X-Chromosome Inactivation in Marsupials

Cooper, D. W.; Johnston, P. G.; VandeBerg, John L.; Robinson, E. S.

doi:10.1071/zo9890411

Cited by 29 publications

(21 citation statements)

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“…Pioneering studies of protein polymorphisms in several marsupial species (for review, see Cooper et al 1990Cooper et al , 1993 indicated that inactivation of paternal X-linked genes was often incomplete, with locus-, species-, and tissue-specific levels of paternal allele leakage. However, it has remained unclear whether incomplete repression is the general pattern for marsupial X-linked genes or is a biased reflection of the small number of loci examined.…”

Section: Discussionmentioning

confidence: 99%

“…These limited data have not enabled many locus-by-locus comparisons within or among species, nor allowed extrapolation of the expression patterns of so few genes to the full X chromosome for any individual species. Thus, it remains unclear whether pXCI in marsupials is a concerted, chromosomewide phenomenon or a piecemeal process that occurs on a region-by-region basis (Cooper et al 1990;Riggs 1990;Al Nadaf et al 2010).…”

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confidence: 99%

“…In addition, genes on the marsupial inactive Xp exhibit levels of ''leaky'' or ''partial'' expression (incomplete repression) that can vary across species, as well as across tissue types, developmental stages, and cultured cells within a species (for review, see VandeBerg et al 1987;Cooper et al 1990Cooper et al , 1993; see also Samollow et al 1995;Hornecker et al 2007). However, only four marsupial X-linked genes have been examined with regard to parent-oforigin allelic and leaky expression (Cooper et al 1993), and simultaneous examination of expression from multiple X-linked loci has been reported for only one species Migeon et al 1989).…”

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Chromosome-wide profiling of X-chromosome inactivation and epigenetic states in fetal brain and placenta of the opossum, Monodelphis domestica

et al. 2013

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Evidence from a few genes in diverse species suggests that X-chromosome inactivation (XCI) in marsupials is characterized by exclusive, but leaky inactivation of the paternally derived X chromosome. To study the phenomenon of marsupial XCI more comprehensively, we profiled parent-of-origin allele-specific expression, DNA methylation, and histone modifications in fetal brain and extra-embryonic membranes in the gray, short-tailed opossum (Monodelphis domestica). The majority of X-linked genes (152 of 176 genes with trackable SNP variants) exhibited paternally imprinted expression, with nearly 100% of transcripts derived from the maternal allele; whereas 24 loci (14%) escaped inactivation, showing varying levels of biallelic expression. In addition to recently reported evidence of marsupial XCI regulation by the noncoding Rsx transcript, strong depletion of H3K27me3 at escaper gene loci in the present study suggests that histone state modifications also correlate strongly with opossum XCI. In contrast to mouse, the opossum did not show an association between X-linked gene expression and promoter DNA methylation, with one notable exception. Unlike all other X-linked genes examined, Rsx was differentially methylated on the maternal and paternal X chromosomes, and expression was exclusively from the inactive (paternal) X chromosome. Our study provides the first comprehensive catalog of parent-of-origin expression status for X-linked genes in a marsupial and sheds light on the regulation and evolution of imprinted XCI in mammals.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Chromosome-wide profiling of X-chromosome inactivation and epigenetic states in fetal brain and placenta of the opossum, Monodelphis domestica

et al. 2013

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“…Imprinted X inactivation was discovered in both embryonic and extra-embryonic tissues in marsupials (Cooper et al 1990;Al Nadaf et al 2010) and in extra-embryonic tissue (which gives rise to placenta) in eutherian mammals. Imprinted X inactivation has been reported in the mouse Lee 2001, 2005;Heard and Disteche 2006), rat (Wake et al 1976), and cow (Xue et al 2002).…”

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confidence: 99%

Random X inactivation in the mule and horse placenta

et al. 2012

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In eutherian mammals, dosage compensation of X-linked genes is achieved by X chromosome inactivation. X inactivation is random in embryonic and adult tissues, but imprinted X inactivation (paternal X silencing) has been identified in the extra-embryonic membranes of the mouse, rat, and cow. Few other species have been studied for this trait, and the data from studies of the human placenta have been discordant or inconclusive. Here, we quantify X inactivation using RNA sequencing of placental tissue from reciprocal hybrids of horse and donkey (mule and hinny). In placental tissue from the equid hybrids and the horse parent, the allelic expression pattern was consistent with random X inactivation, and imprinted X inactivation can clearly be excluded. We characterized horse and donkey XIST gene and demonstrated that XIST allelic expression in female hybrid placental and fetal tissues is negatively correlated with the other X-linked genes chromosome-wide, which is consistent with the XIST-mediated mechanism of X inactivation discovered previously in mice. As the most structurally and morphologically diverse organ in mammals, the placenta also appears to show diverse mechanisms for dosage compensation that may result in differences in conceptus development across species.

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“…Although initiation of X inactivation is generally random, there are cases of either complete or partial skewing. In marsupials (Cooper et al 1971(Cooper et al , 1990 and in certain extraembryonic lineages of rodents (Takagi and Sasaki 1975;Wake et al 1976;Zakian et al 1991), there is imprinted inactivation of the paternally derived X chromosome. Partial nonrandom X inactivation occurs in mice heterozygous at the Xce locus (Cattanach et al 1969), in interspecific vole hybrids (Zakian et al 1991), and also in humans (Naumova et al 1996;Plenge et al 1997).…”

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Skewing X chromosome choice by modulating sense transcription across theXistlocus

Nesterova¹,

Johnston²,

Appanah³

et al. 2003

Genes Dev.

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The X-inactive-specific transcript (Xist) locus is a cis-acting switch that regulates X chromosome inactivation in mammals. Over recent years an important goal has been to understand how Xist is regulated at the initiation of X inactivation. Here we report the analysis of a series of targeted mutations at the 5 end of the Xist locus. A number of these mutations were found to cause preferential inactivation, to varying degrees, of the X chromosome bearing the targeted allele in XX heterozygotes. This phenotype is similar to that seen with mutations that ablate Tsix, an antisense RNA initiated 3 of Xist. Interestingly, each of the 5 mutations causing nonrandom X inactivation was found to exhibit ectopic sense transcription in embryonic stem (ES) cells. The level of ectopic transcription was seen to correlate with the degree of X inactivation skewing. Conversely, targeted mutations which did not affect randomness of X inactivation also did not exhibit ectopic sense transcription. These results indicate that X chromosome choice is determined by the balance of Xist sense and antisense transcription prior to the onset of random X inactivation. X chromosome inactivation in mammals provides dosage compensation for X-linked genes between XX females and XY males (Lyon 1961). One of the two X chromosomes is transcriptionally silenced early in female development, leading to mosaic expression of either the maternal (Xm) or paternal (Xp) X chromosome in different cell populations. Although initiation of X inactivation is generally random, there are cases of either complete or partial skewing. In marsupials (Cooper et al. 1971(Cooper et al. , 1990 and in certain extraembryonic lineages of rodents (Takagi and Sasaki 1975;Wake et al. 1976;Zakian et al. 1991), there is imprinted inactivation of the paternally derived X chromosome. Partial nonrandom X inactivation occurs in mice heterozygous at the Xce locus (Cattanach et al. 1969), in interspecific vole hybrids (Zakian et al. 1991), and also in humans (Naumova et al. 1996;Plenge et al. 1997).X inactivation is regulated by a cis-acting master switch locus, classically referred to as the X inactivation center (Xic). The Xic functions in the in cis propagation of silencing over the entire chromosome, and is required at the initiation of X inactivation to determine how many (counting), and which (choice) X chromosomes are inactivated (for review, see Rastan and Brown 1990). The Xic has been defined at the molecular level and shown to comprise the X-inactive-specific transcript (Xist) gene and associated regulatory elements (for review, see Avner and Heard 2001). The Xist gene produces a large noncoding RNA that localizes to the inactive X chromosome in cis and induces chromosome-wide silencing (Brockdorff et al. 1992;Brown et al. 1992;Clemson et al. 1996;Wutz et al. 2002). The counting and choice functions of the Xic are thought to be attributable to cis-acting sequences that regulate Xist expression.X chromosome counting has been proposed to involve a blocking factor that binds to a...

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X-Chromosome Inactivation in Marsupials

Cited by 29 publications

References 36 publications

Chromosome-wide profiling of X-chromosome inactivation and epigenetic states in fetal brain and placenta of the opossum, Monodelphis domestica

Chromosome-wide profiling of X-chromosome inactivation and epigenetic states in fetal brain and placenta of the opossum, Monodelphis domestica

Random X inactivation in the mule and horse placenta

Skewing X chromosome choice by modulating sense transcription across theXistlocus

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