Single-cell CAS-seq reveals a class of short PIWI-interacting RNAs in human oocytes

Yang, Qiyuan; Li, Ronghong; Lyu, Qifeng; Li, Hou; Liu, Zhen; Sun, Qiang; Liu, Miao; Shi, Huijuan; Xu, Beiying; Yin, Minzhi; Zhou, Yan; Huang, Ying; Liu, Mofang; Li, Yiping; Wu, Ligang

doi:10.1038/s41467-019-11312-8

Cited by 75 publications

(162 citation statements)

References 69 publications

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“…In accordance with previous findings 10,11 , in the present study we observed a reduced oocyte developmental competence in the NBS, as indicated by decreased cleavage and blastocyst rates after in vitro fertilization (IVF), and this was associated to changes in miRNA and transcriptomic profiles both in OOs and FCs. Being miRNAs only one of the small RNA components, as expected those identified in buffalo represent only a fraction of the total small non-coding RNA present in both OOs and FCs 27,28 . The overall miRNA expression pattern was different between OOs obtained in the two seasons.…”

Section: Discussionsupporting

confidence: 55%

Seasonal effects on miRNA and transcriptomic profile of oocytes and follicular cells in buffalo (Bubalus bubalis)

Capra

Lazzari

Russo

et al. 2020

Sci Rep

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Season clearly influences oocyte competence in buffalo (Bubalus bubalis); however, changes in the oocyte molecular status in relation to season are poorly understood. This study characterizes the microRNA (miRNA) and transcriptomic profiles of oocytes (OOs) and corresponding follicular cells (FCs) from buffalo ovaries collected in the breeding (BS) and non-breeding (NBS) seasons. In the BS, cleavage and blastocyst rates are significantly higher compared to NBS. Thirteen miRNAs and two mRNAs showed differential expression (DE) in FCs between BS and NBS. DE-miRNAs target gene analysis uncovered pathways associated with transforming growth factor β (TGFβ) and circadian clock photoperiod. Oocytes cluster in function of season for their miRNA content, showing 13 DE-miRNAs between BS and NBS. Between the two seasons, 22 differentially expressed genes were also observed. Gene Ontology (GO) analysis of miRNA target genes and differentially expressed genes (DEGs) in OOs highlights pathways related to triglyceride and sterol biosynthesis and storage. Co-expression analysis of miRNAs and mRNAs revealed a positive correlation between miR-296-3p and genes related to metabolism and hormone regulation. In conclusion, season significantly affects female fertility in buffalo and impacts on oocyte transcriptomic of genes related to folliculogenesis and acquisition of oocyte competence. Water buffalo (Bubalus bubalis) is an important livestock resource for both developing and developed countries. The major factor affecting buffalo farming profitability is reproductive seasonality, resulting in cycles of calving and milk production. Buffalo is a short-day breeder, with increased fertility in response to decreasing day length 1,2. This photoperiod-dependent seasonality pattern is more pronounced as distance from the equator, together with variations in the light/dark ratio, increases. In Italy, in order to satisfy market demand, out of breeding mating strategy (OBMS), consisting in interrupting sexual promiscuity or the use of artificial insemination (AI) during the breeding season (BS), is commonly utilized 2. The OBMS improves the distribution of calving throughout the year, but it reduces fertility 3. Longer post-partum anoestrus periods as well as higher incidence of embryonic mortality are observed in months with increasing daylight length and particularly in midwinter , which coincides with the transition to seasonal anoestrus at Italian latitudes 1,4. The embryonic mortality is due to inadequate luteal growth and function, resulting in reduced progesterone secretion 5. This has a negative impact on embryo growth, associated with alterations in transcriptomic and proteomic profiles of the embryos and chorioamnios/caruncles 6,7 , which ultimately impair embryo attachment to the uterine endometrium.

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Section: Discussionsupporting

confidence: 55%

Seasonal effects on miRNA and transcriptomic profile of oocytes and follicular cells in buffalo (Bubalus bubalis)

Capra

Lazzari

Russo

et al. 2020

Sci Rep

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“…Recently, it has been reported that, in human oocytes, PIWIL3 associates with a group of relatively short~20 nt piRNAs. We have not detected these short piRNAs in bovine oocytes, and it remains to be established whether piRNA size may be species-dependent [44]. piRNAs from oocytes and TDRKH-IPs map uniquely to intergenic regions of the genome, forming large piRNA clusters.…”

Section: Discussionmentioning

confidence: 82%

PIWIL3 Forms a Complex with TDRKH in Mammalian Oocytes

Tan

Tol

Rosenkranz

et al. 2020

Cells

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P-element induced wimpy testis (PIWIs) are crucial guardians of genome integrity, particularly in germ cells. While mammalian PIWIs have been primarily studied in mouse and rat, a homologue for the human PIWIL3 gene is absent in the Muridae family, and hence the unique function of PIWIL3 in germ cells cannot be effectively modeled by mouse knockouts. Herein, we investigated the expression, distribution, and interaction of PIWIL3 in bovine oocytes. We localized PIWIL3 to mitochondria, and demonstrated that PIWIL3 expression is stringently controlled both spatially and temporally before and after fertilization. Moreover, we identified PIWIL3 in a mitochondrial-recruited three-membered complex with Tudor and KH domain-containing protein (TDRKH) and poly(A)-specific ribonuclease-like domain containing 1 (PNLDC1), and demonstrated by mutagenesis that PIWIL3 N-terminal arginines are required for complex assembly. Finally, we sequenced the piRNAs bound to PIWIL3-TDRKH-PNLDC1 and report here that about 50% of these piRNAs map to transposable elements, recapitulating the important role of PIWIL3 in maintaining genome integrity in mammalian oocytes.

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“…For meiosis and retrotransposon silencing in oocytes, a subclass of siRNAs (endogeneous-siRNAs) known to regulate transcripts [ 103 , 104 ] is necessary [ 105 , 106 ]. However, an oocyte-specific piRNA family (os-piRNAs) may also be involved in the silencing of TEs, as revealed in human oocytes [ 107 ]. The repression of transposable elements is indeed important for oogenesis, seeing as a higher proportion of oocytes from mice expressing elevated levels of retrotransposons undergo apoptosis during meiotic prophase I [ 108 ].…”

Section: Epigenetic Reprogramming During Oogenesismentioning

confidence: 99%

What impact does oocyte vitrification have on epigenetics and gene expression?

Barberet¹,

Barry²,

Choux³

et al. 2020

Clin Epigenet

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Children conceived by assisted reproductive technologies (ART) have a moderate risk for a number of adverse events and conditions. The question whether this additional risk is associated with specific procedures used in ART or whether it is related to the intrinsic biological factors associated with infertility remains unresolved. One of the main hypotheses is that laboratory procedures could have an effect on the epigenome of gametes and embryos. This suspicion is linked to the fact that ART procedures occur precisely during the period when there are major changes in the organization of the epigenome. Oocyte freezing protocols are generally considered safe; however, some evidence suggests that vitrification may be associated with modifications of the epigenetic marks. In this manuscript, after describing the main changes that occur during epigenetic reprogramming, we will provide current information regarding the impact of oocyte vitrification on epigenetic regulation and the consequences on gene expression, both in animals and humans. Overall, the literature suggests that epigenetic and transcriptomic profiles are sensitive to the stress induced by oocyte vitrification, and it also underlines the need to improve our knowledge in this field.

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Single-cell CAS-seq reveals a class of short PIWI-interacting RNAs in human oocytes

Cited by 75 publications

References 69 publications

Seasonal effects on miRNA and transcriptomic profile of oocytes and follicular cells in buffalo (Bubalus bubalis)

Seasonal effects on miRNA and transcriptomic profile of oocytes and follicular cells in buffalo (Bubalus bubalis)

PIWIL3 Forms a Complex with TDRKH in Mammalian Oocytes

What impact does oocyte vitrification have on epigenetics and gene expression?

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