Postovulatory ageing modifies sperm-induced Ca2+ oscillations in mouse oocytes through a conditions-dependent, multi-pathway mechanism

Szpila, Marcin; Walewska, Agnieszka; Sabat-Pośpiech, Dorota; Strączyńska, Patrycja; Ishikawa, Takao; Milewski, Robert; Szczepańska, Katarzyna; Ajduk, Anna

doi:10.1038/s41598-019-48281-3

Cited by 15 publications

(17 citation statements)

References 100 publications

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“…However, we did find that a significant proportion of aged mouse eggs failed to recover from the initial Sr 2+ induced Ca 2+ transients and they usually lysed before the end of the experiment. This is consistent with previous reports that mitochondrial ATP production fails to increase in response to Ca 2+ oscillations in aged mouse eggs ( Szpila et al , 2019 ). Even aged mouse eggs that underwent Sr 2+ induced Ca 2+ oscillations failed to activate and instead showed a fragmented appearance.…”

Section: Discussionsupporting

confidence: 94%

“…We have found that human eggs that have failed to fertilize after IVF or ICSI (and hence they were aged in vitro ) do not display Ca 2+ oscillations or activate in response to Sr 2+ medium that is otherwise effective at inducing immediate Ca 2+ oscillations in mouse eggs. Mammalian eggs that are aged in vitro show a number of biochemical changes that are not seen in freshly ovulated eggs ( Szpila et al , 2019 ). However, we found that in vitro aged mouse eggs reliably show Ca 2+ increases in response to Sr 2+ medium and so a lack of response in human eggs is unlikely to be caused by in vitro ageing itself.…”

Section: Discussionmentioning

confidence: 99%

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The role of ATP in the differential ability of Sr2+ to trigger Ca2+ oscillations in mouse and human eggs

Storey

Elgmati

Wang

et al. 2021

Molecular Human Reproduction

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At fertilization in mice and humans, the activation of the egg is caused by a series of repetitive Ca2+ oscillations which are initiated by phospholipase-C(zeta)ζ that generates inositol-1,4,5-trisphophate (InsP3). Ca2+ oscillations and egg activation can be triggered in mature mouse eggs by incubation in Sr2+ containing medium, but this does not appear to be effective in human eggs. Here, we have investigated the reason for this apparent difference using mouse eggs, and human eggs that failed to fertilize after IVF or ICSI. Mouse eggs incubated in Ca2+-free, Sr2+-containing medium immediately underwent Ca2+ oscillations but human eggs consistently failed to undergo Ca2+ oscillations in the same Sr2+ medium. We tested the InsP3-receptor (IP3R) sensitivity directly by photo-release of caged InsP3 and found that mouse eggs were about 10 times more sensitive to InsP3 than human eggs. There were no major differences in the Ca2+ store content between mouse and human eggs. However, we found that the ATP concentration was consistently higher in mouse compared to human eggs. When ATP levels were lowered in mouse eggs by incubation in pyruvate-free medium, Sr2+ failed to cause Ca2+ oscillations. When pyruvate was added back to these eggs, the ATP levels increased and Ca2+ oscillations were induced. This suggests that ATP modulates the ability of Sr2+ to stimulate IP3R-induced Ca2+ release in eggs. We suggest that human eggs may be unresponsive to Sr2+ medium because they have a lower level of cytosolic ATP.

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Section: Discussionsupporting

confidence: 94%

Section: Discussionmentioning

confidence: 99%

The role of ATP in the differential ability of Sr2+ to trigger Ca2+ oscillations in mouse and human eggs

Storey

Elgmati

Wang

et al. 2021

Molecular Human Reproduction

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“…The rate of decrease of Ca 2+ transients is also smaller in post-ovulatory aged eggs, probably because SERCA2 mRNA and protein levels are reduced [ 269 , 271 , 273 ]. Mitochondrial function is hampered in post-ovulatory aged eggs, which can affect Ca 2+ oscillations in at least two ways [ 272 , 273 ]. ATP production, necessary for SERCA and PMCA pump activity, is reduced and Ca 2+ uptake into the mitochondria is probably diminished.…”

Section: Post-ovulatory Ageingmentioning

confidence: 99%

“…Whether Ca 2+ influx is altered in post-ovulatory aged eggs of other mammalian species is currently unknown. The rate of decrease of Ca 2+ transients is also smaller in post-ovulatory aged eggs, probably because SERCA2 mRNA and protein levels are reduced [269,271,273]. Mitochondrial function is hampered in post-ovulatory aged eggs, which can affect Ca 2+ oscillations in at least two ways [272,273].…”

Section: Post-ovulatory Ageingmentioning

confidence: 99%

Modulators of calcium signalling at fertilization

et al. 2020

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Calcium (Ca 2+ ) signals initiate egg activation across the animal kingdom and in at least some plants. These signals are crucial for the success of development and, in the case of mammals, health of the offspring. The mechanisms associated with fertilization that trigger these signals and the molecules that regulate their characteristic patterns vary widely. With few exceptions, a major contributor to fertilization-induced elevation in cytoplasmic Ca 2+ is release from endoplasmic reticulum stores through the IP3 receptor. In some cases, Ca 2+ influx from the extracellular space and/or release from alternative intracellular stores contribute to the rise in cytoplasmic Ca 2+ . Following the Ca 2+ rise, the reuptake of Ca 2+ into intracellular stores or efflux of Ca 2+ out of the egg drive the return of cytoplasmic Ca 2+ back to baseline levels. The molecular mediators of these Ca 2+ fluxes in different organisms include Ca 2+ release channels, uptake channels, exchangers and pumps. The functions of these mediators are regulated by their particular activating mechanisms but also by alterations in their expression and spatial organization. We discuss here the molecular basis for modulation of Ca 2+ signalling at fertilization, highlighting differences across several animal phyla, and we mention key areas where questions remain.

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“…Postovulatory aging changes are mainly attributed to increased ROS production levels, apoptosis, and oocyte fragmentation [ 8 , 50 , 51 , 52 ]. Therefore, the supplementation of oocytes with exogenous antioxidants post-ovulation or after IVM (before fertilization) can be considered an effective approach to reduce the oocyte damage brought by ROS during aging [ 6 ].…”

Section: Discussionmentioning

confidence: 99%

Lycopene Reduces the In Vitro Aging Phenotypes of Mouse Oocytes by Improving Their Oxidative Status

Rakha

Elmetwally

Ali

et al. 2022

Veterinary Sciences

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Postovulatory aging is a major problem that limits the success of many assisted reproductive technologies (ARTs). Oxidative stress is a leading cause of oocyte aging. This study investigated the effects of lycopene supplementation of in vitro maturation (IVM) medium during the aging of mouse oocytes on the oocytes’ morphology and oxidative stress status. Mouse cumulus-oocyte complexes (COCs) were collected and cultured in the IVM medium either for 17 h, (freshly matured oocytes), or for 48 h, (in vitro-aged oocytes), with or without lycopene. The rate of fragmented and degenerated oocytes and the oocyte levels of hydrogen peroxide (H2O2), malondialdehyde (MDA), total antioxidant capacity (TAC), reduced glutathione (GSH), catalase (CAT), and superoxide dismutase (SOD) were estimated and compared. Oocytes aged with 200 nM lycopene revealed significantly less fragmentation and degeneration, lower H2O2 and MDA levels, and higher TAC, GSH and SOD levels than those aged without lycopene. CAT levels were unchanged by lycopene treatment. Taken together, our data showed beneficial effects of lycopene during in vitro aging of mouse oocytes by reducing the oxidative stress damages that lead to their apoptosis. The present study introduces lycopene as a natural supplement to reduce the postovulatory aging-dependent abnormalities of mammalian oocytes.

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Postovulatory ageing modifies sperm-induced Ca2+ oscillations in mouse oocytes through a conditions-dependent, multi-pathway mechanism

Cited by 15 publications

References 100 publications

The role of ATP in the differential ability of Sr2+ to trigger Ca2+ oscillations in mouse and human eggs

The role of ATP in the differential ability of Sr2+ to trigger Ca2+ oscillations in mouse and human eggs

Modulators of calcium signalling at fertilization

Lycopene Reduces the In Vitro Aging Phenotypes of Mouse Oocytes by Improving Their Oxidative Status

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