Xist RNA is associated with the transcriptionally inactive XY body in mammalian male meiosis

Ayoub, Nabieh; Richler, Carmelit; Wahrman, J.

doi:10.1007/s004120050218

Cited by 70 publications

(44 citation statements)

References 52 publications

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“…The list includes: XY40 (Smith and Benavente 1992;Alsheimer et al 1997), BRCA1 (Scully et al 1997), ATR (Keegan et al 1996), XMR (Escalier and Garchon 2000), and also Xist RNA, a nontranslated RNA involved in the inactivation of the X chromosomes in female somatic cells and X and Y chromosomes in male meiotic cells (Ayoub et al 1997). While the function of many of these proteins remains uncertain, recent works have yielded important clues as regards the roles of BRCA1 and ATR.…”

Section: Brca1 and Atr Associate Specifically To Unsynapsed Sex Chrommentioning

confidence: 99%

Sex chromosomes, synapsis, and cohesins: a complex affair

et al. 2006

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During first meiotic prophase, homologous chromosomes are held together by the synaptonemal complex, a tripartite proteinaceous structure that extends along the entire length of meiotic bivalents. While this feature is applicable for autosomes, sex chromosomes often escape from this rule. Many species present sex chromosomes that differ between them in their morphology, length, and gene content. Moreover, in some species, sex chromosomes appear in a single dose in one of the sexes. In all of these cases, the behavior of sex chromosomes during meiosis is conspicuously affected, and this includes the assembly and dynamics of the synaptonemal complex. We review in this study the structure of the synaptonemal complex in the sex chromosomes of three groups of organisms, namely: mammals, orthopterans, and hemipterans, which present different patterns of sex chromosome structure and behavior. Of special interest is the analysis of the organization of the axial/lateral elements of the synaptonemal complex in relation to other axial structures organized along meiotic chromosomes, mainly the cohesin axis. The differences found in the behavior of both axial structures reveal that while the organization of a cohesin axis along sex chromosomes is a conserved feature in most organisms and it shows very little morphological variations, the axial/lateral elements of the synaptonemal complex present a wide range of structural modifications on these chromosomes.

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Section: Brca1 and Atr Associate Specifically To Unsynapsed Sex Chrommentioning

confidence: 99%

Sex chromosomes, synapsis, and cohesins: a complex affair

et al. 2006

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“…Previous studies demonstrated that several genes on the X chromosome are subject to transcriptional repression during meiosis, beginning at pachytene with reactivation by the spermatid stage (8,9). Furthermore, RNA polymerase II has been shown to be excluded from the XY body at pachytene (10,11). However, the mechanism and even the extent of X and Y inactivation (XYi) during spermatogenesis are not known.…”

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confidence: 99%

Dynamic histone modifications mark sex chromosome inactivation and reactivation during mammalian spermatogenesis

Khalil

Boyar

Driscoll

2004

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

172

158

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Based on the formation of the XY body at pachytene and expression studies of a few X-linked genes, the X and Y chromosomes seem to undergo transcriptional inactivation during mammalian spermatogenesis. However, the extent and the mechanism of X and Y inactivation are not known. Here, we show that both the X and Y chromosomes undergo sequential changes in their histone modifications beginning at the pachytene stage of meiosis. These changes usually are associated with transcriptional inactivation in somatic cells, and they coincide with the exclusion of the phosphorylated (active) form of RNA polymerase II from the XY body. Both sex chromosomes undergo extensive deacetylation at histones H3 and H4 and (di)methylation of lysine (K)9 on histone H3; however, there are no changes in H3-K4 methylation. These changes persist even when the XY body disappears in late pachytene, and the X and Y chromosomes segregate from one another after the first meiotic division. By the spermatid stage, histone modifications of the X and Y chromosomes revert to those of active chromatin and RNA polymerase II reengages with both chromosomes. Our observations indicate that X and Y inactivation is extensive and persists even when the X and Y chromosomes are separated in secondary spermatocytes. These findings provide insights into epigenetic programming and chromatin dynamics in the male germ line.epigenetic ͉ meiosis ͉ X inactivation ͉ chromatin ͉ methylation T he process of spermatogenesis in mammals consists of the sequential stages shown in Fig. 1, starting with diploid spermatogonia and ending in haploid sperm. At the pachytene stage ( Fig. 1), when the pairing of the homologous autosomal chromosomes occurs, the X and Y chromosomes pair only at their pseudoautosomal regions and form the sex, or XY, body (1-6). In cytological preparations, the sex body is heteropycnotic, staining more intensely than the autosomes (7). Previous studies demonstrated that several genes on the X chromosome are subject to transcriptional repression during meiosis, beginning at pachytene with reactivation by the spermatid stage (8, 9). Furthermore, RNA polymerase II has been shown to be excluded from the XY body at pachytene (10, 11). However, the mechanism and even the extent of X and Y inactivation (XYi) during spermatogenesis are not known.Unlike the inactive X in female somatic cells, the promoters of housekeeping genes on the X chromosome remain unmethylated throughout spermatogenesis in both humans and mice (8,12). Xist, the X-inactive-specific transcript gene associated with X inactivation (Xi) in female cells, is transiently transcribed in the mouse testes at pachytene and repressed again in spermatids (13,14). However, Xist transcription is not essential, given that male mice with an ablated Xist gene have normal spermatogenesis (15) and XY bodies (9, 16). Thus, the mechanisms of Xi in female somatic cells and XYi during spermatogenesis appear to have fundamental differences.Recent evidence that the XY body at pachytene is enriched for histone H3-l...

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“…The effect of the hemizygous state on Xist expression was arguably small (twofold). However, because Xist normally is expressed only at very low levels in the male germ line (several RNA copies only) (18,19), the small decrease was likely all that could be observed in the germ line. Xist is not fully up-regulated until the gene is passed on to female progeny.…”

Section: Resultsmentioning

confidence: 99%

“…During imprinted XCI, Xist is expressed for the first time from the X p at the time of zygotic gene activation in the two-cell embryo (16,17). In the paternal germ line, however, Xist RNA is expressed only at low levels, suggesting that it is not required for spermatogenesis (18,19). Consistent with this notion, male mice with an Xist deletion are fertile (12,20).…”

mentioning

confidence: 84%

Xist imprinting is promoted by the hemizygous (unpaired) state in the male germ line

Sun

Payer

Namekawa

et al. 2015

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

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This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2015. Contributed by Jeannie T. Lee, October 1, 2015 (sent for review July 29, 2015; reviewed by Nora Engel and Kathrin Plath)The long noncoding X-inactivation-specific transcript (Xist gene) is responsible for mammalian X-chromosome dosage compensation between the sexes, the process by which one of the two X chromosomes is inactivated in the female soma. Xist is essential for both the random and imprinted forms of X-chromosome inactivation. In the imprinted form, Xist is paternally marked to be expressed in female embryos. To investigate the mechanism of Xist imprinting, we introduce Xist transgenes (Tg) into the male germ line. Although ectopic high-level Xist expression on autosomes can be compatible with viability, transgenic animals demonstrate reduced fitness, subfertility, defective meiotic pairing, and other germ-cell abnormalities. In the progeny, paternal-specific expression is recapitulated by the 200-kb Xist Tg. However, Xist imprinting occurs efficiently only when it is in an unpaired or unpartnered state during male meiosis. When transmitted from a hemizygous father (+/Tg), the Xist Tg demonstrates paternalspecific expression in the early embryo. When transmitted by a homozygous father (Tg/Tg), the Tg fails to show imprinted expression. Thus, Xist imprinting is directed by sequences within a 200-kb X-linked region, and the hemizygous (unpaired) state of the Xist region promotes its imprinting in the male germ line.Xist | imprinting | X inactivation | transgenerational inheritance | meiotic silencing by unpaired DNA

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Xist RNA is associated with the transcriptionally inactive XY body in mammalian male meiosis

Cited by 70 publications

References 52 publications

Sex chromosomes, synapsis, and cohesins: a complex affair

Sex chromosomes, synapsis, and cohesins: a complex affair

Dynamic histone modifications mark sex chromosome inactivation and reactivation during mammalian spermatogenesis

Xist imprinting is promoted by the hemizygous (unpaired) state in the male germ line

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