Abstract
During the first divisions of the female mouse embryo, the paternal X-chromosome is coated by Xist non-coding RNA and gradually silenced. This imprinted X-inactivation principally results from the apposition, during oocyte growth, of an imprint on the X-inactivation master control region: the X-inactivation center (Xic). This maternal imprint of yet unknown nature is thought to prevent Xist upregulation from the maternal X (XM) during early female development. In order to provide further insight into the XM imprinting mechanism, we applied single-cell approaches to oocytes and pre-implantation embryos at different stages of development to analyze the expression of candidate genes within the Xic. We show that, unlike the situation pertaining in most other cellular contexts, in early-growing oocytes, Xist and Tsix sense and antisense transcription occur simultaneously from the same chromosome. Additionally, during early development, Xist appears to be transiently transcribed from the XM in some blastomeres of late 2-cell embryos concomitant with the general activation of the genome indicating that XM imprinting does not completely suppress maternal Xist transcription during embryo cleavage stages. These unexpected transcriptional regulations of the Xist locus call for a re-evaluation of the early functioning of the maternal imprint on the X-chromosome and suggest that Xist/Tsix antagonist transcriptional activities may participate in imprinting the maternal locus as described at other loci subject to parental imprinting.
Highlights
The paternal and maternal genomes are not fully equivalent
Global X-inactivation center (Xic) transcription occurs in early-growing oocytes In order to analyze the transcriptional activities associated with the Xic and with X-linked genes during oogenesis, we collected early-growing MI-oocytes (n D 7), late-growing MI oocytes (n D 22), and mature MII oocytes (n D 20) from 129Sv mice of various ages (Fig. 1B)
In agreement with previous reports indicating that transcription activity is restricted to the growth phase of oogenesis, transcription could barely be detected in SN MI- or in MII-oocytes.[46,52]
Summary
Differences include the presence of parent-of-origin specific marks or “imprints,” which lead to monoallelic expression of either the maternally-inherited or paternally-inherited alleles of imprinted genes in embryonic and/or adult tissues. An extreme example of imprinting is represented by the inactivation of the paternal X chromosome (XP), which characterizes extra-embryonic tissues, as opposed to embryonic and adult tissues, which display a random inactivation of the XP or of the maternal X (XM), leading to tissues that are mosaic for the expression of X-linked genes. The XP is reactivated in the embryonic lineage to allow the establishment of random
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