Preovulatory Aging In Vivo and In Vitro Affects Maturation Rates, Abundance of Selected Proteins, Histone Methylation Pattern and Spindle Integrity in Murine Oocytes

Demond, Hannah; Trapphoff, Tom; Dankert, Deborah; Heiligentag, Martyna; Grümmer, Ruth; Horsthemke, Bernhard; Eichenlaub-Ritter, Ursula

doi:10.1371/journal.pone.0162722

Cited by 25 publications

(15 citation statements)

References 51 publications

(77 reference statements)

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“…H3K4me3 is enriched at active promoters and correlates with transcription at developmentally regulated genes . H3K9me3 is associated with the silencing of transcription and is involved in heterochromatin formation and chromosome stability during meiosis . Our results indicate that the reproductive toxicity caused by PQ exposure might be caused by abnormal epigenetic patterns.…”

Section: Discussionmentioning

confidence: 74%

Melatonin protects against paraquat‐induced damage during in vitro maturation of bovine oocytes

Pang

Jiang

Wang

et al. 2018

Journal of Pineal Research

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Paraquat (PQ), a broad-spectrum agricultural pesticide, causes cellular toxicity by increasing oxidative stress levels in various biological systems, including the reproductive system. PQ exposure causes embryotoxicity and reduces the developmental abilities of embryos. However, there is little information regarding the toxic effects of PQ on oocyte maturation. In this study, we studied the toxic effects of PQ exposure and the effects of melatonin on PQ-induced damage in bovine oocytes. PQ exposure disrupted nuclear and cytoplasmic maturation, which was manifested as decreased cumulus cell expansion, reduced first polar body extrusion, and abnormal distribution patterns of cortical granules and mitochondria. In addition, PQ treatment severely disrupted the ability of the resulted in vitro-produced embryos to develop to the blastocyst stage. Moreover, PQ exposure significantly increased the intracellular reactive oxygen species (ROS) level and early apoptotic rate, and decreased the glutathione (GSH) level, antioxidative CAT and GPx4 mRNA, and apoptotic-related Bcl-2/Bax mRNA ratio. These results indicated that PQ causes reproductive toxicity in bovine oocytes. Melatonin application resulted in significant protection against the toxic effects of PQ in PQ-exposed oocytes. The mechanisms underlying the role of melatonin included the inhibition of PQ-induced p38 mitogen-activated protein kinase (MAPK) activation, and restoration of abnormal trimethyl-histone H3 lysine 4 (H3K4me3) and trimethyl-histone H3 lysine 9 (H3K9me3) levels. These results reveal that melatonin serves as a powerful agent against experimental PQ-induced toxicity during bovine oocyte maturation and could form a basis for further studies to develop therapeutic strategies against PQ poisoning. K E Y W O R D Sbovine, melatonin, oocyte maturation, oxidative damage, paraquat 2 of 15 | PANG et Al.

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Section: Discussionmentioning

confidence: 74%

Melatonin protects against paraquat‐induced damage during in vitro maturation of bovine oocytes

Pang

Jiang

Wang

et al. 2018

Journal of Pineal Research

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“…Thus, in Ccnb2 −/− oocytes, the switchlike entry into and exit from meiosis I was lost, resulting in nonsynchronous, delayed, and sometimes failed MI/anaphase I transitions. The prolonged maturation time of the Ccnb2 −/− oocytes could lead to a phenotype similar to that which is described for oocyte aging, which results in compromised developmental competence (Demond et al, 2016). In addition, the increased aneuploidy rate detected was associated with compromised ability to sustain embryo development.…”

Section: Discussionmentioning

confidence: 71%

Cyclin B2 is required for progression through meiosis in mouse oocytes

et al. 2019

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Cyclins associate with cyclin-dependent serine/threonine kinase 1 (CDK1) to generate the M phase-promoting factor (MPF) activity essential for progression through mitosis and meiosis. Although cyclin B1 (CCNB1) is required for embryo development, previous studies concluded that CCNB2 is dispensable for cell cycle progression. Given previous findings of high Ccnb2 mRNA translation rates in prophasearrested oocytes, we re-evaluated the role of this cyclin during meiosis. Ccnb2 −/− oocytes underwent delayed germinal vesicle breakdown and showed defects during the metaphase-to-anaphase transition. This defective maturation was associated with compromised Ccnb1 and Moloney sarcoma oncogene (Mos) mRNA translation, delayed spindle assembly and increased errors in chromosome segregation. Given these defects, a significant percentage of oocytes failed to complete meiosis I because the spindle assembly checkpoint remained active and anaphase-promoting complex/cyclosome function was inhibited. In vivo, CCNB2 depletion caused ovulation of immature oocytes, premature ovarian failure, and compromised female fecundity. These findings demonstrate that CCNB2 is required to assemble sufficient pre-MPF for timely meiosis re-entry and progression. Although endogenous cyclins cannot compensate, overexpression of CCNB1/ 2 rescues the meiotic phenotypes, indicating similar molecular properties but divergent modes of regulation of these cyclins.

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“…Therefore, we tested post-translational changes of histone H3 in GV oocytes after SIRT1 activation via BML-278. Indeed, GV histone H3 is modified at lysine K9 in a SIRT1-dependent manner, favouring heterochromatin features for gene silencing, chromatin stability and DNA protection [61, 62]. In addition to H3K9me3, H3K4me2 shows a decrease after 0.125 μmol/L BML-278 treatment of GV oocytes.…”

Section: Discussionmentioning

confidence: 99%

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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Preovulatory Aging In Vivo and In Vitro Affects Maturation Rates, Abundance of Selected Proteins, Histone Methylation Pattern and Spindle Integrity in Murine Oocytes

Cited by 25 publications

References 51 publications

Melatonin protects against paraquat‐induced damage during in vitro maturation of bovine oocytes

Melatonin protects against paraquat‐induced damage during in vitro maturation of bovine oocytes

Cyclin B2 is required for progression through meiosis in mouse oocytes

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

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