Fertilization potential in golden hamster eggs consists of recurring hyperpolarizations

Miyazaki, Shunichi; Igusa, Yukio

doi:10.1038/290702a0

Cited by 149 publications

(73 citation statements)

References 21 publications

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“…Nevertheless, whether or not such changes happened during normal fertilization and how their inhibition affected development was unknown. Evidence soon accumulated, first using the luminescent protein "aequorin" synthesized by Shimomura and colleagues (Shimomura and Johnson 1970) that explosive [Ca 2þ ] i increases accompanied fertilization in medaka fish eggs (Ridgway et al 1977) and in sea urchin eggs (Steinhardt et al 1977 (Cuthbertson et al 1981;Miyazaki and Igusa 1981). Although oscillatory [Ca 2þ ] i responses were subsequently reported in nonmammalian species, mammalian eggs are the only ones whose oscillations extend for over several hours (Stricker 1999).…”

Section: Events Of Egg Activation Require [Ca 2þ ] I Increasesmentioning

confidence: 99%

Ca2+ Signaling During Mammalian Fertilization: Requirements, Players, and Adaptations

Wakai¹,

Vanderheyden²,

Fissore³

2011

Cold Spring Harbor Perspectives in Biology

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Changes in the intracellular concentration of calcium ([Ca 2þ ] i ) represent a vital signaling mechanism enabling communication among cells and between cells and the environment. The initiation of embryo development depends on a [Ca 2þ ] i increase(s) in the egg, which is generally induced during fertilization. The [Ca 2þ ] i increase signals egg activation, which is the first stage in embryo development, and that consist of biochemical and structural changes that transform eggs into zygotes. The spatiotemporal patterns of [Ca 2þ ] i at fertilization show variability, most likely reflecting adaptations to fertilizing conditions and to the duration of embryonic cell cycles. In mammals, the focus of this review, the fertilization [Ca 2þ ] i signal displays unique properties in that it is initiated after gamete fusion by release of a sperm-derived factor and by periodic and extended [Ca 2þ ] i responses. Here, we will discuss the events of egg activation regulated by increases in [Ca 2þ ] i , the possible downstream targets that effect these egg activation events, and the property and identity of molecules both in sperm and eggs that underpin the initiation and persistence of the [Ca 2þ ] i responses in these species.A n increase in the intracellular concentration of calcium ([Ca 2þ ] i ) underlies the initiation, progression and/or completion of a wide variety of cellular processes, including fertilization, muscle contraction, secretion, cell division, and apoptosis (Berridge et al. 2000). To survive and proliferate, cells and organisms must communicate, and changes in [Ca 2þ ] i allow them to quickly respond to environmental, nutritional, or ligand challenges with responses that regulate cell fate and function. Cells devote significant amounts of their energy reserves to create and maintain ionic gradients between extracellular and intracellular milieus and also within the latter, thereby allowing brief alterations in these gradients to have profound signaling effects. In the case of Ca 2þ , myriad proteins have acquired the ability to bind Ca 2þ , which allows them to interpret and transform these elevations into cellular functions. This review will examine the cellular modifications induced by [Ca 2þ ] i changes during fertilization in mature mammalian oocytes, henceforth referred to as eggs.Oocytes during maturation ready themselves for fertilization and the initiation of embryogenesis. During this transition, oocytes undergo changes that include the resumption and progression of meiosis, the development of polyspermy-preventing mechanisms, the reorganization of the cytoskeleton with spindle formation and displacement to the cortex, and the translation, accumulation, and degradation of specific mRNAs and proteins involved in development (Horner and Wolfner 2008b (Stricker 1999;Miyazaki and Ito 2006). Elucidation of the signaling cascades and identification of the molecules/receptor(s) that initiate the Ca 2þ signal at fertilization has proven elusive, and this review will not dwell on th...

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Section: Events Of Egg Activation Require [Ca 2þ ] I Increasesmentioning

confidence: 99%

Ca2+ Signaling During Mammalian Fertilization: Requirements, Players, and Adaptations

Wakai¹,

Vanderheyden²,

Fissore³

2011

Cold Spring Harbor Perspectives in Biology

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“…While non-mammalian species (i.e. frogs, several marine invertebrates) use a membrane block that involves a rapid and transient depolarization of egg membrane potential (Jaffe & Gould 1985, Gould & Stephano 2003, it appears that the mammalian membrane block works by a different mechanism as membrane depolarization is not observed in fertilized mouse, hamster, or rabbit eggs (Miyazaki & Igusa 1981, Igusa et al 1983, Jaffe et al 1983, McCulloh et al 1983.…”

Section: Introductionmentioning

confidence: 99%

Establishment of the mammalian membrane block to polyspermy: evidence for calcium-dependent and -independent regulation

2007

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One crucial result of egg activation is the establishment of blocks on the zona pellucida and the egg plasma membrane to prevent fertilization by additional sperm. The mechanism(s) by which a mammalian egg regulates the establishment of the membrane block to polyspermy is largely unknown. Since Ca 2C signaling regulates several egg activation events, this study investigates how sperm-induced Ca 2C transients affect the membrane block to polyspermy, building on our previous work (Biology of ] cyt regulate the timing of membrane block establishment, as this block is established more slowly in eggs that experience one or no sperm-induced Ca 2C transients. Finally, our studies produce the intriguing discovery that there is also a Ca 2C -independent event that is associated with fertilization in the pathway leading to membrane block establishment. Taken together, these data indicate that Ca 2C plays a role in facilitating membrane block establishment by regulating the timing with which this change in egg membrane function occurs, and also that the membrane block differs from other post-fertilization egg activation responses as Ca 2C is not the only stimulus.The membrane block to polyspermy in mammalian eggs is likely to be the culmination of multiple post-fertilization events that together modify the egg membrane's receptivity to sperm.

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“…Release of a spermspecific phospholipase C isoform (PLCζ) likely initiates the inositol 1,4,5-trisphosphate (IP 3 )-mediated increase in [Ca 2+ ] i (3). In mammalian eggs, this increase in [Ca 2+ ] i takes the form of repetitive Ca 2+ transients (oscillations) that last several hours (4,5). Although Ca 2+ oscillations can induce all of the EEA, individual events require different numbers of [Ca 2+ ] i transients to be initiated and completed, with early events requiring fewer oscillations than late events (6).…”

mentioning

confidence: 99%

The γ isoform of CaM kinase II controls mouse egg activation by regulating cell cycle resumption

Backs

Stein

Backs

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

107

110

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Fertilization triggers a rise in intracellular Ca 2+ concentration ([Ca 2+ ] i ) in the egg that initiates a series of events known as egg activation. These events include cortical granule exocytosis that establishes a block to polyspermy, resumption of meiosis, and recruitment of maternal mRNAs into polysomes for translation. Several calcium-dependent proteins, including calcium/calmodulin-dependent protein kinase II (CaMKII), have been implicated in egg activation. However, the precise role of CaMKII in mediating specific events of egg activation and the identity of the isoform(s) present in mouse eggs have not been unequivocally established. Through targeted deletion of the γ isoform of CaMKII, we find that CaMKIIγ is the predominant CaMKII isoform in mouse eggs and that it is essential for egg activation. Although CaMKIIγ −/− eggs exhibit a normal pattern of Ca 2+ oscillations after insemination and undergo cortical granule exocytosis, they fail to resume meiosis or to recruit maternal mRNAs. Surprisingly, we find that the recruitment of maternal mRNAs does not directly depend on CaMKII, but requires elevated [Ca 2+ ] i and metaphase II exit. We conclude that CaMKIIγ specifically controls mouse egg activation by regulating cell cycle resumption.T he transition from a fertilization-competent mammalian egg to a developing embryo entails a sequence of events collectively known as egg activation. Early events of egg activation include modifications of the zona pellucida (ZP) that prevent polyspermy, exit from metaphase II arrest, and completion of meiosis, whereas late events include recruitment of maternal mRNAs into polysomes for translation and formation of male and female pronuclei (1). In all animal species studied to date, a rise in intracellular calcium ([Ca 2+ ] i ) is the universal trigger of all of the events of egg activation (EEA) (2). Release of a spermspecific phospholipase C isoform (PLCζ) likely initiates the inositol 1,4,5-trisphosphate (IP 3 )-mediated increase in [Ca 2+ ] i (3). In mammalian eggs, this increase in [Ca 2+ ] i takes the form of repetitive Ca 2+ transients (oscillations) that last several hours (4, 5). Although Ca 2+ oscillations can induce all of the EEA, individual events require different numbers of [Ca 2+ ] i transients to be initiated and completed, with early events requiring fewer oscillations than late events (6).The pathways that connect the rise in [Ca 2+ ] i to the different EEA have only been partially elucidated. Protein kinases, including calcium/calmodulin-dependent protein kinase II (CaM-KII), and the phosphatase calcineurin have been postulated as integrators of the Ca 2+ signal during egg activation (7-9). However, direct genetic evidence for involvement of these enzymes through loss-of-function studies is lacking, leaving open questions as to whether any single enzyme is essential for all of the EEA or whether these Ca 2+ -dependent events are mediated by different effectors.The CaMKII family of serine/threonine kinases mediates many cellular responses to C...

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Fertilization potential in golden hamster eggs consists of recurring hyperpolarizations

Cited by 149 publications

References 21 publications

Ca2+ Signaling During Mammalian Fertilization: Requirements, Players, and Adaptations

Ca2+ Signaling During Mammalian Fertilization: Requirements, Players, and Adaptations

Establishment of the mammalian membrane block to polyspermy: evidence for calcium-dependent and -independent regulation

The γ isoform of CaM kinase II controls mouse egg activation by regulating cell cycle resumption

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