Spatial Distribution of Histone Isoforms on the Bovine Active and Inactive X Chromosomes

Coppola, G.; Pinton, Alain; Joudrey, E.M.; Basrur, P.K.; King, W.A.

doi:10.1159/000117715

Cited by 19 publications

(21 citation statements)

References 103 publications

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“…However, Chadwick and Willard (6) described an enrichment of these modified histones on human Xi and noted that they are spatially distributed in regions that are nonoverlapping with regions of elevated H3K27me3. Also, in bovine models, H3K27me3 and H3K9me3 are spatially distributed in nonoverlapping regions (7). This observed pattern of the mutually exclusive presence of H3K27me3 and H3K9me3 supports our findings in the mouse and possum that although H3K27 has an enhanced presence on the mouse Xi, it is not such a clear XCI mark in the possum.…”

Section: Discussionsupporting

confidence: 85%

“…In addition, Xi chromatin is enriched in the histone variants macroH2A1 and macroH2A2 (5). In human and bovine models, H3K27me3 and H3K9me3 are spatially distributed in nonoverlapping regions (6,7). These stable histone modifications appear shortly after the accumulation of Xist RNA along the X with H3K9 methylation as the first modification occurring at the onset of XCI (8,9).…”

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confidence: 99%

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Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation

Rens

Wallduck

Lovell

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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X chromosome dosage compensation in female eutherian mammals is regulated by the noncoding Xist RNA and is associated with the differential acquisition of active and repressive histone modifications, resulting in repression of most genes on one of the two X chromosome homologs. Marsupial mammals exhibit dosage compensation; however, they lack Xist, and the mechanisms conferring epigenetic control of X chromosome dosage compensation remain elusive. Oviparous mammals, the monotremes, have multiple X chromosomes, and it is not clear whether they undergo dosage compensation and whether there is epigenetic dimorphism between homologous pairs in female monotremes. Here, using antibodies against DNA methylation, eight different histone modifications, and HP1, we conduct immunofluorescence on somatic cells of the female Australian marsupial possum Trichosurus vulpecula, the female platypus Ornithorhynchus anatinus, and control mouse cells. The two marsupial X's were different for all epigenetic features tested. In particular, unlike in the mouse, both repressive modifications, H3K9me3 and H4K20Me3, are enriched on one of the X chromosomes, and this is associated with the presence of HP1 and hypomethylation of DNA. Using sequential labeling, we determine that this DNA hypomethylated X correlates with histone marks of inactivity. These results suggest that female marsupials use a repressive histone-mediated inactivation mechanism and that this may represent an ancestral dosage compensation process that differs from eutherians that require Xist transcription and DNA methylation. In comparison to the marsupial, the monotreme exhibited no epigenetic differences between homologous X chromosomes, suggesting the absence of a dosage compensation process comparable to that in therians.DNA methylation | histone modifications | X chromosome inactivation I n mammals, X inactivation has evolved to solve the difference in X chromosome gene dosage between homogametic female mammals and heterogametic male mammals. Inactivation of one of the two female X chromosomes provides an equal dose in eutherian mammals and marsupials. In the mouse, X-chromosome inactivation (XCI) is imprinted in early development and is then reprogrammed at the blastocyst stage to become random, where, in response to expression of Xist RNA from the future inactive X (Xi), repressive histone modifications, histone variants, and DNA methylation are acquired (1, 2). This results in transcriptional repression of most X-linked genes. In particular, the eutherian Xi is late in replicating and is distinguished from the active X by a specific set of covalent histone modifications. The Xi is hypoacetylated on the NH 2 -terminal lysines of nearly all histones (3, 4) and lacks H3K4me2 and H3K4me3 but carries H3K9me2, H3K9me3, and H3K27me3 (1). In addition, Xi chromatin is enriched in the histone variants macroH2A1 and macroH2A2 (5). In human and bovine models, H3K27me3 and H3K9me3 are spatially distributed in nonoverlapping regions (6, 7). These stable histone modifications ...

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Section: Discussionsupporting

confidence: 85%

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confidence: 99%

Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation

Rens

Wallduck

Lovell

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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“…4a). The bovine Xi chromosome displays two intense H3K27me3-rich bands at metaphase [55]. During interphase, a bright, heavily labeled patch was visible in the nucleus (Fig.…”

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confidence: 94%

Nuclear Profiles of H3 Histones Trimethylated on Lys27 in Bovine (Bos taurus) Embryos Obtained after In Vitro Fertilization or Somatic Cell Nuclear Transfer

Breton

Bourhis

Audouard

et al. 2010

Journal of Reproduction and Development

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Abstract. Histone H3 trimethylation on lysine 27 is one of the histone modifications associated with chromatin of silenced regions. H3K27me3 labeling is initially asymmetrical between pronuclei in mammalian embryos, and then it is remodeled during early development. However, in mouse embryos obtained after somatic cell nuclear transfer (SCNT), H3K27me3 histones inherited from the somatic female cell and associated with X chromosome inactivation have been reported to escape remodeling. Using immunostaining, we investigated the remodeling of H3K27me3 in Bos taurus embryos obtained after in vitro fertilization (IVF) and SCNT. In this species, transfer-induced chromatin remodeling can be clearly separated from embryonic genome activation (EGA), which occurs at the 8-16-cell stage, and cloning by SCNT is 10 times more successful than in the mouse. In early IVF bovine embryos, dense H3K27me3 labeling was localized in the pericentric heterochromatin as recently described in the mouse. Labeling was however unevenly distributed up to the 8-cell stage, suggesting that the parental genomes partitioned before EGA. In female IVF blastocysts, a somatic-like female profile appeared in 21% of the trophoblast cells. This profile, which had one major nuclear H3K27me3 patch, the putative inactive X chromosome (Xi), was absent in male blastocysts. In contrast, the somatic-like female H3K27me3 profile was observed in the majority of the nuclei of female bovine SCNT embryos before EGA. At the 8-16-cell stage, this profile was transiently replaced by pericentric-like labeling in most nuclei. Immunostaining of mitotic chromosomes suggested that the ratio of H3K27me3 labeling in pericentric heterochromatin vs. euchromatin was then rapidly altered. Finally, Xi-like H3K27me3 staining appeared again in trophoblast cells in female SCNT blastocysts. These results suggest a role for EGA in H3K27me3 remodeling, which affects the heterochromatin inherited from the donor cell or produced during development. Key words: Heterochromatin, Preimplantation embryo, Somatic cloning (J. Reprod. Dev. 56: [379][380][381][382][383][384][385][386][387][388] 2010) he low developmental potential of embryos obtained after somatic cell nuclear transfer (SCNT) into oocyte cytoplasm suggests that the transformation of nuclei of differentiated cells into a fully totipotent state in the early SCNT embryo is inefficient [1]. One of the hypotheses to explain this faulty 'reprogramming' points to the different nuclear factors that make up the environment surrounding the DNA and that are transmitted by the donor cell, i.e., epigenetic factors [2,3]. Epigenetic nuclear factors include methylation of the DNA, nucleosome structure and association of non-histone proteins. In nucleosomes, covalent histone modifications have emerged as a key mechanism that is very closely linked to transcriptional regulation [46]. In the case of SCNT, the nucleus of the donor cell carries its own epigenetic structures, which are different from the ones carried by the gametes, and may preve...

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“…Taking advantage of the morphological mark provided by this translocation to distinguish inactive from active X chromosome, an examination was carried out on the spatial distribution of a variety of histone isoforms including the histone H3, trimethylated at lysine-9 (H3K9me3) and at lysine-27 (H3K27me3), and two macro histones (macroH2A1 and macroH2A2). Comparison of the active and inactivated Xs in normal and translocation carrier bovine immunostained cells revealed that the histone variants H3K9me3, H3K27me3 and macroH2A1 are preferentially concentrated and consistently located in bands on the inactivated X in both types of bovine cells, as described for the human X chromosome (Brinkman et al, 2006) whereas H3K27me3 was identified in two intense bands on the inactivated X, at Xp22 and Xq31, representing the early replication regions of the X chromosome (Coppola et al, 2008). H3K27me3 and macroH2A1 overlapped in the Xq31 region, while macroH2A1 and macro-H2A2 were localized in the pericentric regions of all bovine autosomes.…”

Section: Heterochromatin Epigenetics and Chromatin Re-modelingmentioning

confidence: 63%

Veterinary cytogenetics: past and perspective

Basrur

Stranzinger²

2008

Cytogenet Genome Res

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Cytogenetics was conceived in the late 1800s and nurtured through the early 1900s by discoveries pointing to the chromosomal basis of inheritance. The relevance of chromosomes to human health and disease was realized more than half a century later when improvements in techniques facilitated unequivocal chromosome delineation. Veterinary cytogenetics has benefited from the information generated in human cytogenetics which, in turn, owes its theoretical and technical advancement to data gathered from plants, insects and laboratory mammals. The scope of this science has moved from the structure and number of chromosomes to molecular cytogenetics for use in research or for diagnostic and prognostic purposes including comparative genomic hybridization arrays, single nucleotide polymorphism array-based karyotyping and automated systems for counting the results of standard FISH preparations. Even though the counterparts to a variety of human diseases and disorders are seen in domestic animals, clinical applications of veterinary cytogenetics will be less well exploited mainly because of the cost-driven nature of demand on diagnosis and treatment which often out-weigh emotional and sentimental attachments. An area where the potential of veterinary cytogenetics will be fully exploited is reproduction since an inherited aberration that impacts on reproductive efficiency can compromise the success achieved over the years in animal breeding. It is gratifying to note that such aberrations can now be tracked and tackled using sophisticated cytogenetic tools already commercially available for RNA expression analysis, chromatin immunoprecipitation, or comparative genomic hybridization using custom-made microarray platforms that allow the construction of microarrays that match veterinary cytogenetic needs, be it for research or for clinical applications. Judging from the technical refinements already accomplished in veterinary cytogenetics since the 1960s, it is clear that the importance of the achievements to date are bound to be matched or out-weighed by what awaits to be accomplished in the not-too-far future.

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Spatial Distribution of Histone Isoforms on the Bovine Active and Inactive X Chromosomes

Cited by 19 publications

References 103 publications

Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation

Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation

Nuclear Profiles of H3 Histones Trimethylated on Lys27 in Bovine (Bos taurus) Embryos Obtained after In Vitro Fertilization or Somatic Cell Nuclear Transfer

Veterinary cytogenetics: past and perspective

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