mRNA 3′ uridylation and poly(A) tail length sculpt the mammalian maternal transcriptome

Morgan, Marcos; Much, Christian; Giacomo, Monica Di; Azzi, Chiara; Ivanova, Ivayla; Vitsios, Dimitrios; Pistolic, Jelena; Collier, Paul; Moreira, Pedro Ventura De Oliveira; Beneš, Vladimı́r; Enright, Anton J.; O’Carroll, Dónal

doi:10.1038/nature23318

Cited by 147 publications

(171 citation statements)

References 43 publications

(59 reference statements)

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“…We also observed that TUT4/7 knockdown partially blocks the increase of uridylation during Xenopus oocyte maturation ( Figures S4A and S4B). Thus, TUT4 and/or TUT7 are responsible for mRNA uridylation in fish and frog, as well as in mammals Morgan et al, 2017). Conversely, the splicing-blocking morpholinos had no detectable effect during these stages (data not shown), which is consistent with a previous report (Thornton et al, 2014).…”

Section: U Tails Emerge At the Onset Of The Mzt In Vertebratessupporting

confidence: 92%

Terminal Uridylyltransferases Execute Programmed Clearance of Maternal Transcriptome in Vertebrate Embryos

et al. 2018

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During the maternal-to-zygotic transition (MZT), maternal RNAs are actively degraded and replaced by newly synthesized zygotic transcripts in a highly coordinated manner. However, it remains largely unknown how maternal mRNA decay is triggered in early vertebrate embryos. Here, through genome-wide profiling of RNA abundance and 3' modification, we show that uridylation is induced at the onset of maternal mRNA clearance. The temporal control of uridylation is conserved in vertebrates. When the homologs of terminal uridylyltransferases TUT4 and TUT7 (TUT4/7) are depleted in zebrafish and Xenopus, maternal mRNA clearance is significantly delayed, leading to developmental defects during gastrulation. Short-tailed mRNAs are selectively uridylated by TUT4/7, with the highly uridylated transcripts degraded faster during the MZT than those with unmodified poly(A) tails. Our study demonstrates that uridylation plays a crucial role in timely mRNA degradation, thereby allowing the progression of early development.

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Section: U Tails Emerge At the Onset Of The Mzt In Vertebratessupporting

confidence: 92%

Terminal Uridylyltransferases Execute Programmed Clearance of Maternal Transcriptome in Vertebrate Embryos

et al. 2018

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“…However, although little Ccnb1 mRNA loading onto ribosomes was detected in GV-arrested oocytes, Ccnb2 mRNA loading was considerably higher. These indirect measures of translation were corroborated by mining data sets assessing the poly(A)-tail length of mRNAs in GV-arrested oocytes (Morgan et al, 2017). Ccnb2 mRNA had a significantly longer poly(A)-tail compared with Ccnb1 (Fig.…”

Section: Resultsmentioning

confidence: 66%

Cyclin B2 is required for progression through meiosis in mouse oocytes

et al. 2019

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Cyclins associate with cyclin-dependent serine/threonine kinase 1 (CDK1) to generate the M phase-promoting factor (MPF) activity essential for progression through mitosis and meiosis. Although cyclin B1 (CCNB1) is required for embryo development, previous studies concluded that CCNB2 is dispensable for cell cycle progression. Given previous findings of high Ccnb2 mRNA translation rates in prophasearrested oocytes, we re-evaluated the role of this cyclin during meiosis. Ccnb2 −/− oocytes underwent delayed germinal vesicle breakdown and showed defects during the metaphase-to-anaphase transition. This defective maturation was associated with compromised Ccnb1 and Moloney sarcoma oncogene (Mos) mRNA translation, delayed spindle assembly and increased errors in chromosome segregation. Given these defects, a significant percentage of oocytes failed to complete meiosis I because the spindle assembly checkpoint remained active and anaphase-promoting complex/cyclosome function was inhibited. In vivo, CCNB2 depletion caused ovulation of immature oocytes, premature ovarian failure, and compromised female fecundity. These findings demonstrate that CCNB2 is required to assemble sufficient pre-MPF for timely meiosis re-entry and progression. Although endogenous cyclins cannot compensate, overexpression of CCNB1/ 2 rescues the meiotic phenotypes, indicating similar molecular properties but divergent modes of regulation of these cyclins.

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“…Several recent studies demonstrated that uridylation is a key factor in germline development, early embryogenesis and differentiation [30,74]. The expression of TUT4/7 is elevated during embryogenesis, which indicates their importance in development.…”

Section: (E) the Role Of Mrna Uridylation In Developmentmentioning

confidence: 98%

“…The expression of TUT4/7 is elevated during embryogenesis, which indicates their importance in development. TUT4/7 play a major role in the establishment of the mammalian maternal transcriptome during oogenesis [30]. Each stage of oogenesis expresses a specific transcriptome.…”

Section: (E) the Role Of Mrna Uridylation In Developmentmentioning

confidence: 99%

“…Oocytes need to have the ability to selectively degrade mRNAs that are specific to the previous stage. This selective removal is regulated by deadenylation and uridylation [30]. The uridylation activities of TUT4 and TUT7 are required to mediate the selective removal of mRNA pools with short poly(A)-tails in several stages during oogenesis.…”

Section: (E) the Role Of Mrna Uridylation In Developmentmentioning

confidence: 99%

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The role of 3′ end uridylation in RNA metabolism and cellular physiology

Zigáčková¹,

Vaňáčová²

2018

Phil. Trans. R. Soc. B

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One contribution of 11 to a theme issue '5 0 and 3 0 modifications controlling RNA degradation'.Most eukaryotic RNAs are posttranscriptionally modified. The majority of modifications promote RNA maturation, others may regulate function and stability. The 3 0 terminal non-templated oligouridylation is a widespread modification affecting many cellular RNAs at some stage of their life cycle. It has diverse roles in RNA metabolism. The most prevalent is the regulation of stability and quality control. On the cellular and organismal level, it plays a critical role in a number of pathways, such as cell cycle regulation, cell death, development or viral infection. Defects in uridylation have been linked to several diseases. This review summarizes the current knowledge about the role of the 3 0 terminal oligo(U)-tailing in biology of various RNAs in eukaryotes and describes key factors involved in these pathways.This article is part of the theme issue '5 0 and 3 0 modifications controlling RNA degradation'.

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mRNA 3′ uridylation and poly(A) tail length sculpt the mammalian maternal transcriptome

Cited by 147 publications

References 43 publications

Terminal Uridylyltransferases Execute Programmed Clearance of Maternal Transcriptome in Vertebrate Embryos

Terminal Uridylyltransferases Execute Programmed Clearance of Maternal Transcriptome in Vertebrate Embryos

Cyclin B2 is required for progression through meiosis in mouse oocytes

The role of 3′ end uridylation in RNA metabolism and cellular physiology

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