Marking Xs, together and separately

Abstract

Figure 1The paired X and Y chromosomes of the mammalian spermatocyte form a unique chromatin domain, marked here by immunostaining for phosphorylated histone H2AX (green), which is not found in the autosomal domain (red, immunostained for SYCP3, a protein of the synaptonemal complex).Imprinting is an epigenetic modification that endows chromatin with a mark of parental origin 1 . In mammals, specific chromosomal regions, and whole chromosomes, are marked as maternal or paternal. The nature of the mark is not fully understood, but both methylation of DNA and chromatin modifications have been implicated. This epigenetic mark can result in differences in transcriptional activity, which is how many imprinting effects are discovered. On page 100 of this issue, Bean et al. 2 provide a new twist to the imprinting story. They find that in Caenorhabditis elegans, an unpaired X chromosome acquires a chromatin imprint during gametogenic meiosis. Singled outNematode sex is unorthodox. XX individuals are hermaphrodites and produce both sperm and eggs, whereas XO individuals are committed males, producing only sperm. Previous work 3,4 showed dimorphism in the behavior of the X chromosome in these two germ lines. In both germ lines, the X chromosome is inactive through most of meiotic prophase. But in XX individuals, the X chromosome accumulates activating histone modifications late in meiotic prophase during oogenesis, whereas the univalent, unpaired X chromosome in XO spermatocytes remains condensed and inactive.Bean et al. 2 asked if these modifications might predict differences between the maternal and paternal X chromosome in XX zygotes produced by mating XO males with XX individuals. They assayed accumulation on chromosomes of histone modifications associated with transcriptional activation-dimethylation of histone H3 at Lys4 and acetylation of H3. In early embryos they found an exceptional chromosome that did not have the histone modifications found on all other chromosomes until after several rounds of cell division. This chromosome was the paternally derived X chromosome. No such exceptional chromosome was found in the XO embryos, whose sole X chromosome is maternally derived. They found an X chromosome without activating histone modifications in the sperm pronucleus of self-progeny, but it accumulates activating histones earlier than does the X chromosome derived from XO males.What could this mean? Obviously, germline sex is important since the paternal X chromosome differs from the maternal X chromosome. But this is not the complete story, because the X chromosome from an XO male germ line has a more stable imprint than the paternal X chromosome from hermaphroditic (XX) male germ cells. So Bean et al. 2 asked if the meiotic pairing status of the X chromosome might influence the imprint, with an unpaired X chromosome acquiring a more stable imprint. They used the C. elegans sex determination system and sex-reversing mutants to show that pairing status of the X chromosome, more than germline sex, determines the chroma...

Trimethylation of Histone H3 Lysine 4 is an Epigenetic Mark at Regions Escaping Mammalian X Inactivation

“…21 Analysis of the male X and Y during spermatogenesis using an antibody for RNA polymerase II (H5) when phosphorylated at serine 2 suggest that there are several regions that escape XY inactivation (XYi), which begins at the pachytene stage of meiosis. 20,21,23,32 The reason for escaping XYi during male meiosis is yet to be determined. Comparison of H3K4me3 bands on the mouse female somatic inactive X chromosome to the male inactive X chromosome during mouse meiosis suggest that regions that are enriched in H3K4me3 and PolII (both markers of gene expression) are the same in female somatic cells and male spermatocytes.…”

Enrichment of H3K9me2 on Unsynapsed Chromatin inCaenorhabditis elegansDoes Not Targetde NovoSites

“…Moreover, as the tissue that gives rise to subsequent generations, the germ line undergoes distinctive processes during gamete formation. One distinctive aspect of germline chromatin regulation conserved in many animal species is a process called meiotic sex chromosome inactivation (MSCI), whereby the heterogametic sex chromosomes acquire histone modifications during first meiotic prophase that are consistent with a heterochromatic state (reviewed by Handel 2004 ; Kelly and Aramayo 2007 ; Maine 2010 ; Turner 2007 ). Similarly during first meiotic prophase, any homologous chromosomes that fail to synapse because of mutation, translocation, or duplication acquire elevated levels of heterochromatin-associated histone modifications in a process variably termed meiotic silencing of unpaired chromatin or meiotic silencing of unsynapsed chromosomes (MSUC) ( Maine 2010 ) .…”

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

“…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)(2)(3)(4)(5)(6). In cytological preparations, the sex body is heteropycnotic, staining more intensely than the autosomes (7).…”