Genome wide analysis of 3′ UTR sequence elements and proteins regulating mRNA stability during maternal-to-zygotic transition in zebrafish

Vejnar, Charles E.; Messih, Mario Abdel; Takacs, Carter M.; Yartseva, Valeria; Oikonomou, Panos; Christiano, Romain; Stoeckius, Marlon; Lau, Stephanie; Lee, Miler T.; Beaudoin, Jean-Denis; Musaev, Damir; Darwich-Codore, Hiba; Walther, Tobias C.; Tavazoie, Saeed; Cifuentes, Daniel; Giráldez, Antonio J.

doi:10.1101/gr.245159.118

Cited by 60 publications

(67 citation statements)

References 89 publications

(131 reference statements)

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“…RNA-seq and data processing of high-throughput sequencing. The total RNA of unfertilized eggs and embryos at different developmental stages of wild type and mutant zebrafish were isolated with TRIzol reagent, and mRNA was purified from total RNA as described previously 41 . Purified mRNAs and RIP-RNAs were fragmented and RNA library was constructed using NEBNext® Ultra II Directional RNA Library Prep Kit for Illumina (NEB, E7760) according to the manufacturer's instructions.…”

Section: Methodsmentioning

confidence: 99%

Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish

et al. 2020

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Early embryogenesis relies on maternally inherited mRNAs. Although the mechanism of maternal mRNA degradation during maternal-to-zygotic transition (MZT) has been extensively studied in vertebrates, how the embryos maintain maternal mRNA stability remains unclear. Here, we identify Igf2bp3 as an important regulator of maternal mRNA stability in zebrafish. Depletion of maternal igf2bp3 destabilizes maternal mRNAs prior to MZT and leads to severe developmental defects, including abnormal cytoskeleton organization and cell division. However, the process of oogenesis and the expression levels of maternal mRNAs in unfertilized eggs are normal in maternal igf2bp3 mutants. Gene ontology analysis revealed that these functions are largely mediated by Igf2bp3-bound mRNAs. Indeed, Igf2bp3 depletion destabilizes while its overexpression enhances its targeting maternal mRNAs. Interestingly, igf2bp3 overexpression in wild-type embryos also causes a developmental delay. Altogether, these findings highlight an important function of Igf2bp3 in controlling early zebrafish embryogenesis by binding and regulating the stability of maternal mRNAs.

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Section: Methodsmentioning

confidence: 99%

Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish

et al. 2020

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“…The 3 UTRs of zebrafish mRNAs are structurally dynamic and changes in their structure can regulate the stability of mRNAs during MZT by modulating miRNA activity [39]. In addition, the 3 UTRs of zebrafish mRNAs are enriched in cis-acting regulatory elements that control mRNA decay during MZT and have been characterized in detail using a high-throughput RNA-element selection assay (RESA), which enables to identify sequences regulating RNA stability with near nucleotide resolution [75]. An in vivo study of heat-regulated RNA structuromes in rice showed that mRNA unfolding is correlated with RNA half-life and supports the importance of both UTRs for mRNA stability in plants [52].…”

Section: Rna Structure In Relation To Rna Stability and Degradationmentioning

confidence: 99%

On the Way to Understanding the Interplay between the RNA Structure and Functions in Cells: A Genome-Wide Perspective

Andrzejewska

Zawadzka

Pachulska-Wieczorek

2020

IJMS

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RNAs adopt specific structures in order to perform their biological activities. The structure of RNA is an important layer of gene expression regulation, and can impact a plethora of cellular processes, starting with transcription, RNA processing, and translation, and ending with RNA turnover. The development of high-throughput technologies has enabled a deeper insight into the sophisticated interplay between the structure of the cellular transcriptome and the living cells environment. In this review, we present the current view on the RNA structure in vivo resulting from the most recent transcriptome-wide studies in different organisms, including mammalians, yeast, plants, and bacteria. We focus on the relationship between the mRNA structure and translation, mRNA stability and degradation, protein binding, and RNA posttranscriptional modifications.

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“…Similarly, an SNP site in the 3′ UTR of the human BMP2 gene is associated with the formation of human subcutaneous fat [22]. It is widely believed that 3′ UTR regulatory regions are involved in post-transcriptional regulation and play an important regulatory role in mRNA stability, gene transcription efficiency, and expression localization [23][24][25]. It remains to be seen whether the three sites we found in the 3′ UTR of the sheep BMP2 gene contribute to post-transcriptional regulation.…”

Section: Discussionmentioning

confidence: 79%

Association Between BMP2 Functional Polymorphisms and Sheep Tail Type

Liu

Han

et al. 2020

Animals

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Bone morphogenetic protein 2 (BMP2) is strongly selected in both fat-tailed and thin-tailed sheep and may be a candidate gene for sheep tail type selection. However, the mechanism of action of BMP2 in sheep tail fat deposition remains unclear. This study investigated genetic variation and haplotype combinations of the BMP2 gene in sheep with different tail types, aiming to reveal the molecular mechanism of BMP2 in sheep tail fat deposition. We detected a total of three single nucleotide polymorphisms (SNPs) (g.48401619 T > A, g.48401272 C > A, and g.48401136 C > T) among 533 sheep. The alleles and genotype frequencies of these SNPs were in Hardy–Weinberg equilibrium and showed significant correlations with tail length. Linkage disequilibrium existed between the g.48401272 C > A and g.48401136 C > T sites, where CACT was the predominant genotype. At the cellular level, the expression levels of peroxisome proliferator-activated receptor gamma (PPARγ) and lipoprotein lipase (LPL) were upregulated after BMP2 overexpression; there were significantly higher levels of PPARγ than controls at 0 d and 1 d, and of LPL than controls at 1 d and 7 d. These results indicate that the BMP2 gene may participate in sheep tail fat deposition and could be used for molecular-marker-assisted selection of sheep tail type.

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Genome wide analysis of 3′ UTR sequence elements and proteins regulating mRNA stability during maternal-to-zygotic transition in zebrafish

Cited by 60 publications

References 89 publications

Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish

Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish

On the Way to Understanding the Interplay between the RNA Structure and Functions in Cells: A Genome-Wide Perspective

Association Between BMP2 Functional Polymorphisms and Sheep Tail Type

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