Sperm acrosome overgrowth and infertility in mice lacking chromosome 18 pachytene piRNA

Choi, Heejin; Wang, Zhengpin; Dean, Jurrien

doi:10.1371/journal.pgen.1009485

Cited by 52 publications

(53 citation statements)

References 72 publications

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“…[40][41][42][44][45][46] and reach a peak abundance in spermatocytes rivalling that of ribosomes 16 . Pachytene piRNAs tune the abundance of mRNAs required for spermiogenesis, the process by which round spermatids become sperm [47][48][49][50] . Pachytene piRNAs have been proposed to direct MIWI and MILI to cleave specific mRNAs, ensuring appropriate levels of their protein products 47,[50][51][52] .…”

Section: Mainmentioning

confidence: 99%

The conserved zinc-finger protein GTSF1 helps PIWI proteins achieve their full catalytic potential

Arif

Özata

Anderson

et al. 2021

Preprint

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Argonaute proteins use nucleic acid guides to find and bind specific DNA or RNA target sequences. Argonaute proteins can be found in all kingdoms of life, and play diverse biological functions including genome defense, gene regulation, and chromosome partitioning. Many Argonautes retain their ancestral endoribonuclease activity, cleaving the phosphodiester bond between target nucleotides t10 and t11. In animals, a specialized class of Argonautes, the PIWI proteins, use 21–35 nt PIWI-interacting RNAs (piRNAs) to direct transposon silencing, protect the germline genome, and regulate gene expression during gametogenesis1. The piRNA pathway is required for fertility in one or both sexes of nearly all animals. Both piRNA production and function require RNA cleavage catalyzed by PIWI proteins. Spermatogenesis in mice and other placental mammals requires three distinct, developmentally regulated PIWI proteins: MIWI (PIWIL1), MILI (PIWIL2), and MIWI2 (PIWIL4)2 4; the piRNA-guided endoribonuclease activities of MIWI and MILI are essential to produce functional sperm5,6. piRNA-directed silencing in mice, insects, and worms also requires Gametocyte-Specific Factor 1 (GTSF1), a PIWI-associated protein of unknown function7 12. Here, we report that GTSF1 potentiates the weak, intrinsic, piRNA-directed RNA cleavage activities of PIWI proteins, transforming them into efficient endoribonucleases. GTSF1 represents the first example of an auxiliary protein that potentiates the catalytic activity of an Argonaute protein.

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Section: Mainmentioning

confidence: 99%

The conserved zinc-finger protein GTSF1 helps PIWI proteins achieve their full catalytic potential

Arif

Özata

Anderson

et al. 2021

Preprint

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“…Notable exceptions are the mouse pachytene piRNAs, which are derived from so-called 'pachytene piRNA clusters' that are expressed during spermatogenesis at the pachytene stage of meiosis 1,2,6,7 . Pachytene piRNA clusters show no enrichment of transposon-complementary sequences but may regulate some protein-coding genes [8][9][10][11] .…”

Section: Introductionmentioning

confidence: 99%

An evolutionarily conserved stop codon enrichment at the 5’ ends of mammalian piRNAs

Bornelöv

Czech

Hannon

2021

Preprint

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SUMMARYPIWI-interacting RNAs (piRNAs) are small RNAs required to recognize and silence transposable elements. The 5’ ends of mature piRNAs are defined through cleavage of long precursor transcripts, primarily by Zucchini (Zuc). Zuc-dependent cleavage typically occurs immediately upstream of a uridine. However, Zuc lacks sequence preference in vitro, pointing towards additional unknown specificity factors. We examined murine piRNAs and revealed a strong and specific enrichment of three sequences (UAA, UAG, UGA)— corresponding to stop codons—at piRNA 5’ ends. This pattern was robust across 101 analysed samples. Stop codon sequences were also enriched immediately after piRNA processing intermediates, reflecting their Zuc-dependent tail-to-head arrangement. Further analysis suggested that Zuc has an in vivo cleavage preference at stop codon sequences. Finally, this enrichment was conserved across mammals and possibly further. Our work provides new insights into Zuc-dependent cleavage and may point to a previously unrecognized connection between piRNA biogenesis and the translational machinery.

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“…Defective capacitation and failure to bind and penetrate the zona pellucida have been reported in pachytene piRNA mutant sperm (Wu et al, 2020). Choi et al found sperm acrosome growth and infertility in mice lacking chromosome 18 pachytene piRNA (Choi et al, 2021). In light of the significant regulatory role of ERK1/2 in boar sperm capacitation (Awda and Buhr, 2010), piR-121380 might have an indirect role in regulating acrosomal reaction through ERK2 phosphorylation in mature boar sperm.…”

Section: Discussionmentioning

confidence: 99%

piR-121380 Is Involved in Cryo-Capacitation and Regulates Post-Thawed Boar Sperm Quality Through Phosphorylation of ERK2 via Targeting PTPN7

Wang

Yuan

Ali

et al. 2022

Front. Cell Dev. Biol.

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Cryopreservation induces capacitation-like (cryo-capacitation) changes, similar to natural capacitation, and affects the fertility potential of post-thawed sperm. The molecular mechanism of sperm cryo-capacitation during cryopreservation remains unknown. PIWI-interacting RNAs (piRNAs) have been reported to be involved in cryo-capacitation of post-thawed sperm and regulation of sperm motility, capacitation, and chemotaxis. In this study, protein tyrosine phosphatase nonreceptor type 7 (PTPN7) was positively targeted by piR-121380 after a dual luciferase assay. The mRNA expression of PTPN7 and piR-121380 was significantly decreased (p < 0.01); however, PTPN7 protein was significantly increased (p < 0.01) in post-thawed boar sperm. Furthermore, E1RK1/2 phosphorylation was reduced during cryopreservation. Six hours after transfection with piR-121380 mimic and inhibitor, the phosphorylation of ERK2 was significantly increased and decreased (p < 0.01), respectively. Furthermore, the highest and lowest total sperm motility, forward motility, and capacitation rate were observed after piR-121380 mimic and inhibitor treatments, respectively. The concentration of intracellular calcium ([Ca2+]i) showed no significant difference after transfection with either piR-121380 mimic or inhibitor at 1, 3, and 6 h. In conclusion, we demonstrated that piR-121380 modulates ERK2 phosphorylation by targeting PTPN7, which induces sperm cryo-capacitation, and eventually affects the motility and fertility potential of post-thawed sperm.

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Sperm acrosome overgrowth and infertility in mice lacking chromosome 18 pachytene piRNA

Cited by 52 publications

References 72 publications

The conserved zinc-finger protein GTSF1 helps PIWI proteins achieve their full catalytic potential

The conserved zinc-finger protein GTSF1 helps PIWI proteins achieve their full catalytic potential

An evolutionarily conserved stop codon enrichment at the 5’ ends of mammalian piRNAs

piR-121380 Is Involved in Cryo-Capacitation and Regulates Post-Thawed Boar Sperm Quality Through Phosphorylation of ERK2 via Targeting PTPN7

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