Small RNA class transition from siRNA/piRNA to miRNA during pre-implantation mouse development

Ohnishi, Yusuke; Totoki, Yasushi; Toyoda, Atsushi; Watanabe, Toshiaki; Yamamoto, Yasuhiro; Tokunaga, Katsushi; Sakaki, Yoshiyuki; Sasaki, Hidetada; Hohjoh, Hirohiko

doi:10.1093/nar/gkq229

Cited by 130 publications

(123 citation statements)

References 49 publications

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“…Therefore, it is apparent that different types of small RNAs vary during spermatogenesis in a wellcoordinated manner. A similar change in major small RNA classes also occurs during pre-implantation development (Ohnishi et al 2010).…”

Section: Discussionmentioning

confidence: 60%

piRNA profiling during specific stages of mouse spermatogenesis

Gan

Lin²,

Zhang³

et al. 2011

RNA

111

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PIWI-interacting RNAs (piRNAs) are a class of small RNAs abundantly expressed in animal gonads. piRNAs that map to retrotransposons are generated by a ''ping-pong'' amplification loop to suppress the activity of retrotransposons. However, the biogenesis and function of other categories of piRNAs have yet to be investigated. In this study, we first profiled the expression of small RNAs in type A spermatogonia, pachytene spermatocytes, and round spermatids by deep sequencing. We then focused on the computational analysis of the potential piRNAs generated in the present study as well as other published sets. piRNAs mapping to retrotransposons, mRNAs, and intergenic regions had different length distributions and were differentially regulated in spermatogenesis. piRNA-generating mRNAs (PRMRs), whose expression positively correlated with their piRNA products, constituted one-third of the protein-coding genes and were evolutionarily conserved and enriched with splicing isoforms and antisense transcripts. PRMRs with piRNAs preferentially mapped to CDSs and 39 UTRs partitioned into three clusters differentially expressed during spermatogenesis and enriched with unique sets of functional annotation terms related to housekeeping activities as well as spermatogenesis-specific processes. Intergenic piRNAs were divided into 2992 clusters probably representing novel transcriptional units that have not been reported. The transcripts of a large number of genes involved in spermatogenesis are the precursors of piRNAs, and these genes are intricately regulated by alternative splicing and antisense transcripts. piRNAs, whose regulatory role in gene expression awaits to be identified, are clearly products of a novel regulatory process that needs to be defined.

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Section: Discussionmentioning

confidence: 60%

piRNA profiling during specific stages of mouse spermatogenesis

Gan

Lin²,

Zhang³

et al. 2011

RNA

111

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“…Several studies have suggested that endogenous siRNAs against TEs play an important role in TE silencing [33][34][35][36]. Despite that this endogenous siRNA silencing system is functional in zygotes [37], certain classes of TEs somehow find a way to escape this silencing system for their activation in zygotes.…”

Section: Tet3-mediated 5mc Oxidation Is Dispensable For Zygotic Gene mentioning

confidence: 99%

Transcriptional activation of transposable elements in mouse zygotes is independent of Tet3-mediated 5-methylcytosine oxidation

2012

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The methylation state of the paternal genome is rapidly reprogrammed shortly after fertilization. Recent studies have revealed that loss of 5-methylcytosine (5mC) in zygotes correlates with appearance of 5-hydroxymethylcytosine (5hmC), 5-formylcytosine (5fC), and 5-carboxylcytosine (5caC). This process is mediated by Tet3 and the 5mC oxidation products generated in zygotes are gradually lost during preimplantation development through a replicationdependent dilution process. Despite these findings, the biological significance of Tet3-mediated oxidation of 5mC to 5hmC/5fC/5caC in zygotes is unknown. DNA methylation plays an important role in silencing gene expression including the repression of transposable elements (TEs). Given that the activation of TEs during preimplantation development correlates with loss of DNA methylation, it is believed that paternal DNA demethylation may have an important role in TE activation. Here we examined this hypothesis and found that Tet3-mediated 5mC oxidation does not have a significant contribution to TE activation. We show that the expression of LINE-1 (long interspersed nucleotide element 1) and ERVL (endogenous retroviruses class III) are activated from both paternal and maternal genomes in zygotes. Inhibition of 5mC oxidation by siRNA-mediated depletion of Tet3 affected neither TE activation, nor global transcription in zygotes. Thus, our study provides the first evidence demonstrating that activation of both TEs and global transcription in zygotes are independent of Tet3-mediated 5mC oxidation.

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“…The dynamic changes in the expression of miRNAs in preimplantation embryos (6)(7)(8) and the increased synthesis of miRNAs after the two-cell stage in mouse embryos (7,9) suggest that miRNAs have a functional role in the preimplantation period. This evidence is supported by the observations that mouse oocytes without the miRNA-processing enzyme Dicer have a minimal amount of miRNA, that their resulting zygotes cannot pass through the first cleavage division (7), and that Dicer-null embryos carrying maternal dicer die at embryonic day 7.5 (E7.5) (10).…”

mentioning

confidence: 99%

Sperm-borne microRNA-34c is required for the first cleavage division in mouse

Liu

Pang

Chiu

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

382

335

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In mammals, the sperm deliver mRNA of unknown function into the oocytes during fertilization. The role of sperm microRNAs (miRNAs) in preimplantation development is unknown. miRNA profiling identified six miRNAs expressed in the sperm and the zygotes but not in the oocytes or preimplantation embryos. Sperm contained both the precursor and the mature form of one of these miRNAs, miR-34c. The absence of an increased level of miR-34c in zygotes derived from α-amanitin-treated oocytes and in parthenogenetic oocytes supported a sperm origin of zygotic miR-34c. Injection of miR-34c inhibitor into zygotes inhibited DNA synthesis and significantly suppressed first cleavage division. A 3′ UTR luciferase assay and Western blotting demonstrated that miR-34c regulates B-cell leukemia/lymphoma 2 (Bcl-2) expression in the zygotes. Coinjection of anti-Bcl-2 antibody in zygotes partially reversed but injection of Bcl-2 protein mimicked the effect of miR-34c inhibition. Oocyte activation is essential for the miR-34c action in zygotes, as demonstrated by a decrease in 3′ UTR luciferase reporter activity and Bcl-2 expression after injection of precursor miR-34c into parthenogenetic oocytes. Our findings provide evidence that sperm-borne miR-34c is important for the first cell division via modulation of Bcl-2 expression.

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Small RNA class transition from siRNA/piRNA to miRNA during pre-implantation mouse development

Cited by 130 publications

References 49 publications

piRNA profiling during specific stages of mouse spermatogenesis

piRNA profiling during specific stages of mouse spermatogenesis

Transcriptional activation of transposable elements in mouse zygotes is independent of Tet3-mediated 5-methylcytosine oxidation

Sperm-borne microRNA-34c is required for the first cleavage division in mouse

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