Rapid evolution of primate ESX1 , an X-linked placenta- and testis-expressed homeobox gene

Wang, Xiaoxia; Zhang, Jianzhi

doi:10.1093/hmg/ddm153

Cited by 18 publications

(16 citation statements)

References 46 publications

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“…The Tex19 gene was first identified as a unique gene and with a male germ cell-specific expression [11]. Subsequently, we showed that Tex19 is duplicated in the mouse and rat, giving rise to Tex19.1 and Tex19.2 paralogs [2].…”

Section: Discussionmentioning

confidence: 99%

“…Many genes have been ascribed a specific expression either in somatic or germ cells in the gonads and in placental cell populations. This is the case for Esx1 [11] and a cluster of genes representing the Rhox homeobox gene family, which includes Rhox5 (or Pem) [12], Rhox6 (or Psx1) [13] and Rhox9 (also known as Psx2 or Gpbox) [14]. Three of these genes have been successfully ablated in the mouse.…”

Section: Discussionmentioning

confidence: 99%

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<i>Tex 19</i> Paralogs Exhibit a Gonad and Placenta-Specific Expression in the Mouse

et al. 2012

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Abstract.We have previously suggested that TEX19, a mammalian-specific protein of which two paralogs exist in rodents, could be implicated in stem cell self-renewal and pluripotency. We have established here the expression profiles of Tex19.1 and Tex19.2 during mouse development and adulthood. We show that both genes are coexpressed in the ectoderm and then in primordial germ cells (PGCs). They are also coexpressed in the testis from embryonic day 13.5 to adulthood, whereas only Tex19.1 transcripts are detected in the developing and adult ovary as well as in the placenta and its precursor tissue, the ectoplacental cone. The presence of both Tex19.1 and Tex19.2 in PGCs, gonocytes and spermatocytes opens the possibility that these two genes could play redundant functions in male germ cells. Furthermore, the placental expression of Tex19.1 can explain why Tex19.1 knockout mice show embryonic lethality, in addition to testis defects. T ex19 (Testis expressed gene 19) was initially identified as testis specific through a cDNA subtraction strategy [1]. Tex19 is restricted to mammals, is present as a unique gene in humans, and has been duplicated in the mouse and rat giving rise to the paralogs Tex19.1 and Tex19.2. Through protein comparison in 11 mammalian species, two highly Tex19-conserved domains named MCP and VPTEL domains have been characterized [2]. However, none of them shares homologies with known proteins, therefore preventing any functional prediction. Interestingly, an N-Ter cysteine was recently found to be bound to Ubr2, which may help Tex19 stabilization [3].Analysis of Tex19.1 knockout (KO) mice highlights a critical role for Tex19 in spermatogenesis, where it seems to act as a repressor of transposable elements. It was also reported that about half of the homozygous pups are missing, suggesting a function of Tex19.1 in survival during the perinatal period [4,5]. It was further shown that Tex19.1 is expressed by different pluripotent stem cells such as embryonic stem (ES), embryonic germ (EG) and embryonic carcinoma cells (ECC) and that the pattern of Tex19.1 expression almost parallels that of Oct4, a canonical marker of cell pluripotency. Altogether, these latter observations suggest that Tex19.1, as well as its human ortholog, could be a new factor involved in the maintenance of self-renewal or pluripotency of stem cells. Up to now, the expression patterns of Tex19.1 and Tex19.2 have been essentially analyzed by RT-PCR [2], thus limiting the amount of information on the cell types expressing these genes.With the aim of helping to evaluate Tex19.1 and Tex19.2 functions, we decided to precisely determine their expression patterns at the cellular level by in situ hybridization (ISH) of whole mounts and/or histological sections from E (embryonic day) 7.5 to adulthood. Our results indicate notably that Tex19.1 and Tex19.2 expression patterns mostly overlap in male mice and thus that functional redundancy between these two genes could attenuate the Tex19.1 KO phenotype. Materials and Methods Embryos and go...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

<i>Tex 19</i> Paralogs Exhibit a Gonad and Placenta-Specific Expression in the Mouse

et al. 2012

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“…Another intriguing aspect of Esx1 is that, like Rhox5, it has undergone rapid evolution in mammals (Wang & Zhang 2007). Evidence suggests that positive selection for rapid changes has primarily occurred in the C-terminal region, which is the region that regulates cyclin degradation and cell division.…”

Section: Esx1/esx1mentioning

confidence: 99%

The Rhox genes

MacLean¹,

Wilkinson²

2010

Reproduction

110

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Homeobox genes encode transcription factors that have crucial roles in embryogenesis. A recently discovered set of homeobox genes -the Rhox genes -are expressed during both embryogenesis and in adult reproductive tissues. The 33 known mouse Rhox genes are clustered together in a single region on the X chromosome, while likely descendents of the primodial Rhox cluster, Arx and Esx1, have moved to other positions on the X chromosome. Here, we summarize what is known about the regulation and function of Rhox cluster and Rhox-related genes during embryogenesis and gametogenesis. The founding member of the Rhox gene cluster -Rhox5 (previously known as Pem) -has been studied in the most depth and thus is the focus of this review. We also discuss the unusually rapid evolution of the Rhox gene cluster.

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“…X-linked genes are believed to evolve more rapidly than their autosomal orthologues due to their hemizygosity in males [17,18]. The mammalian sex chromosomes emerged from an ancestral pair of autosomes [19] and have received specific additions and deletions in each lineage.…”

Section: Introductionmentioning

confidence: 99%

Differential roles of TGIF family genes in mammalian reproduction

Shaw

et al. 2011

BMC Dev Biol

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BackgroundTG-interacting factors (TGIFs) belong to a family of TALE-homeodomain proteins including TGIF1, TGIF2 and TGIFLX/Y in human. Both TGIF1 and TGIF2 act as transcription factors repressing TGF-β signalling. Human TGIFLX and its orthologue, Tex1 in the mouse, are X-linked genes that are only expressed in the adult testis. TGIF2 arose from TGIF1 by duplication, whereas TGIFLX arose by retrotransposition to the X-chromosome. These genes have not been characterised in any non-eutherian mammals. We therefore studied the TGIF family in the tammar wallaby (a marsupial mammal) to investigate their roles in reproduction and how and when these genes may have evolved their functions and chromosomal locations.ResultsBoth TGIF1 and TGIF2 were present in the tammar genome on autosomes but TGIFLX was absent. Tammar TGIF1 shared a similar expression pattern during embryogenesis, sexual differentiation and in adult tissues to that of TGIF1 in eutherian mammals, suggesting it has been functionally conserved. Tammar TGIF2 was ubiquitously expressed throughout early development as in the human and mouse, but in the adult, it was expressed only in the gonads and spleen, more like the expression pattern of human TGIFLX and mouse Tex1. Tammar TGIF2 mRNA was specifically detected in round and elongated spermatids. There was no mRNA detected in mature spermatozoa. TGIF2 protein was specifically located in the cytoplasm of spermatids, and in the residual body and the mid-piece of the mature sperm tail. These data suggest that tammar TGIF2 may participate in spermiogenesis, like TGIFLX does in eutherians. TGIF2 was detected for the first time in the ovary with mRNA produced in the granulosa and theca cells, suggesting it may also play a role in folliculogenesis.ConclusionsThe restricted and very similar expression of tammar TGIF2 to X-linked paralogues in eutherians suggests that the evolution of TGIF1, TGIF2 and TGIFLX in eutherians was accompanied by a change from ubiquitous to tissue-specific expression. The distribution and localization of TGIF2 in tammar adult gonads suggest that there has been an ultra-conserved function for the TGIF family in fertility and that TGIF2 already functioned in spermatogenesis and potentially folliculogenesis long before its retrotransposition to the X-chromosome of eutherian mammals. These results also provide further evidence that the eutherian X-chromosome has actively recruited sex and reproductive-related genes during mammalian evolution.

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Rapid evolution of primate ESX1 , an X-linked placenta- and testis-expressed homeobox gene

Cited by 18 publications

References 46 publications

<i>Tex 19</i> Paralogs Exhibit a Gonad and Placenta-Specific Expression in the Mouse

<i>Tex 19</i> Paralogs Exhibit a Gonad and Placenta-Specific Expression in the Mouse

The Rhox genes

Differential roles of TGIF family genes in mammalian reproduction

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