Epigenome Modification and Ubiquitin‐Dependent Proteolysis During Pronuclear Development of the Mammalian Zygote: Animal Models to Study Pronuclear Development

Nevoral, Jan; Šutovský, Peter

doi:10.1002/9781118881286.ch17

Cited by 3 publications

(2 citation statements)

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“…Various PTMs of canonical histones affect residual histones in sperm and have crucial roles with respect to several specific properties of the spermatozoon: the replacement of most core histones via protamination, transcriptional inactivity, and a haploid genome designed for fusion with oocytes. Therefore, the sperm histone code is an important determinant of sperm fertilization ability and the destiny of paternal chromatin in embryos (Nevoral and Sutovsky 2017). Moreover, the histone code is sensitive to the environment, which influences sperm quality via epigenetic mechanisms (Delbes et al 2010;Jenkins et al 2017;Gunes et al 2018).…”

Section: Resultsmentioning

confidence: 99%

H3K4me2 accompanies chromatin immaturity in human spermatozoa: an epigenetic marker for sperm quality assessment

Štiavnická

García-Álvarez

et al. 2019

Systems Biology in Reproductive Medicine

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Chromatin remodeling, including histone post-translational modifications, during spermatogenesis can affect sperm quality and fertility, and epigenetic marks may therefore be useful for clinical evaluations of sperm. Together with histone hyperacetylation, the dimethylation of histone H3 on lysine K4 (H3K4me2) is also required during protamination. Accordingly, we evaluated the utilization of this epigenetic mark for the identification of sperm with decrease quality and immature chromatin. In this study, 99 semen samples, including 22 normozoospermic (N), 63 asthenozoospermic (A), and 14 oligoasthenozoospermic (OA) samples, were comprehensively analyzed with respect to H3K4me2 levels, DNA damage (DNA fragmentation index, DFI), and sperm immaturity (high DNA stainability, %HDS), as determined by a sperm chromatin structure assay using flow cytometry. We detected a significant relationship between H3K4me2 and %HDS (r = 0.47; p < 0.001). Furthermore, we observed negative correlations between H3K4me2 and sperm concentration, motility, and mitochondrial activity (p < 0.05). The increase in immaturity as semen quality decreased (N > A > OA) indicates the importance of chromatin immaturity and histone code deviations in sperm evaluations. Using various approaches, our study elucidated H3K4me2 as a molecular marker of sperm quality with potential use in reproductive medicine.

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Section: Resultsmentioning

confidence: 99%

H3K4me2 accompanies chromatin immaturity in human spermatozoa: an epigenetic marker for sperm quality assessment

Štiavnická

García-Álvarez

et al. 2019

Systems Biology in Reproductive Medicine

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“…Proteasomal inhibitors alter male pronuclear chromatin (Huo et al, 2004;Rawe et al, 2008) possibly interfering with protamine removal and/or oocyte–somatic histone swap. The ensemble of epigenetic histone marks, the zygotic histone code, which is reset at the onset of embryo development, is also influenced by UPS (Nevoral and Sutovsky, 2017), possibly through UPS regulation of sirtuin 1 (SIRT1), a histone deacetylase (Adamkova et al, 2017). The involvement of UPS extends beyond the zygote.…”

Section: Pronuclear Developmentmentioning

confidence: 99%

Review: Sperm–oocyte interactions and their implications for bull fertility, with emphasis on the ubiquitin–proteasome system

Šutovský

2018

Animal

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Fertilization is an intricate cascade of events that irreversibly alter the participating male and female gamete and ultimately lead to the union of paternal and maternal genomes in the zygote. Fertilization starts with sperm capacitation within the oviductal sperm reservoir, followed by gamete recognition, sperm-zona pellucida interactions and sperm-oolemma adhesion and fusion, followed by sperm incorporation, oocyte activation, pronuclear development and embryo cleavage. At fertilization, bull spermatozoon loses its acrosome and plasma membrane components and contributes chromosomes, centriole, perinuclear theca proteins and regulatory RNAs to the zygote. While also incorporated in oocyte cytoplasm, structures of the sperm tail, including mitochondrial sheath, axoneme, fibrous sheath and outer dense fibers are degraded and recycled. The ability of some of these sperm contributed components to give rise to functional zygotic structures and properly induce embryonic development may vary between bulls, bearing on their reproductive performance, and on the fitness, health, fertility and production traits of their offspring. Proper functioning, recycling and remodeling of gamete structures at fertilization is aided by the ubiquitin-proteasome system (UPS), the universal substrate-specific protein recycling pathway present in bovine and other mammalian oocytes and spermatozoa. This review is focused on the aspects of UPS relevant to bovine fertilization and bull fertility.

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Epigenetic and non-epigenetic mode of SIRT1 action during oocyte meiosis progression

Nevoral

Landsmann

Štiavnická

et al. 2019

J Animal Sci Biotechnol

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Background SIRT1 histone deacetylase acts on many epigenetic and non-epigenetic targets. It is thought that SIRT1 is involved in oocyte maturation; therefore, the importance of the ooplasmic SIRT1 pool for the further fate of mature oocytes has been strongly suggested. We hypothesised that SIRT1 plays the role of a signalling molecule in mature oocytes through selected epigenetic and non-epigenetic regulation. Results We observed SIRT1 re-localisation in mature oocytes and its association with spindle microtubules. In mature oocytes, SIRT1 distribution shows a spindle-like pattern, and spindle-specific SIRT1 action decreases α-tubulin acetylation. Based on the observation of the histone code in immature and mature oocytes, we suggest that SIRT1 is mostly predestined for an epigenetic mode of action in the germinal vesicles (GVs) of immature oocytes. Accordingly, BML-278-driven trimethylation of lysine K9 in histone H3 in mature oocytes is considered to be a result of GV epigenetic transformation. Conclusions Taken together, our observations point out the dual spatiotemporal SIRT1 action in oocytes, which can be readily switched from the epigenetic to non-epigenetic mode of action depending on the progress of meiosis. Electronic supplementary material The online version of this article (10.1186/s40104-019-0372-3) contains supplementary material, which is available to authorized users.

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Epigenome Modification and Ubiquitin‐Dependent Proteolysis During Pronuclear Development of the Mammalian Zygote: Animal Models to Study Pronuclear Development

Cited by 3 publications

References 296 publications

H3K4me2 accompanies chromatin immaturity in human spermatozoa: an epigenetic marker for sperm quality assessment

H3K4me2 accompanies chromatin immaturity in human spermatozoa: an epigenetic marker for sperm quality assessment

Review: Sperm–oocyte interactions and their implications for bull fertility, with emphasis on the ubiquitin–proteasome system

Epigenetic and non-epigenetic mode of SIRT1 action during oocyte meiosis progression

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