105. MEIOTIC ACROBATS: MONOTREME SEX CHROMOSOME ORGANISATION DURING SPERMATOGENESIS

2010 ◽  
Vol 22 (9) ◽  
pp. 23
Author(s):  
F. Grutzner ◽  
A. Casey ◽  
T. Daish
Keyword(s):  
Sex Chromosomes ◽  
Meiotic Prophase ◽  
Sex Chromosome ◽  
National Academy Of Sciences ◽  
Prophase I ◽  
Meiotic Prophase I ◽  
Meiotic Sex Chromosome Inactivation ◽  
Y Chromosomes ◽  
Specific Order ◽  
Active Transcription

Monotremes feature an extraordinarily complex sex chromosome system which shares extensive homology with bird sex chromosomes but no homology to sex chromosomes of other mammals (1,2,3). At meiotic prophase I the ten sex chromosomes in platypus (nine in echidna) assemble in a sex chromosome chain. We previously identified the multiple sex chromosomes in platypus and echidna that form the meiotic chain in males (1,2,4). We showed that sex chromosomes assembly in the chain in a specific order (5) and that they segregate alternately (1). In secondary spermatocytes we observed clustering of X and Y chromosomes in sperm (6). Our current research investigates the formation of the synaptonemal complex, recombination and meiotic silencing of monotreme sex chromosomes. Meiotic sex chromosome inactivation (MSCI) has been observed in eutherian mammals, marsupials and birds but has so far not been investigated experimentally in monotremes. We found that during pachytene the X5Y5 end of the chain closely associates with the nucleolus and accumulates repressive chromatin marks (e.g. histone variant mH2A). In contrast to the differential accumulation of mH2A we observe extensive loading of the cohesin SMC3 on sex chromosomes in particular during the pachytene stage of meiotic prophase I. We have also used markers of active transcription and gene expression analysis to investigate gene activity in platypus meiotic cells. I will discuss how these findings contribute to our current understanding of the meiotic organisation of monotreme sex chromosomes and the evolution of MSCI in birds and mammals. (1) Grützner et al. (2004), Nature 432: 913–917.(2) Rens et al. (2007), Genome Biology 16;8(11): R243.(3) Veyrunes et al. (2008), Genome Research, 18(6): 995–1004.(4) Rens et al. (2004), Proceedings of the National Academy of Sciences USA. 101 (46): 16 257–16 261.(5) Daish et al. (2009), Reprod Fertil Dev. 21(8): 976–84.(6) Tsend-Ayush et al. (2009), Chromosoma 118(1): 53–69.

scholarly journals Dynamics of Meiotic Sex Chromosome Inactivation and Pachytene Activation in Mice Spermatogenesis

2019 ◽  
Author(s):  
Ábel Vértesy ◽  
Javier Frias-Aldeguer ◽  
Zeliha Sahin ◽  
Nicolas Rivron ◽  
Alexander van Oudenaarden ◽  
...  
Keyword(s):  
Single Molecule ◽  
Meiotic Prophase ◽  
Sex Chromosome ◽  
Chromosome Inactivation ◽  
Specific Gene ◽  
Prophase I ◽  
Meiotic Prophase I ◽  
Meiotic Sex Chromosome Inactivation ◽  
Sex Chromosome Inactivation

AbstractDuring germ cell development, cells undergo a drastic switch from mitosis to meiosis to form haploid germ cells. Sequencing and computational technologies now allow studying development at the single-cell level. Here we developed a multiplexed trajectory reconstruction to create a high-resolution developmental map of spermatogonia and prophase-I spermatocytes from testes of a Dazl-GFP reporter mouse. We identified three main transitions in the meiotic prophase-I: meiotic entry, the meiotic sex chromosome inactivation (MSCI), and concomitant pachytene activation. We validated the key features of these transitions in vivo using single molecule FISH. Focusing on MSCI, we found that 34% of sex chromosomal genes are induced shortly before MSCI, that silencing time is diverse and correlates with specific gene functions. These highlight a previously underappreciated level of regulation of MSCI. Finally, we found that spermatozoal genes in pachytene are activated in a temporal pattern reflecting the future anatomic and functional order of the sperm cell. Altogether we highlighted how precise and sequential changes in gene expression regulate cellular states in meiotic prophase-I.

scholarly journals Epigenetic Dysregulation of Mammalian Male Meiosis Caused by Interference of Recombination and Synapsis

Cells ◽  
2021 ◽  
Vol 10 (9) ◽  
pp. 2311
Author(s):  
Roberto de la Fuente ◽  
Florencia Pratto ◽  
Abrahan Hernández-Hernández ◽  
Marcia Manterola ◽  
Pablo López-Jiménez ◽  
...  
Keyword(s):  
Transcriptional Regulation ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Male Meiosis ◽  
Epigenetic Marks ◽  
Prophase I ◽  
Recombination Proteins ◽  
Meiotic Sex Chromosome Inactivation ◽  
Y Chromosomes ◽  
Genes Encoding

Meiosis involves a series of specific chromosome events, namely homologous synapsis, recombination, and segregation. Disruption of either recombination or synapsis in mammals results in the interruption of meiosis progression during the first meiotic prophase. This is usually accompanied by a defective transcriptional inactivation of the X and Y chromosomes, which triggers a meiosis breakdown in many mutant models. However, epigenetic changes and transcriptional regulation are also expected to affect autosomes. In this work, we studied the dynamics of epigenetic markers related to chromatin silencing, transcriptional regulation, and meiotic sex chromosome inactivation throughout meiosis in knockout mice for genes encoding for recombination proteins SPO11, DMC1, HOP2 and MLH1, and the synaptonemal complex proteins SYCP1 and SYCP3. These models are defective in recombination and/or synapsis and promote apoptosis at different stages of progression. Our results indicate that impairment of recombination and synapsis alter the dynamics and localization pattern of epigenetic marks, as well as the transcriptional regulation of both autosomes and sex chromosomes throughout prophase-I progression. We also observed that the morphological progression of spermatocytes throughout meiosis and the dynamics of epigenetic marks are processes that can be desynchronized upon synapsis or recombination alteration. Moreover, we detected an overlap of early and late epigenetic signatures in most mutants, indicating that the normal epigenetic transitions are disrupted. This can alter the transcriptional shift that occurs in spermatocytes in mid prophase-I and suggest that the epigenetic regulation of sex chromosomes, but also of autosomes, is an important factor in the impairment of meiosis progression in mammals.

scholarly journals Transcriptional progression during meiotic prophase I reveals sex-specific features and X chromosome dynamics in human fetal female germline

PLoS Genetics ◽  
2021 ◽  
Vol 17 (9) ◽  
pp. e1009773
Author(s):  
Xueying Fan ◽  
Ioannis Moustakas ◽  
Vanessa Torrens-Juaneda ◽  
Qijing Lei ◽  
Geert Hamer ◽  
...  
Keyword(s):  
Germ Cells ◽  
Meiotic Prophase ◽  
Sex Chromosome ◽  
Prophase I ◽  
Meiotic Prophase I ◽  
Male Gametes ◽  
Meiotic Sex Chromosome Inactivation ◽  
Transcriptomics Data ◽  
Molecular Components ◽  
Female Germline

During gametogenesis in mammals, meiosis ensures the production of haploid gametes. The timing and length of meiosis to produce female and male gametes differ considerably. In contrast to males, meiotic prophase I in females initiates during development. Hence, the knowledge regarding progression through meiotic prophase I is mainly focused on human male spermatogenesis and female oocyte maturation during adulthood. Therefore, it remains unclear how the different stages of meiotic prophase I between human oogenesis and spermatogenesis compare. Analysis of single-cell transcriptomics data from human fetal germ cells (FGC) allowed us to identify the molecular signatures of female meiotic prophase I stages leptotene, zygotene, pachytene and diplotene. We have compared those between male and female germ cells in similar stages of meiotic prophase I and revealed conserved and specific features between sexes. We identified not only key players involved in the process of meiosis, but also highlighted the molecular components that could be responsible for changes in cellular morphology that occur during this developmental period, when the female FGC acquire their typical (sex-specific) oocyte shape as well as sex-differences in the regulation of DNA methylation. Analysis of X-linked expression between sexes during meiotic prophase I suggested a transient X-linked enrichment during female pachytene, that contrasts with the meiotic sex chromosome inactivation in males. Our study of the events that take place during meiotic prophase I provide a better understanding not only of female meiosis during development, but also highlights biomarkers that can be used to study infertility and offers insights in germline sex dimorphism in humans.

scholarly journals The behavior of the X- and Y-chromosomes in the oocyte during meiotic prophase in the B6.YTIR sex-reversed mouse ovary

Reproduction ◽  
2008 ◽  
Vol 135 (2) ◽  
pp. 241-252 ◽  
Author(s):  
Michelle Alton ◽  
Mau Pan Lau ◽  
Michele Villemure ◽  
Teruko Taketo
Keyword(s):  
Y Chromosome ◽  
Germ Cells ◽  
Sex Chromosomes ◽  
Meiotic Prophase ◽  
Transcriptional Repression ◽  
Transcriptional Activity ◽  
Sex Chromosome ◽  
Nuclear Antigen ◽  
Mouse Ovary ◽  
Y Chromosomes

Sexual differentiation of the germ cells follows gonadal differentiation, which is determined by the presence or the absence of the Y-chromosome. Consequently, oogenesis and spermatogenesis take place in the germ cells with XX and XY sex chromosomal compositions respectively. It is unclear how sexual dimorphic regulation of meiosis is associated with the sex-chromosomal composition. In the present study, we examined the behavior of the sex chromosomes in the oocytes of the B6.YTIRsex-reversed female mouse, in comparison with XO and XX females. As the sex chromosomes fail to pair in both XY and XO oocytes during meiotic prophase, we anticipated that the pairing failure may lead to excessive oocyte loss. However, the total number of germ cells, identified by immunolabeling of germ cell nuclear antigen 1 (GCNA1), did not differ between XY and XX ovaries or XO and XX ovaries up to the day of delivery. The progression of meiotic prophase, assessed by immunolabeling of synaptonemal complex components, was also similar between the two genotypes of ovaries. These observations suggest that the failure in sex-chromosome pairing is not sufficient to cause oocyte loss. On the other hand, labeling of phosphorylated histone γH2AX, known to be associated with asynapsis and transcriptional repression, was seen over the X-chromosome but not over the Y-chromosome in the majority of XY oocytes at the pachytene stage. For comparison, γH2AX labeling was seen only in the minority of XX oocytes at the same stage. We speculate that the transcriptional activity of sex chromosomes in the XY oocyte may be incompatible with ooplasmic maturation.

scholarly journals Deficiency of SYCP3-related XLR3 Disrupts the Initiation of Meiotic Sex Chromosome Inactivation in Mouse Spermatogenesis

2021 ◽  
Author(s):  
Michael John O'Neill ◽  
Natali Sobel Naveh ◽  
Robert Foley ◽  
Katelyn DeNegre ◽  
Tristan Evans ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Transcriptional Repression ◽  
Sex Chromosome ◽  
Chromosome Inactivation ◽  
Nuclear Compartment ◽  
Xy Body ◽  
Meiotic Sex Chromosome Inactivation ◽  
Y Chromosomes ◽  
Multiple Clusters ◽  
Sex Chromosome Inactivation

In mammals, the X and Y chromosomes share only small regions of homology called pseudo-autosomal regions (PAR) where pairing and recombination in spermatocytes can occur. Consequently, the sex chromosomes remain largely unsynapsed during meiosis I and are sequestered in a nuclear compartment known as the XY body where they are transcriptionally silenced in a process called meiotic sex chromosome inactivation (MSCI). MSCI mirrors meiotic silencing of unpaired chromatin (MSUC), the sequestration and transcriptional repression of unpaired DNA observed widely in eukaryotes. MSCI is initiated by the assembly of the axial elements of the synaptonemal complex (SC) comprising the structural proteins SYCP2 and SYCP3 followed by the ordered recruitment of DNA Damage Response (DDR) factors to effect gene silencing. However, the precise mechanism of how unsynapsed chromatin is detected in meiocytes is poorly understood. The sex chromosomes in eutherian mammals harbor multiple clusters of SYCP3-like amplicons comprising the Xlr gene family, only a handful of which have been functionally studied. We used a shRNA-transgenic mouse model to create a deficiency in the testis-expressed multicopy Xlr3 genes to investigate their role in spermatogenesis. Here we show that knockdown of Xlr3 in mice leads to spermatogenic defects and a skewed sex ratio that can be traced to MSCI breakdown. Spermatocytes deficient in XLR3 form the XY body and the SC axial elements therein, but are compromised in their ability to recruit DDR components to the XY body.

scholarly journals Sex chromosome pairing mediated by euchromatic homology in Drosophila male meiosis

2019 ◽  
Author(s):  
Christopher A. Hylton ◽  
Katie Hansen ◽  
Andrew Bourgeois ◽  
John E. Tomkiel
Keyword(s):  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Intergenic Spacer ◽  
Male Meiosis ◽  
Early Prophase ◽  
Dna Breaks ◽  
Late Prophase ◽  
Prophase I ◽  
Y Chromosomes ◽  
Meiosis I

ABSTRACTTo maintain proper ploidy, haploid sex cells must undergo two subsequent meiotic divisions. During meiosis I, homologs pair and remain conjoined until segregation at anaphase. Drosophila melanogaster spermatocytes are unique in that the canonical events of meiosis I including synaptonemal complex (SC) formation, double-strand DNA breaks, and chiasmata are absent. Sex chromosomes pair at intergenic spacer sequences within the heterochromatic rDNA while euchromatin is required to pair and segregate autosomal homologies, suggesting that pairing may be limited to specific sequences. However, previous work generated from genetic segregation assays or observations of late prophase I/prometaphase I chromosome associations fail to differentiate pairing from conjunction. Here, we separately examined the capability of X euchromatin to pair and conjoin using an rDNA-deficient X and a series of Dp(1;Y) chromosomes. Genetic assays showed that duplicated X euchromatin can substitute for endogenous rDNA pairing sites. Segregation was not proportional to homology length, and pairing could be mapped to nonoverlapping sequences within a single Dp(1;Y). Using fluorescent in situ hybridization (FISH) to early prophase I spermatocytes, we showed that pairing occurred with high fidelity at all homologies tested. Pairing was unaffected by the presence of X rDNA, nor could it be explained by rDNA magnification. By comparing genetic and cytological data, we determined that centromere proximal pairings were best at segregation. Segregation was dependent on the conjunction protein Stromalin in Meiosis while the autosomal-specific Teflon was dispensable. Overall, our results suggest that pairing may occur at all homologies, but there may be sequence or positional requirements for conjunction.ARTICLE SUMMARYDrosophila males have evolved a unique system of chromosome segregation in meiosis that lacks recombination. Chromosomes pair at selected sequences suggesting that early steps of meiosis may also differ in this organism. Using Y chromosomes carrying portions of X material, we show that pairing between sex chromosomes can be mediated by sequences other than the previously identified rDNA pairing sites. We propose that pairing may simply be homology-based and may not differ from canonical meiosis observed in females. The main difference in males may be that conjunctive mechanisms that join homologs in the absence of crossovers.

M31 and macroH2A1.2 colocalise at the pseudoautosomal region during mouse meiosis

2001 ◽  
Vol 114 (18) ◽  
pp. 3367-3375 ◽  
Author(s):  
James M. A. Turner ◽  
Paul S. Burgoyne ◽  
Prim B. Singh
Keyword(s):  
Meiotic Prophase ◽  
Sex Chromosome ◽  
Centromeric Heterochromatin ◽  
Pseudoautosomal Region ◽  
Male And Female ◽  
Female Mice ◽  
Steroid Sulphatase ◽  
Meiotic Sex Chromosome Inactivation ◽  
Y Chromosomes ◽  
Surface Spread

Progression through meiotic prophase is associated with dramatic changes in chromosome condensation. Two proteins that have been implicated in effecting these changes are the mammalian HP1-like protein M31 (HP1β or MOD1) and the unusual core histone macroH2A1.2. Previous analyses of M31 and macroH2A1.2 localisation in mouse testis sections have indicated that both proteins are components of meiotic centromeric heterochromatin and of the sex body, the transcriptionally inactive domain of the X and Y chromosomes. This second observation has raised the possibility that these proteins co-operate in meiotic sex chromosome inactivation. In order to investigate the roles of M31 and macroH2A1.2 in meiosis in greater detail, we have examined their localisation patterns in surface-spread meiocytes from male and female mice. Using this approach, we report that, in addition to their previous described staining patterns, both proteins localise to a focus within the portion of the pseudoautosomal region (PAR) that contains the steroid sulphatase (Sts) gene. In light of the timing of its appearance and of its behaviour in sex-chromosomally variant mice, we suggest a role for this heterochromatin focus in preventing complete desynapsis of the terminally associated X and Y chromosomes prior to anaphase I.

scholarly journals Bisection of the X chromosome disrupts the initiation of chromosome silencing during meiosis in Caenorhabditis elegans

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Yisrael Rappaport ◽  
Hanna Achache ◽  
Roni Falk ◽  
Omer Murik ◽  
Oren Ram ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Rna Polymerase Ii ◽  
X Chromosome ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Transcription Analysis ◽  
X Chromosomes ◽  
Unique Character ◽  
Active Transcription ◽  
Heterogametic Sex

AbstractDuring meiosis, gene expression is silenced in aberrantly unsynapsed chromatin and in heterogametic sex chromosomes. Initiation of sex chromosome silencing is disrupted in meiocytes with sex chromosome-autosome translocations. To determine whether this is due to aberrant synapsis or loss of continuity of sex chromosomes, we engineered Caenorhabditis elegans nematodes with non-translocated, bisected X chromosomes. In early meiocytes of mutant males and hermaphrodites, X segments are enriched with euchromatin assembly markers and active RNA polymerase II staining, indicating active transcription. Analysis of RNA-seq data showed that genes from the X chromosome are upregulated in gonads of mutant worms. Contrary to previous models, which predicted that any unsynapsed chromatin is silenced during meiosis, our data indicate that unsynapsed X segments are transcribed. Therefore, our results suggest that sex chromosome chromatin has a unique character that facilitates its meiotic expression when its continuity is lost, regardless of whether or not it is synapsed.

scholarly journals The CSN/COP9 Signalosome Regulates Synaptonemal Complex Assembly during Meiotic Prophase I of Caenorhabditis elegans

PLoS Genetics ◽  
2014 ◽  
Vol 10 (11) ◽  
pp. e1004757 ◽  
Author(s):  
Heather Brockway ◽  
Nathan Balukoff ◽  
Martha Dean ◽  
Benjamin Alleva ◽  
Sarit Smolikove
Keyword(s):  
Caenorhabditis Elegans ◽  
Synaptonemal Complex ◽  
Meiotic Prophase ◽  
Cop9 Signalosome ◽  
Complex Assembly ◽  
Prophase I ◽  
Meiotic Prophase I
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