The RNase III Enzyme DROSHA Is Essential for MicroRNA Production and Spermatogenesis

Wu, Qiuxia; Song, Rui; Ortogero, Nicole; Zheng, Huili; Evanoff, Ryan; Small, Christopher; Griswold, Michael D.; Namekawa, Satoshi H.; Royo, Hélène; Turner, James M. A.; Yan, Wei

doi:10.1074/jbc.m112.362053

Cited by 185 publications

(186 citation statements)

References 89 publications

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“…To further explore potential roles of MIWI2 in the meiotic and haploid phases of spermatogenesis, we crossed Miwi2 loxp mice with three germ cell-specific Cre lines to inactivate Miwi2 in the male germ line at different developmental time points. The Ddx4-Cre line has been used to delete a floxed allele in PGCs/prospermatogonia with an onset of CRE expression at E15.5, 39 whereas Stra8-Cre mice display CRE expression in prospermatogonia at P3 although the full penetrance of CRE activity is not reached until pachytene spermatocytes at P12 10,40,41 ( Figure 1d). The Prm-Cre line has Cre expression starting in round spermatids, but the protein expression may be delayed due to posttranscriptional regulation 42 ( Figure 1d).…”

Section: Resultsmentioning

confidence: 99%

“…[4][5][6][7] piRNAs represent a distinct small noncoding RNA (sncRNA) species with an average length of 25-31nt, and piRNA biogenesis is independent of the RNase III enzymes DROSHA and DICER, which are essential for the production of miRNAs and siRNAs. [8][9][10] piRNAs can generally be divided into two groups based on their genomic origin: repeat-associated and non-repeat-associated. 4,7,11 Repeatassociated piRNAs are mostly derived from retrotransposon loci and appear to be synthesized through two successive steps: primary piRNA processing and secondary piRNA cleavage achieved by the so-called 'ping-pong' amplification cycle.…”

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confidence: 99%

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Conditional inactivation of Miwi2 reveals that MIWI2 is only essential for prospermatogonial development in mice

Bao

Schuster

et al. 2014

Cell Death Differ

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The PIWI-piRNA pathway serves as a critical defense mechanism through which the genome of the male germline is protected from invasion by transposable elements (TEs). MIWI2/PIWIL4, a member of the murine PIWI subclade of the Argonaute family, has been shown to be expressed in primordial germ cells (PGCs) and prospermatogonia in fetal and prepubertal testes. Global inactivation of Miwi2 leads to male sterility due to an early meiotic arrest, which correlates with retrotransposon desuppression. However, it remains unclear whether MIWI2 functions beyond the PGC stage and whether MIWI2 has a role beyond TE suppression during male germ line development. Through conditional inactivation of Miwi2, we demonstrate herein that MIWI2 function is restricted to a narrow time window during male PGC reprograming and that Miwi2 is dispensable for postnatal male germline development and testicular function in mice. Moreover, persistent activation of LINE1 and IAP retrotransposons caused by Miwi2 inactivation is compatible with mitotic cell cycle progression of spermatogonia during the first wave of spermatogenesis, but can cause zygotene to pachytene arrest in early meiosis due to multiple defects including enhanced DNA double-strand breaks, aberrant histone modifications and altered mRNA transcriptome. Our data not only validate those from global Miwi2 KO studies, but also suggest that MIWI2 and MIWI2-associated piRNAs have functions beyond TE suppression. Cell Death and Differentiation (2014) 21, 783-796; doi:10.1038/cdd.2014; published online 24 January 2014The Argonaute family of proteins contains two subclasses, argonaute (AGO) and p-element induced wimpy testis (PIWI), both of which are highly conserved from plants to animals. 1The AGO subfamily members (for example, AGO1-4) are expressed ubiquitously in a wide range of tissues/cell types and function through associations with miRNAs and siRNAs.

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Conditional inactivation of Miwi2 reveals that MIWI2 is only essential for prospermatogonial development in mice

Bao

Schuster

et al. 2014

Cell Death Differ

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“…Two biological replicates of FACS-purified Sertoli cells from control, Dicer cKO, and Drosha cKO testes (n ϭ 2) were sequenced using the Ion Torrent Personal Genome Machine (PGM) (Invitrogen) as described (17,18). Briefly, sncRNAs were isolated using the mirVana miRNA isolation kit (Invitrogen), and cDNA libraries were generated using the Ion Total RNA-Seq kit v2 (Invitrogen).…”

Section: Methodsmentioning

confidence: 99%

“…sncRNA deep sequencing (sncRNA-Seq) (17,38). Sequencing reads aligned to known piRNAs were used for differential pilRNA expression analyses.…”

Section: Identification Of Pilrnas In Somaticmentioning

confidence: 99%

A Novel Class of Somatic Small RNAs Similar to Germ Cell Pachytene PIWI-interacting Small RNAs

Ortogero

Schuster

Oliver

et al. 2014

Journal of Biological Chemistry

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Background: Germ cells exclusively express PIWI-interacting small RNAs for transposon and gene regulation. Results: Somatic cells express similar RNAs that do not require known small RNA proteins and that partially complement mRNAs. Conclusion: These somatic small RNAs represent a novel small RNA population, which potentially regulates mRNA translation. Significance: Defining novel small RNAs is essential for elucidating the mechanisms that control gene expression.

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“…Some evidences point to a great variety of biological processes in which miRNAs are involved, including among others embryo development, cell proliferation or apoptosis (Wang and Xu 2015). Dicer1 or Drosha knockout mouse models, in which miRNA processing is compromised, resulted also in impaired spermatogenesis and fertility after birth due to faulty germ cell proliferation (Maatouk et al 2008;Wu et al 2012).The essential and multiple functions played by miRNAs during spermatogenesis have been largely evaluated (Jodar et al 2013;Kotaja 2014;Luo et al 2015). In addition, an implication of paternal miRNAs in embryo development has been hypothesized because the potential capacity for repressing translation of zygotic transcripts, or regulating transcription by interaction with specific promoters (Jodar et al 2013).…”

Section: Controlling Gene Expression With Mirnamentioning

confidence: 99%

Paternal contribution to development: Sperm genetic damage and repair in fish

et al. 2017

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In this review we provide an overview of the components of the spermatozoa playing an important role in reproductive success beyond fertilization, showing the relationship between the integrity of the diverse elements and the development of a healthy offspring. The present knowledge about fish sperm chromatin organization, epigenetic modifications of DNA and histones and sperm-borne RNAs, essential in controlling embryo development, is summarized, pointing out the possibility of using specific genes or transcripts as biomarkers of sperm quality. Data about commercial species are reported when available and more detailed information about zebrafish sperm is presented.Considering the implications that the integrity of sperm genome and epigenome has on the preservation of a proper genotype and phenotype in the progeny, the methods applied for the study of chromatin damage and for the study of transcriptome are described. Moreover we discuss some injuring agents affecting paternal information, from the presence of contaminants in the aquatic environment, to the reproductive *Manuscript Click here to download Manuscript: Herrez et al revised aquaculture.docx Click here to view linked References practices applied in fish farming. The consequences of fertilizing with damaged spermatozoa, as well as the zygotic ability to repair damage are also reviewed.

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The RNase III Enzyme DROSHA Is Essential for MicroRNA Production and Spermatogenesis

Cited by 185 publications

References 89 publications

Conditional inactivation of Miwi2 reveals that MIWI2 is only essential for prospermatogonial development in mice

Conditional inactivation of Miwi2 reveals that MIWI2 is only essential for prospermatogonial development in mice

A Novel Class of Somatic Small RNAs Similar to Germ Cell Pachytene PIWI-interacting Small RNAs

Paternal contribution to development: Sperm genetic damage and repair in fish

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