Transmission of Y chromosomes from XY female mice was made possible by the replacement of cytoplasm during oocyte maturation

Obata, Yayoi; Villemure, Michele; Kono, Toru; Taketo, Teruko

doi:10.1073/pnas.0802680105

Cited by 16 publications

(27 citation statements)

References 52 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This leads to gonads blocked in an apparently undifferentiated state ( [31] and references therein). Moreover, recall that absence or dysfunction of SRY in an XY background generally leads to a streak gonad or to an impaired ovary, [13,32] which argues for the existence of autonomous signal(s) in the somatic cells but also of signals resulting from a dialog with the gonocytes that would help in the making of a functional ovary. The contrary remains to be shown but is highly predictable.…”

Section: Foxl2: a Molecular Actor In The Spotlightmentioning

confidence: 99%

FOXL2 versus SOX9: A lifelong “battle of the sexes”

Veitia

2010

BioEssays

View full text Add to dashboard Cite

Testis determination in most mammals is regulated by a genetic hierarchy initiated by the SRY gene. Early ovarian development has long been thought of as a default pathway switched on passively by the absence of SRY. Recent studies challenge this view and show that the ovary constantly represses male-specific genes, from embryonic stages to adulthood. Notably, the absence of the crucial ovarian transcription factor FOXL2 (alone or in combination with other factors) induces a derepression of male-specific genes during development, postnatally and, even more interestingly, during adulthood. Strikingly, in the adult, targeted ablation of Foxl2 leads to a molecular transdifferentiation of the supporting cells of the ovary, which acquire cytological and transcriptomic characteristics of the supporting cells of the testes. These studies bring many answers to the field of gonadal determination, differentiation and maintenance, but also open many questions. Keywords:.F OXL2; ovary determination; ovarian maintenance IntroductionGonadal sex determination is a process that implies a unique decision to make a testis or an ovary out of a bipotential primordium. In most mammals, sex determination is equated with testis determination, whereas ovarian determination has been considered a default process. That is, absence of the testisdetermining factor would automatically lead to the development of an ovary (in appropriate conditions). Recent articles challenge this view and show that in the ovary active mechanisms are required to maintain the differentiated state. [1,2] The bipotential gonad is made up of four presumptive cell lineages: germ cells (which have an extraembryonic origin) and three types of somatic cells. The somatic component involves the supporting cell precursors, which will give rise to Sertoli cells in the male or granulosa cells in the female, the steroidogenic precursors, which differentiate into Leydig cells (male) and theca cells (female), and finally the connective tissue cells yielding other important structures. [3] From a genetic perspective, the SRY gene is pivotal in switching on the testis-determining cascade.[4] Indeed, murine Sry transcripts appear in the presumptive Sertoli cells from 10.5 days postcoitum and for about 2 days, at the right moment for testis determination. [5] In other mammals, including man, SRY is expressed from the period of testis determination until adulthood [6]). It seems now that the main task of Sry/SRY is to directly activate the gene Sox9, which also encodes a transcription factor. Recently a gonad-specific enhancer that mediates testis Sox9 expression, called TESCO, has been identified. [7] Indeed, Sry along with the steroidogenic factor 1 (Sf1) binds to multiple elements within the TESCO. Moreover, mutation, co-transfection, and sex-reversal studies suggest the existence of a positive feedback circuit. First, Sf1 and Sry cooperatively up-regulate Sox9 transcription. Then, Sox9 and Sf1 recognize the enhancer to maintain the expression of the former in the absence of Sr...

show abstract

Section: Foxl2: a Molecular Actor In The Spotlightmentioning

confidence: 99%

FOXL2 versus SOX9: A lifelong “battle of the sexes”

Veitia

2010

BioEssays

View full text Add to dashboard Cite

show abstract

“…Our previous studies have shown that the MII-oocytes from XY females are defective in their cytoplasm, which causes abnormal MII-spindle assembly and blocks subsequent embryonic development (Obata et al, 2008). These defects can be overcome by transferring the nucleus of the XY oocyte into an enucleated XX oocyte, more efficiently when the nuclear transfer is performed at the GV-stage than at the MII-stage.…”

Section: Low Glycolytic Gene Expression In the Ccs Of Xy Cocs Is Revementioning

confidence: 96%

“…Our previous studies have shown that when COCs are collected from XY antral follicles and immediately subjected to IVM, the enclosed oocytes reach the MII-stage but their meiotic spindles are morphologically abnormal, resulting in a zygotic developmental failure (Villemure et al, 2007;Obata et al, 2008). Our current studies indicated that while ATP contents in fully grown XY oocytes were lower than those in XX oocytes when collected from antral follicles, they increased to comparable levels after COCs were incubated in the presence of milrinone for 20 h (preincubation).…”

Section: Preincubation Of Cocs In the Presence Of Milrinone Followedmentioning

confidence: 99%

“…We have previously reported that the infertility of the XY female mouse is intrinsic to its oocytes; all XX-XY chimeric females are fertile and produce offspring only derived from XX oocytes (Amleh and Taketo, 1998). Furthermore, the XY oocytes collected from antral follicles can reach the second meiotic metaphase (MII) in culture, but they contain abnormal MII-spindles and fail in proper chromosome segregation upon fertilization or parthenogenic activation (Amleh et al, 1996;Obata et al, 2008;Villemure et al, 2007). This spindle defects can largely be attributed to the XY ooplasm because healthy pups are produced from the nuclei of XY oocytes which have been transferred into enucleated XX oocytes (Obata et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, the XY oocytes collected from antral follicles can reach the second meiotic metaphase (MII) in culture, but they contain abnormal MII-spindles and fail in proper chromosome segregation upon fertilization or parthenogenic activation (Amleh et al, 1996;Obata et al, 2008;Villemure et al, 2007). This spindle defects can largely be attributed to the XY ooplasm because healthy pups are produced from the nuclei of XY oocytes which have been transferred into enucleated XX oocytes (Obata et al, 2008). To identify the defective cytoplasmic components in the XY oocyte, we compared gene expression profiles in the fullygrown oocytes collected from XX and XY females by cDNAmicroarray (Xu et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Bi-directional communication with the cumulus cells is involved in the deficiency of XY oocytes in the components essential for proper second meiotic spindle assembly

Noohi

Shin

et al. 2014

Developmental Biology

Self Cite

View full text Add to dashboard Cite

The oocyte becomes competent for embryonic development by involving mutual communication with cumulus cells (CCs) during folliculogenesis. How this communication takes place under physiological conditions is not fully understood. Current study examined oocyte-CCs communication in the XY sex-revered female mouse. We have previously found that the XY oocyte is defective in its cytoplasm, causing abnormal MII-spindle assembly and a failure in embryonic development. Our present study showed that transcript levels of Pfkp, Pkm2 and Ldh1 involved in glycolysis were lower in the CCs surrounding XY oocytes than in those surrounding XX oocytes. ATP contents in XY oocytes were also lower than those in XX oocytes, suggesting that lower glycolytic gene expression in CCs resulted in lower ATP contents in the enclosed oocyte. Co-culture of oocytectomized CC-oocyte complexes (COCs) with denuded oocytes showed that XY oocytes were less efficient than XX oocytes in promoting glycolytic gene expression in CCs. Furthermore, both glycolytic gene expression levels in CCs and ATP contents in oocytes of XY COCs increased to similar levels to those of XX COCs after culture for 20h in the presence of milrinone (=preincubation), which prevented spontaneous oocyte maturation. By increasing ATP levels in XY oocytes by either COC preincubation or ATP microinjection into oocytes prior to in vitro maturation, an improvement in MII-spindle assembly was observed. We conclude that the XY oocyte produces lesser amounts of paracrine factors that affect its companion CCs, which in turn make the ooplasm deficient in its components, including ATP, essential for MII-spindle assembly.

show abstract

Oocyte heterogeneity with respect to the meiotic silencing of unsynapsed X chromosomes in the XY female mouse

Taketo

Naumova

2013

Chromosoma

View full text Add to dashboard Cite

In the XY pachytene spermatocyte, the sex chromosomes do not synapse except for the pseudoautosomal region and become transcriptionally silenced. It has been suggested that the meiotic silencing of unsynapsed chromatin (MSUC) also occurs in oocytes. In the XY sex-reversed female mouse, the sex chromosomes fail to pair in the majority of oocytes and a greater number of oocytes are eliminated during the meiotic prophase compared to the XX female. Yet, many XY oocytes survive to reach the second meiotic metaphase. The goal of our current study was to determine whether the single X chromosome shows the characteristics of asynapsis and meiotic silencing in a proportion of XY oocytes, which can explain the survival of the remaining oocytes. We first examined the accumulation of markers associated with asynapsis or transcriptional silencing, i.e., BRCA1, γH2AX, H3K9me3, and H3K27me3, at the single X chromosome in the XY oocyte. We found that γH2AX and BRCA1 were enriched on the single X chromosome whereas H3K9me3 was not, and H3K27me3 was enriched at all chromosomes in the majority of XY oocytes. We next examined the meiotic silencing of the single X chromosome using enrichment of the X-encoded ATRX protein. On average, ATRX enrichment was lower in XY oocytes than in XX oocytes as expected from its half gene dosage. However, the intensity of ATRX staining in XY oocytes harboring γH2AX domains showed a remarkable heterogeneity. We conclude that MSUC occurs with varying consequences, resulting in a heterogeneous population of oocytes with respect to protein enrichment in the XY female mouse.

show abstract

Transmission of Y chromosomes from XY female mice was made possible by the replacement of cytoplasm during oocyte maturation

Cited by 16 publications

References 52 publications

FOXL2 versus SOX9: A lifelong “battle of the sexes”

FOXL2 versus SOX9: A lifelong “battle of the sexes”

Bi-directional communication with the cumulus cells is involved in the deficiency of XY oocytes in the components essential for proper second meiotic spindle assembly

Oocyte heterogeneity with respect to the meiotic silencing of unsynapsed X chromosomes in the XY female mouse

Contact Info

Product

Resources

About