Histone Ubiquitination and Chromatin Remodeling in Mouse Spermatogenesis

Baarends, Willy M.; Hoogerbrugge, Jos W.; Roest, Henk P.; Ooms, M. P.; Vreeburg, J. T. M.; Hoeijmakers, Jan H.J.; Grootegoed, J. Anton

doi:10.1006/dbio.1998.9155

Cited by 265 publications

(234 citation statements)

References 51 publications

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“…Similarly to what has been described here, it was found that core histone acetylation did not block the binding of linker histones to nucleosomes (70) and that this modification did not have any major role for uH2A (8,9,11) as well as its very recent involvement in Polycomb silencing (10). As we pointed out, the mechanisms by which uH2A contributes to PcG silencing are not known.…”

Section: Histone H1 Equally Affects the Positioning Of The Histone Ocsupporting

confidence: 85%

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Histone H2A Ubiquitination Does Not Preclude Histone H1 Binding, but It Facilitates Its Association with the Nucleosome

Jason

Finn

Lindsey

et al. 2005

Journal of Biological Chemistry

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Histone H2A ubiquitination is a bulky posttranslational modification that occurs at the vicinity of the binding site for linker histones in the nucleosome. Therefore, we took several experimental approaches to investigate the role of ubiquitinated H2A (uH2A) in the binding of linker histones. Our results showed that uH2A was present in situ in histone H1-containing nucleosomes. Notably in vitro experiments using nucleosomes reconstituted onto 167-bp random sequence and 208-bp (5 S rRNA gene) DNA fragments showed that ubiquitination of H2A did not prevent binding of histone H1 but it rather enhanced the binding of this histone to the nucleosome. We also showed that ubiquitination of H2A did not affect the positioning of the histone octamer in the nucleosome in either the absence or the presence of linker histones.Despite the renewed interest in histone H2A/H2B ubiquitination (1-3), the functional role of uH2A 1 still remains controversial. This is in contrast to ubiquitinated H2B where a strong correlation with transcriptional activation has long been established (2), and even a molecular mechanism involving a transhistone regulatory pathway has been shown to be involved in this process (4, 5). With uH2A, there is almost as much experimental evidence for its association to actively transcribing chromatin as there is to the opposite. For instance, it was shown that nucleosomes from the transcriptionally poised hsp70 and copia genes from Drosophila contain 50% uH2A (6). Also nucleosomes containing mono-and diubiquitinated H2A were found to preferentially occur near the 5Ј-end of the transcribed mouse dihydrofolate reductase gene (7). On the other hand, early studies with rat liver nuclei linked the disappearance of uH2A to increased transcription (8), and it was shown that Drosophila nucleosomes consisting of non-transcribed 1.705 satellite DNA showed an enrichment in uH2A (9). In support of these early data, a role for histone uH2A in Polycomb silencing has been demonstrated recently (10). Furthermore uH2A has been shown to be concentrated in the heterochromatic inactive sex body in pachytene spermatocytes (11). Nevertheless the molecular mechanism(s) involved remains completely unknown.Despite the controversy, ubiquitinated histones have been associated with chromatin partially depleted of linker histones (12) and transcriptionally active or poised sequences (1, 2, 6, 7, 13) that are thought to be have a reduced linker histone content or have altered association with linker histones (for a review, see Ref. 14). However, there is evidence that suggests that histone H2A ubiquitination does not interfere with linker histone binding. Two independent studies have shown that H1 can be cross-linked to uH2A in vitro (15) and in vivo (16). Moreover, in the cross-linking studies performed in mouse cells, the molar ratio of H1-uH2A to H1-H2A was the same as the molar ratio of uH2A to H2A (16).Linker histones are required for the stabilization of well defined chromatin fibers (17-19), and interference with the binding of lin...

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Section: Histone H1 Equally Affects the Positioning Of The Histone Ocsupporting

confidence: 85%

“…In support of these early data, a role for histone uH2A in Polycomb silencing has been demonstrated recently (10). Furthermore uH2A has been shown to be concentrated in the heterochromatic inactive sex body in pachytene spermatocytes (11). Nevertheless the molecular mechanism(s) involved remains completely unknown.…”

mentioning

confidence: 74%

Histone H2A Ubiquitination Does Not Preclude Histone H1 Binding, but It Facilitates Its Association with the Nucleosome

Jason

Finn

Lindsey

et al. 2005

Journal of Biological Chemistry

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“…Other histone modifications (e.g. ubiquitination) also occur simultaneously with histone acetylation and may play roles in nucleosome destabilization for facilitating histone-to-protamine transition (130). In summary, histone epigenetic landscape can be transmitted to subsequent generation via gametes and can be targeted by environmental factors.…”

Section: Discussionmentioning

confidence: 99%

Exposure to the widely used herbicide atrazine results in deregulation of global tissue-specific RNA transcription in the third generation and is associated with a global decrease of histone trimethylation in mice

et al. 2016

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The epigenetic events imposed during germline reprogramming and affected by harmful exposure can be inherited and transferred to subsequent generations via gametes inheritance. In this study, we examine the transgenerational effects promoted by widely used herbicide atrazine (ATZ). We exposed pregnant outbred CD1 female mice and the male progeny was crossed for three generations with untreated females. We demonstrate here that exposure to ATZ affects meiosis, spermiogenesis and reduces the spermatozoa number in the third generation (F3) male mice. We suggest that changes in testis cell types originate from modified transcriptional network in undifferentiated spermatogonia. Importantly, exposure to ATZ dramatically increases the number of transcripts with novel transcription initiation sites, spliced variants and alternative polyadenylation sites. We found the global decrease in H3K4me3 occupancy in the third generation males. The regions with altered H3K4me3 occupancy in F3 ATZ-derived males correspond to altered H3K4me3 occupancy of F1 generation and 74% of changed peaks in F3 generation are associated with enhancers. The regions with altered H3K4me3 occupancy are enriched in SP family and WT1 transcription factor binding sites. Our data suggest that the embryonic exposure to ATZ affects the development and the changes induced by ATZ are transferred up to three generations.

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“…Brdt-mutant sperm is, however, capable of supporting normal embryonic development when used for intracytoplasmic sperm injection (ICSI) [80]. Histones are also ubiquitinated in elongating spermatids [81]. In particular, the E3 ubiquitin ligase Rnf8 is required for normal histone eviction during spermatogenesis [82].…”

Section: Global Chromatin Remodeling During Spermiogenesismentioning

confidence: 99%

Parental epigenetic control of embryogenesis: a balance between inheritance and reprogramming?

Gill

Erkek

Peters

2012

Current Opinion in Cell Biology

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At fertilization, fusion of two differentiated gametes forms the zygote that is capable of forming all of the varied cell lineages of an organism. It is widely thought that the acquisition of totipotency involves extensive epigenetic reprogramming of the germline state into an embryonic state. However, recent data argue that this reprogramming is incomplete and that substantial epigenetic information passes from one generation to the next. In this review we summarize the changes in chromatin states that take place during mammalian gametogenesis and examine the evidence that early mammalian embryogenesis may be affected by inheritance of epigenetic information from the parental generation.

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Histone Ubiquitination and Chromatin Remodeling in Mouse Spermatogenesis

Cited by 265 publications

References 51 publications

Histone H2A Ubiquitination Does Not Preclude Histone H1 Binding, but It Facilitates Its Association with the Nucleosome

Histone H2A Ubiquitination Does Not Preclude Histone H1 Binding, but It Facilitates Its Association with the Nucleosome

Exposure to the widely used herbicide atrazine results in deregulation of global tissue-specific RNA transcription in the third generation and is associated with a global decrease of histone trimethylation in mice

Parental epigenetic control of embryogenesis: a balance between inheritance and reprogramming?

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