The mammalian-specific Tex19.1 gene plays an essential role in spermatogenesis and placenta-supported development

Tarabay, Yara; Kieffer, Emmanuelle; Teletin, Marius; Célébi, Catherine; Montfoort, Aafke P.A. van; Zamudio, Natasha; Achour, Mayada; Ramy, Rosy El; Gazdag, Emese; Tropel, Philippe; Mark, Manuel; Bourc’his, Déborah; Viville, Stéphane

doi:10.1093/humrep/det129

“…1E). Conversely, after 2 h of maturation, the mRNA coding for Tex19.1, a suppressor of transposon activation (Ollinger et al, 2008;Reichmann et al, 2013;Tarabay et al, 2013), became progressively associated with ribosomes up to the MII stage (Fig. 1E).…”

Section: Resultsmentioning

confidence: 99%

“…Both ribosome loading and protein expression show that TEX19.1 progressively accumulates during meiotic progression, with a maximum reached in MII. Tex19.1-null mice have been generated, but the inactivation of this gene in females either produces no phenotype (Tarabay et al, 2013) or decreased fecundity (Ollinger et al, 2008), suggesting that oocyte maturation is not prevented or only marginally affected when Tex19.1 is ablated. Conversely, TEX19.1 plays an essential role during male spermatogenesis as Tex19.1-null males are infertile owing to spermatogenic arrest at meiosis between pachytene and metaphase of MI.…”

Section: Discussionmentioning

confidence: 99%

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DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation

Martins

¹

,

Liu

²

,

Oke

³

et al. 2016

Journal of Cell Science

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Meiotic progression requires exquisitely coordinated translation of maternal messenger (m)RNA that has accumulated during oocyte growth. A major regulator of this program is the cytoplasmic polyadenylation element binding protein 1 (CPEB1). However, the temporal pattern of translation at different meiotic stages indicates the function of additional RNA binding proteins (RBPs). Here, we report that deleted in azoospermia-like (DAZL) cooperates with CPEB1 to regulate maternal mRNA translation. Using a strategy that monitors ribosome loading onto endogenous mRNAs and a prototypic translation target, we show that ribosome loading is induced in a DAZL-and CPEB1-dependent manner, as the oocyte reenters meiosis. Depletion of the two RBPs from oocytes and mutagenesis of the 3′ untranslated regions (UTRs) demonstrate that both RBPs interact with the Tex19.1 3′ UTR and cooperate in translation activation of this mRNA. We observed a synergism between DAZL and cytoplasmic polyadenylation elements (CPEs) in the translation pattern of maternal mRNAs when using a genome-wide analysis. Mechanistically, the number of DAZL proteins loaded onto the mRNA and the characteristics of the CPE might define the degree of cooperation between the two RBPs in activating translation and meiotic progression.

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“…5C). A literature search revealed that homozygous knockouts for Spint1 (Tanaka et al, 2005), Plac1 (Jackman et al, 2012), Tex19.1 (Tarabay et al, 2013), Kcnk1 (Millar et al, 2006), Tfap2a (Schorle et al, 1996;Zhang et al, 1996) and Prom2 (Tang et al, 2010) had been phenotypically characterized previously, with three, namely Spint1, Plac1 and Tex19.1, displaying a placenta phenotype. Whereas Plac1 −/− and Tex19.1 −/− mice exhibit milder placenta defects that manifest in late pregnancy (Jackman et al, 2012;Tarabay et al, 2013), Spint1 −/− mice have been reported to display an early placenta defect with lethality at E10.5 (Tanaka et al, 2005;Fan et al, 2007;Szabo et al, 2007), similar to the phenotype we found in Grhl2 −/− mice.…”

Section: Identification Of Placental Grhl2 Target Genes By Integratedmentioning

confidence: 99%

A Grhl2-dependent gene network controls trophoblast branching morphogenesis

Walentin

¹

,

Hinze

²

,

Werth

³

et al. 2015

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Healthy placental development is essential for reproductive success; failure of the feto-maternal interface results in pre-eclampsia and intrauterine growth retardation. We found that grainyhead-like 2 (GRHL2), a CP2-type transcription factor, is highly expressed in chorionic trophoblast cells, including basal chorionic trophoblast (BCT) cells located at the chorioallantoic interface in murine placentas. Placentas from Grhl2-deficient mouse embryos displayed defects in BCT cell polarity and basement membrane integrity at the chorioallantoic interface, as well as a severe disruption of labyrinth branching morphogenesis. Selective Grhl2 inactivation only in epiblast-derived cells rescued all placental defects but phenocopied intraembryonic defects observed in global Grhl2 deficiency, implying the importance of Grhl2 activity in trophectoderm-derived cells. ChIP-seq identified 5282 GRHL2 binding sites in placental tissue. By integrating these data with placental gene expression profiles, we identified direct and indirect Grhl2 targets and found a marked enrichment of GRHL2 binding adjacent to genes downregulated in Grhl2(-/-) placentas, which encoded known regulators of placental development and epithelial morphogenesis. These genes included that encoding the serine protease inhibitor Kunitz type 1 (Spint1), which regulates BCT cell integrity and labyrinth formation. In human placenta, we found that human orthologs of murine GRHL2 and its targets displayed co-regulation and were expressed in trophoblast cells in a similar domain as in mouse placenta. Our data indicate that a conserved Grhl2-coordinated gene network controls trophoblast branching morphogenesis, thereby facilitating development of the site of feto-maternal exchange. This might have implications for syndromes related to placental dysfunction

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“…Conversely, TEX19.1 plays an essential role during male spermatogenesis as Tex19.1-null males are infertile owing to spermatogenic arrest at meiosis between pachytene and metaphase of MI. It has also been found that Line 1 and intracisternal A-particle (IAP) transposon levels are increased in the Tex19.1-null mice (Ollinger et al, 2008, Tarabay et al, 2013. Spermatogenesis is very sensitive to the activation of endogenous retroviruses, as documented by several knockout models, whereas transposon activation has less of an effect on mammalian oogenesis.…”

Section: Discussionmentioning

confidence: 99%

DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation

Martins¹,

Liu²,

Oke³

et al. 2016

View full text Add to dashboard Cite

Meiotic progression requires exquisitely coordinated translation of maternal messenger (m)RNA that has accumulated during oocyte growth. A major regulator of this program is the cytoplasmic polyadenylation element binding protein 1 (CPEB1). However, the temporal pattern of translation at different meiotic stages indicates the function of additional RNA binding proteins (RBPs). Here, we report that deleted in azoospermia-like (DAZL) cooperates with CPEB1 to regulate maternal mRNA translation. Using a strategy that monitors ribosome loading onto endogenous mRNAs and a prototypic translation target, we show that ribosome loading is induced in a DAZL-and CPEB1-dependent manner, as the oocyte reenters meiosis. Depletion of the two RBPs from oocytes and mutagenesis of the 3′ untranslated regions (UTRs) demonstrate that both RBPs interact with the Tex19.1 3′ UTR and cooperate in translation activation of this mRNA. We observed a synergism between DAZL and cytoplasmic polyadenylation elements (CPEs) in the translation pattern of maternal mRNAs when using a genome-wide analysis. Mechanistically, the number of DAZL proteins loaded onto the mRNA and the characteristics of the CPE might define the degree of cooperation between the two RBPs in activating translation and meiotic progression.

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The mammalian-specific Tex19.1 gene plays an essential role in spermatogenesis and placenta-supported development

Cited by 21 publications

References 31 publications

DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation

DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation

A Grhl2-dependent gene network controls trophoblast branching morphogenesis

DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation

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