Caffeine alleviates the deterioration of Ca<sup>2+</sup> release mechanisms and fragmentation of in vitro‐aged mouse eggs

Zhang, Nan; Wakai, Toshifumi; Fissore, Rafael A.

doi:10.1002/mrd.21366

Cited by 42 publications

(47 citation statements)

References 99 publications

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“…However, post-ovulatory aged oocytes experience a decline in IP 3 receptor/channel functionality (Zhang et al 2011), as well as suppressed ER Ca 2C -ATPase activity, and exhibit a consequential depletion of Ca 2C stores that reside within the ER (Takahashi et al 2000). As a result of this impaired Ca 2C homoeostasis, aged oocytes exhibit abnormal Ca 2C oscillations at fertilization that have significantly higher frequency and lower amplitude than those of fertilized fresh oocytes (Igarashi et al 1997, Takahashi et al 2003.…”

Section: Decreased Fertilization Ratementioning

confidence: 99%

“…The functionality of the mitochondria does, however, become compromised with extended periods of time following ovulation, a factor that is thought to heavily influence oocyte quality. Diminished mitochondrial integrity in the in vitro aged oocyte has been demonstrated by a loss of mitochondrial membrane potential (Zhang et al 2011) and a decline in levels of ATP production (Chi et al 1988).…”

Section: Mitochondrial Dysfunctionmentioning

confidence: 99%

“…Additionally, recent studies have established that the addition of caffeine or MG132 (a proteasome inhibitor) to oocyte culture can increase fertilization rates by ICSI and decrease fragmentation in embryos (Ono et al 2011). Further modes of action for caffeine in relation to postovulatory ageing include a delay in the deterioration of Ca 2C release mechanisms, although the underlying pharmacology is not yet clear (Zhang et al 2011).…”

Section: Maintenance Of Mpf Levelsmentioning

confidence: 99%

“…Post-ovulatory aged oocytes exhibit numerous aberrations in their cell biology including partial cortical granule exocytosis (Szollosi 1971, Dodson et al 1989, Ducibella et al 1990, Xu et al 1997, zona hardening (Longo 1981, Dodson et al 1989, Xu et al 1997, a decrease in critical cell cycle factors including maturation-promoting factor (MPF) and MAPK (Kikuchi et al 2002), mitochondrial dysfunction (Chi et al 1988, Takahashi et al 2003, Tatone et al 2011, Zhang et al 2011, Lord et al 2013, spindle abnormalities (Wakayama et al 2004), losses of chromosomal integrity (Spielmann et al 1985, Mailhes et al 1998, Wakayama et al 2004) and epigenetic changes (Liang et al 2008; Table 1). Not surprisingly, the process of post-ovulatory ageing culminates in apoptosis (Fujino et al 1996) as a result of decreases in expression of the anti-apoptotic protein BCL2 (Gordo et al 2002, Ma et al 2005) and the activation of caspases (Takai et al 2007, Lord et al 2013.…”

Section: Introductionmentioning

confidence: 99%

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Oxidative stress and ageing of the post-ovulatory oocyte

2013

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With extended periods of time following ovulation, the metaphase II stage oocyte experiences deterioration in quality referred to as post-ovulatory oocyte ageing. Post-ovulatory ageing occurs both in vivo and in vitro and has been associated with reduced fertilization rates, poor embryo quality, post-implantation errors and abnormalities in the offspring. Although the physiological consequences of post-ovulatory oocyte ageing have largely been established, the molecular mechanisms controlling this process are not well defined. This review analyses the relationships between biochemical changes exhibited by the ageing oocyte and the symptoms associated with the ageing phenotype. We also discuss molecular events that are potentially involved in orchestrating post-ovulatory ageing with a particular focus on the role of oxidative stress. We propose that oxidative stress may act as the initiator for a cascade of events that create the aged oocyte phenotype. Specifically, oxidative stress has the capacity to cause a decline in levels of critical cell cycle factors such as maturation-promoting factor, impair calcium homoeostasis, induce mitochondrial dysfunction and directly damage multiple intracellular components of the oocyte such as lipids, proteins and DNA. Finally, this review addresses current strategies for delaying post-ovulatory oocyte ageing with a particular focus on the potential use of compounds such as caffeine or selected antioxidants in the development of more refined media for the preservation of oocyte integrity during IVF procedures.

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Section: Decreased Fertilization Ratementioning

confidence: 99%

Section: Mitochondrial Dysfunctionmentioning

confidence: 99%

Section: Maintenance Of Mpf Levelsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Oxidative stress and ageing of the post-ovulatory oocyte

2013

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“…In addition, Marutino et al observed that oocyte energy/oxidative status was affected by within/ between-subject, in vivo versus IVM and age-related variations [8]. Moreover, it was confirmed that oocytes aged in vitro exhibited decreased mitochondrial membrane potential and Ca 2+ levels in the endoplasmic reticulum, and that addition of caffeine ameliorates most of these aging-associated changes [9].Thus far, mitochondrial function in mammalian oocytes has been assessed by analyzing mitochondrial localization ATP content and mitochondrial membrane potential [7,10,11]. However, these techniques can be disruptive and are indirect methods for assessing physiological mitochondrial function.…”

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confidence: 93%

Oxidative Phosphorylation-linked Respiration in Individual Bovine Oocytes

et al. 2012

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Abstract. Mitochondrial bioenergetics in mammalian oocytes has not been sufficiently characterized. In this study, the function of oxidative phosphorylation (OXPHOS), a major pathway in mitochondria, was investigated in individual bovine oocytes by monitoring oxygen consumption using modified scanning electrochemical microscopy (SECM). At the germinal vesicle (GV) stage, 65% of basal respiration was used for mitochondrial respiration, which was inhibited by complex IV inhibitor. Around 63% of mitochondrial respiration was coupled to ATP synthesis, as determined by sensitivity to an ATP synthase inhibitor, and the remaining 37% was attributed to proton leak. In contrast, 50% and 43% of mitochondrial respiration were used for ATP synthesis in in vivo-and in vitro-derived metaphase II (MII)-stage oocytes, respectively. ATP-linked respiration, in both in vivo-and in vitro-derived MII-stage oocytes, was significantly lower than in GV-stage oocytes, suggesting that OXPHOS in bovine oocytes is more active at the GV stage compared with the MII stage. Interestingly, basal respiration in in vitro-derived MII oocytes was significantly higher than for in vivo-derived oocytes, reflecting an increase in proton leak. Next, we assessed respiration in MII oocytes cultured for 8 h. The aged oocytes had a significantly reduced maximum respiratory capacity, which was stimulated by a mitochondrial uncoupler, and reduced ATP-linked respiration compared with non-aged oocytes. However, the aging-related phenomenon could be prevented by caffeine treatment. We conclude that OXPHOS in bovine oocytes varies in the transition from GV to MII stage, in vitro maturation and the aging process. This approach will be particularly useful for analyzing mitochondrial bioenergetics in individual mammalian oocytes. Key words: Bovine, Mitochondrial function, Oocyte, Oxidative phosphorylation, Oxygen consumption (J. Reprod. Dev. 58: [636][637][638][639][640][641] 2012) M itochondria play fundamental roles in the cell, and mitochondrial dysfunction has been linked with several pathologies, including infertility and developmental failure. Although they share general characteristics, mitochondria can have distinct features based on inner membrane invaginations and matrix structures. Depending on their cell type and functional status, mitochondria present an extensive range of morphologies, are functionally heterogeneous [1], and vary in number [2]. Oxidative phosphorylation (OXPHOS), the process that couples substrate oxidation to ATP synthesis, is the major and best-known metabolic function of mitochondria. During OXPHOS, electrons are transferred from nutrients to reducing equivalents (e.g., NADH), then to electron carriers, and finally to oxygen. Such electron transfer is mediated by oxido-reductive reactions of the tricarboxylic acid cycle in the mitochondrial matrix and by electron transport in the inner mitochondrial membrane. The energy harvested during these oxido-reductive reactions is stored in a proton gradient across the inner mitochondrial ...

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Role of Caspase-3 Cleaved IP₃R1 on Ca²⁺Homeostasis and Developmental Competence of Mouse Oocytes and Eggs

Zhang

Fissore

2014

J. Cell. Physiol

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Apoptosis in most cell types is accompanied by altered Ca2+ homeostasis. During apoptosis, caspase-3 mediated cleavage of the type 1 inositol 1,4,5-trisphosphate receptor (IP3R1) generates a 95-kDa C-terminal fragment (C-IP3R1), which represents the channel domain of the receptor. Aged mouse eggs display abnormal Ca2+ homeostasis and express C-IP3R1, although whether or not C-IP3R1 expression contributes to Ca2+ misregulation or a decrease in developmental competency is unknown. We sought to answer these questions by injecting in mouse oocytes and eggs cRNAs encoding CIP3R1. We found that: 1) expression of C-IP3R1 in eggs lowered the Ca2+ content of the endoplasmic reticulum (ER), although, as C-IP3R1 is quickly degraded at this stage, its expression did not impair pre-implantation embryo development; 2) expression of CIP3R1 in eggs enhanced fragmentation associated with aging; 3) endogenous IP3R1 is required for aging associated apoptosis, as its down-regulation prevented fragmentation, and expression of C-IP3R1 in eggs with downregulated IP3R1 partly restored fragmentation; 4) C-IP3R1 expression in GV oocytes resulted in persistent levels of protein, which abolished the increase in the ER releasable Ca2+ pool that occurs during maturation, undermined the Ca2+ oscillatory ability of matured eggs and their activation potential. Collectively, this study supports a role for IP3R1 and C-IP3R1 in regulating Ca2+ homeostasis and the ER Ca2+ content during oocyte maturation. Nevertheless, the role of C-IP3R1 on Ca2+ homeostasis in aged eggs seems minor, as in MII eggs the majority of endogenous IP3R1 remains intact and C-IP3R1 undergoes rapid turnover.

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Caffeine alleviates the deterioration of Ca²⁺ release mechanisms and fragmentation of in vitro‐aged mouse eggs

Cited by 42 publications

References 99 publications

Oxidative stress and ageing of the post-ovulatory oocyte

Oxidative stress and ageing of the post-ovulatory oocyte

Oxidative Phosphorylation-linked Respiration in Individual Bovine Oocytes

Role of Caspase-3 Cleaved IP₃R1 on Ca²⁺Homeostasis and Developmental Competence of Mouse Oocytes and Eggs

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Caffeine alleviates the deterioration of Ca2+ release mechanisms and fragmentation of in vitro‐aged mouse eggs

Cited by 42 publications

References 99 publications

Oxidative stress and ageing of the post-ovulatory oocyte

Oxidative stress and ageing of the post-ovulatory oocyte

Oxidative Phosphorylation-linked Respiration in Individual Bovine Oocytes

Role of Caspase-3 Cleaved IP3R1 on Ca2+Homeostasis and Developmental Competence of Mouse Oocytes and Eggs

Contact Info

Product

Resources

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Caffeine alleviates the deterioration of Ca²⁺ release mechanisms and fragmentation of in vitro‐aged mouse eggs

Role of Caspase-3 Cleaved IP₃R1 on Ca²⁺Homeostasis and Developmental Competence of Mouse Oocytes and Eggs