X-chromosome inactivation in monkey embryos and pluripotent stem cells

Tachibana, Masahito; Ma, Hong; Sparman, Michelle; Lee, Hyo Sang; Ramsey, Cathy; Woodward, Joy; Sritanaudomchai, Hathaitip; Masterson, Keith; Wolff, E; Jia, Yibing; Mitalipov, Shoukhrat

doi:10.1016/j.ydbio.2012.08.009

Cited by 22 publications

(12 citation statements)

References 56 publications

(92 reference statements)

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“…Therefore, although the situation appears to be controversial, the latter is consistent with earlier studies demonstrating that XIST expression in human embryos is detectable by RT-PCR in both sexes at the blastocyst stage (Daniels et al 1997, Ray et al 1997. Another study in the rhesus monkey demonstrated that, based on RT-PCR not RNA-FISH, XIST is expressed not only from both X chromosomes in females but also from a single X in males at the blastocyst stage (Tachibana et al 2012). In addition, X-liked G6PD was apparently coexpressed with XIST, suggesting that XIST RNA expressed in the blastocyst had not yet induced silencing in the rhesus monkey.…”

Section: R134 T Sado and T Sakaguchisupporting

confidence: 82%

Species-specific differences in X chromosome inactivation in mammals

Sado

Sakaguchi

2013

Reproduction

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In female mammals, the dosage difference in X-linked genes between XX females and XY males is compensated for by inactivating one of the two X chromosomes during early development. Since the discovery of the X inactive-specific transcript (XIST) gene in humans and its subsequent isolation of the mouse homolog, Xist, in the early 1990s, the molecular basis of X chromosome inactivation (X-inactivation) has been more fully elucidated using genetically manipulated mouse embryos and embryonic stem cells. Studies on X-inactivation in other mammals, although limited when compared with those in the mice, have revealed that, while their inactive X chromosome shares many features with those in the mice, there are marked differences in not only some epigenetic modifications of the inactive X chromosome but also when and how X-inactivation is initiated during early embryonic development. Such differences raise the issue about what extent of the molecular basis of X-inactivation in the mice is commonly shared among others. Recognizing similarities and differences in X-inactivation among mammals may provide further insight into our understanding of not only the evolutionary but also the molecular aspects for the mechanism of X-inactivation. Here, we reviewed species-specific differences in X-inactivation and discussed what these differences may reveal.

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Section: R134 T Sado and T Sakaguchisupporting

confidence: 82%

Species-specific differences in X chromosome inactivation in mammals

Sado

Sakaguchi

2013

Reproduction

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“…Monkey ESC colonies are usually propagated by manual dissociation to small cell clusters 13,44 rather than single cells, as enzymatic treatment results in dramatic decrease in plating efficiency (< 1%) 13 . However, to enrich haploid cells, monkey PG-haESCs should be disaggregated into single cells for FACS.…”

Section: Discussionmentioning

confidence: 99%

Generation of haploid embryonic stem cells from Macaca fascicularis monkey parthenotes

et al. 2013

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Recent success in the derivation of haploid embryonic stem cells (haESCs) from mouse via parthenogenesis and androgenesis has enabled genetic screening in mammalian cells and generation of gene-modified animals. However, whether haESCs can be derived from primates remains unknown. Here, we report the derivation of haESCs from parthenogenetic blastocysts of Macaca fascicularis monkeys. These cells, termed as PG-haESCs, are pluripotent and can differentiate to cells of three embryonic germ layers in vitro or in vivo. Interestingly, the haploidy of one monkey PG-haESC line (MPH1) is more stable compared with that of the other one (MPH2), as shown by the existence of haploid cells for more than 140 days without fluorescence-activated cell sorting (FACS) enrichment of haploid cells. Importantly, transgenic monkey PG-haESC lines can be generated by lentivirus- and piggyBac transposon-mediated gene transfer. Moreover, genetic screening is feasible in monkey PG-haESCs. Our results demonstrate that PG-haESCs can be generated from monkeys, providing an ideal tool for genetic analyses in primates.

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“…Furthermore, in these species, XIST was not imprinted, and both X chromosomes remained active in the ICM and TE of blastocysts. In addition, several studies found that the paternal X chromosome does not undergo imprinted X inactivation in human embryos and in extra-embryonic tissues (Skuse et al, 1997; Skuse, 2005; Moreira de Mello et al, 2010; Penaherrera et al, 2012; Tachibana et al, 2012). Similarly, XCI does not occur in bovine blastocysts.…”

Section: Introductionmentioning

confidence: 99%

Characterization of X-Chromosome Gene Expression in Bovine Blastocysts Derived by In vitro Fertilization and Somatic Cell Nuclear Transfer

2017

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To better understand X-chromosome reactivation (XCR) during early development, we analyzed transcriptomic data obtained from bovine male and female blastocysts derived by in-vitro fertilization (IVF) or somatic-cell nuclear transfer (SCNT). We found that X-linked genes were upregulated by almost two-fold in female compared with male IVF blastocysts. The upregulation of X-linked genes in female IVFs indicated a transcriptional dimorphism between the sexes, because the mean autosomal gene expression levels were relatively constant, regardless of sex. X-linked genes were expressed equivalently in the inner-cell mass and the trophectoderm parts of female blastocysts, indicating no imprinted inactivation of paternal X in the trophectoderm. All these features of X-linked gene expression observed in IVFs were also detected in SCNT blastocysts, although to a lesser extent. A heatmap of X-linked gene expression revealed that the initial resemblance of X-linked gene expression patterns between male and female donor cells turned sexually divergent in host SCNTs, ultimately resembling the patterns of male and female IVFs. Additionally, we found that sham SCNT blastocysts, which underwent the same nuclear-transfer procedures, but retained their embryonic genome, closely mimicked IVFs for X-linked gene expression, which indicated that the embryo manipulation procedure itself does not interfere with XCR in SCNT blastocysts. Our findings indicated that female SCNTs have less efficient XCR, suggesting that clonal reprogramming of X chromosomes is incomplete and occurs variably among blastocysts, and even among cells in a single blastocyst.

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X-chromosome inactivation in monkey embryos and pluripotent stem cells

Cited by 22 publications

References 56 publications

Species-specific differences in X chromosome inactivation in mammals

Species-specific differences in X chromosome inactivation in mammals

Generation of haploid embryonic stem cells from Macaca fascicularis monkey parthenotes

Characterization of X-Chromosome Gene Expression in Bovine Blastocysts Derived by In vitro Fertilization and Somatic Cell Nuclear Transfer

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