4me1-enrichment at transcription regulatory genes in HFD fathers vs. control mice. These results suggest that dietary exposure can modulate histone composition at regulatory genes implicated in developmental processes.

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“…Western blot analysis of total acid extracts has revealed that both core histones (Gatewood et al, 1987;Zalenskaya et al, 2000) and many testis-specific histone variants (TH2B, H2AX and H3.3) are all detected in human spermatozoa Van der Heijden et al, 2008) and as some reports now indicate, these histones are localised to the annular region of the human sperm nucleus (Li et al, 2008).…”

Section: Evidence For Histone Domains Retained In Spermmentioning

confidence: 99%

The effects of methyl-donor deficiency on mutation induction and transgenerational instability in mice

Voutounou

Glen

Dubrova

2012

Mutation Research/Fundamental and Molecular Mechanisms of Mutag

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Sperm-derived histones contribute to zygotic chromatin in humans

Cited by 163 publications

References 33 publications

Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa

Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa

Effect of high fat diet on paternal sperm histone distribution and male offspring liver gene expression

The effects of methyl-donor deficiency on mutation induction and transgenerational instability in mice

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