Formation of mos RNA granules in the zebrafish oocyte that differ from cyclin B1 RNA granules in distribution, density and regulation

Horie, Mayu; Kotani, Tomoya

doi:10.1016/j.ejcb.2016.10.001

Cited by 15 publications

(21 citation statements)

References 54 publications

(78 reference statements)

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“…For example, surprisingly, Vasa and Mos Drosophila genes were not predicted by BioMart to have an ortholog in vertebrates, although they do possess one ( Gebauer and Richter 1997 ; Elis et al. 2008 ; Horie and Kotani 2016 ; Song et al. 2016 ).…”

Section: Discussionmentioning

confidence: 99%

Genes Involved in Drosophila melanogaster Ovarian Function Are Highly Conserved Throughout Evolution

Elis

Desmarchais

Cardona

et al. 2018

Genome Biology and Evolution

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This work presents a systematic approach to study the conservation of genes between fruit flies and mammals. We have listed 971 Drosophila genes involved in female reproduction at the ovarian level and systematically looked for orthologs in the Ciona, zebrafish, coelacanth, lizard, chicken, and mouse. Depending on the species, the percentage of these Drosophila genes with at least one ortholog varies between 69% and 78%. In comparison, only 42% of all the Drosophila genes have an ortholog in the mouse genome (P < 0.0001), suggesting a dramatically higher evolutionary conservation of ovarian genes. The 177 Drosophila genes that have no ortholog in mice and other vertebrates correspond to genes that are involved in mechanisms of oogenesis that are specific to the fruit fly or the insects. Among 759 genes with at least one ortholog in the zebrafish, 73 have an expression enriched in the ovary in this species (RNA-seq data). Among 760 genes that have at least one ortholog in the mouse; 76 and 11 orthologs are reported to be preferentially and exclusively expressed in the mouse ovary, respectively (based on the UniGene expressed sequence tag database). Several of them are already known to play a key role in murine oogenesis and/or to be enriched in the mouse/zebrafish oocyte, whereas others have remained unreported. We have investigated, by RNA-seq and real-time quantitative PCR, the exclusive ovarian expression of 10 genes in fish and mammals. Overall, we have found several novel candidates potentially involved in mammalian oogenesis by an evolutionary approach and using the fruit fly as an animal model.

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Section: Discussionmentioning

confidence: 99%

Genes Involved in Drosophila melanogaster Ovarian Function Are Highly Conserved Throughout Evolution

Elis

Desmarchais

Cardona

et al. 2018

Genome Biology and Evolution

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“…mos mRNA encodes a kinase activating the mitogen-activated protein kinase (MAPK) pathway [ 41 ], and cyclin B1 mRNA encodes a regulatory subunit of maturation/M-phase-promoting factor (MPF) [ 42 ]. These mRNAs are accumulated in the animal polar cytoplasm of zebrafish oocytes as a translationally repressed form [ 28 , 29 , 31 , 32 , 35 , 43 ].…”

Section: Resultsmentioning

confidence: 99%

“…Large numbers of cyclin B1 RNA granules were localized at the animal polar cytoplasm in stage III (Fig. 4d ) and fully grown, stage IV oocytes [ 31 , 32 , 50 ]. The localization and granular structure of dazl mRNA were maintained in stage III and IV oocytes, but the granules were broadly distributed in the vegetal polar cytoplasm (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…A previous study showed that zebrafish cyclin B1 mRNA is initially distributed throughout the cytoplasm of oocytes (stages I and II) and becomes localized at the animal polar cytoplasm after stage III, when DIG-labeled RNA probes were recognized by an AP-coupled anti-DIG antibody, followed by detection of signals by precipitation of AP substrates [ 28 ]. Fluorescence in situ hybridization with the TSA system has revealed the localization of cyclin B1 mRNA at the animal polar cytoplasm as RNA granules [ 31 , 32 , 50 ], and this study revealed changes in cyclin B1 mRNA distribution and localization during oocyte development; i.e., cyclin B1 mRNA was initially distributed throughout the cytoplasm of oocytes in stage I and subsequently moved to the animal pole in stage II (Fig. 4a - c ), and a granular structure was first found in stage Ib oocytes and persisted in later stages (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Our results demonstrated similarity and difference of the mRNA regulations in zebrafish and mouse species. Granular structures of mRNAs have been suggested to function in regulating the timing of translational activation of the mRNAs [ 31 , 32 ]. mRNAs encoding Cyclin B1 and Dazl appeared to form granular structures in both zebrafish and mouse oocytes, suggesting translational regulation of these mRNAs.…”

Section: Discussionmentioning

confidence: 99%

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High-Sensitivity and High-Resolution In Situ Hybridization of Coding and Long Non-coding RNAs in Vertebrate Ovaries and Testes

et al. 2018

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BackgroundSubcellular localization of coding and non-coding RNAs has emerged as major regulatory mechanisms of gene expression in various cell types and many organisms. However, techniques that enable detection of the subcellular distribution of these RNAs with high sensitivity and high resolution remain limited, particularly in vertebrate adult tissues and organs. In this study, we examined the expression and localization of mRNAs encoding Pou5f1/Oct4, Mos, Cyclin B1 and Deleted in Azoospermia-like (Dazl) in zebrafish and mouse ovaries by combining tyramide signal amplification (TSA)-based in situ hybridization with paraffin sections which can preserve cell morphology of tissues and organs at subcellular levels. In addition, the distribution of a long non-coding RNA (lncRNA), lncRNA-HSVIII, in mouse testes was examined by the same method.ResultsThe mRNAs encoding Mos, Cyclin B1 and Dazl were found to assemble into distinct granules that were distributed in different subcellular regions of zebrafish and mouse oocytes, suggesting conserved and specific regulations of these mRNAs. The lncRNA-HSVIII was first detected in the nucleus of spermatocytes at prophase I of the meiotic cell cycle and was then found in the cytoplasm of round spermatids, revealing expression patterns of lncRNA during germ cell development. Collectively, the in situ hybridization method demonstrated in this study achieved the detection and comparison of precise distribution patterns of coding and non-coding RNAs at subcellular levels in single cells of adult tissues and organs.ConclusionsThis high-sensitivity and high-resolution in situ hybridization is applicable to many vertebrate species and to various tissues and organs and will be useful for studies on the subcellular regulation of gene expression at the level of RNA localization.Electronic supplementary materialThe online version of this article (10.1186/s12575-018-0071-z) contains supplementary material, which is available to authorized users.

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Regulation of Translationally Repressed mRNAs in Zebrafish and Mouse Oocytes

Kotani

Maehata

Takei

2017

Results and Problems in Cell Differentiation

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From the beginning of oogenesis, oocytes accumulate tens of thousands of mRNAs for promoting oocyte growth and development. A large number of these mRNAs are translationally repressed and localized within the oocyte cytoplasm. Translational activation of these dormant mRNAs at specific sites and timings plays central roles in driving progression of the meiotic cell cycle, axis formation, mitotic cleavages, transcriptional initiation, and morphogenesis. Regulation of the localization and temporal translation of these mRNAs has been shown to rely on cis-acting elements in the mRNAs and trans-acting factors recognizing and binding to the elements. Recently, using model vertebrate zebrafish, localization itself and formation of physiological structures such as RNA granules have been shown to coordinate the accurate timings of translational activation of dormant mRNAs. This subcellular regulation of mRNAs is also utilized in other animals including mouse. In this chapter, we review fundamental roles of temporal regulation of mRNA translation in oogenesis and early development and then focus on the mechanisms of mRNA regulation in the oocyte cytoplasm by which the activation of dormant mRNAs at specific timings is achieved.

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Formation of mos RNA granules in the zebrafish oocyte that differ from cyclin B1 RNA granules in distribution, density and regulation

Cited by 15 publications

References 54 publications

Genes Involved in Drosophila melanogaster Ovarian Function Are Highly Conserved Throughout Evolution

Genes Involved in Drosophila melanogaster Ovarian Function Are Highly Conserved Throughout Evolution

High-Sensitivity and High-Resolution In Situ Hybridization of Coding and Long Non-coding RNAs in Vertebrate Ovaries and Testes

Regulation of Translationally Repressed mRNAs in Zebrafish and Mouse Oocytes

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