Thapsigargin induces cytoplasmic free Ca2+ oscillations in mouse oocytes

Lawrence, Yvonne; Cuthbertson, K. S. R.

doi:10.1016/0143-4160(95)90084-5

Cited by 14 publications

(14 citation statements)

References 45 publications

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“…Additionally, it can not be ruled out that the effect of [Ca 2+ ] ER is related to changes in cytosolic [Ca 2+ ] i in the IP 3 R1 microdomain, as it is well known that cytosolic Ca 2+ is a major regulator of IP 3 R1 activity. Furthermore, little is known about how [Ca 2+ ] ER is controlled in oocytes, although the presence of SERCA has been surmised in these cells by the alteration in [Ca 2+ ] i levels caused by exposure to thapsigargin (Kline and Kline, 1992; Lawrence and Cuthbertson, 1995; Machaty et al, 2002) and here to CPA. Importantly, our results with CPA and plcζ show that without a full [Ca 2+ ] ER the first [Ca 2+ ] i rise is compromised, and that under persistent inhibition of SERCA and inability to refill [Ca 2+ ] ER, the amplitude of the rises is diminished and oscillations cease prematurely.…”

Section: Discussionmentioning

confidence: 99%

Regulation of inositol 1,4,5‐trisphosphate receptor function during mouse oocyte maturation

Wakai

Vanderheyden

Yoon

et al. 2011

Journal Cellular Physiology

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At the time of fertilization, an increase in the intracellular Ca2+ concentration ([Ca2+]i) underlies egg activation and initiation of development in all species studied to date. The inositol 1,4,5-trisphosphate receptor (IP3R1), which is mostly located in the endoplasmic reticulum (ER) mediates the majority of this Ca2+ release. The sensitivity of IP3R1, i.e. its Ca2+ releasing capability, is increased during oocyte maturation so that the optimum [Ca2+]i response concurs with fertilization, which in mammals occurs at metaphase of second meiosis. Multiple IP3R1 modifications affect its sensitivity, including phosphorylation, sub-cellular localization and ER Ca2+ concentration ([Ca2+]ER). Here we evaluated using mouse oocytes how each of these factors affected IP3R1 sensitivity. The capacity for IP3-induced Ca2+ release markedly increased at the germinal vesicle breakdown stage, although oocytes only acquire the ability to initiate fertilization-like oscillations at later stages of maturation. The increase in IP3R1 sensitivity was underpinned by an increase in [Ca2+]ER and receptor phosphorylation(s) but not by changes in IP3R1 cellular distribution, as inhibition of the former factors reduced Ca2+ release, whereas inhibition of the latter had no impact. Therefore, the results suggest that the regulation of [Ca2+]ER and IP3R1 phosphorylation during maturation enhance IP3R1 sensitivity rendering oocytes competent to initiate oscillations at the expected time of fertilization. The temporal discrepancy between the initiation of changes in IP3R1 sensitivity and acquisition of mature oscillatory capacity suggest that other mechanisms that regulate Ca2+ homeostasis also shape the pattern of oscillations in mammalian eggs.

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Section: Discussionmentioning

confidence: 99%

Regulation of inositol 1,4,5‐trisphosphate receptor function during mouse oocyte maturation

Wakai

Vanderheyden

Yoon

et al. 2011

Journal Cellular Physiology

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“…ATPases (SERCAs), and/or extrude it by the action of plasma membrane (PM) Ca 2þ ATPases (PMCAs) and Na þ /Ca 2þ exchangers (Berridge et al 2000;Bootman et al 2001). Few studies have addressed the function of these molecules in mammalian oocytes/eggs, although the presence of SERCA2b can be surmised by the alteration of [Ca 2þ ] i levels caused by exposure to thapsigargin, an inhibitor of SERCA (Kline and Kline 1992b;Lawrence and Cuthbertson 1995;Machaty et al 2002). Exposure of MII eggs to thapsigargin causes a slow and steady increase in [Ca 2þ ] i followed by a protracted decline, whereas in fertilized eggs it prevents the continuation of oscillations (Kline and Kline 1992b).…”

Section: Ip 3 R1 In Maturing Oocytesmentioning

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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“…4C; Fig influx also contributes to the robust first [Ca 2+ ] i rise (Halet et al, 2004 (Dumollard et al, 2004;Liu et al, 2001). To ascertain whether inhibition of mitochondrial function involved ER Ca 2+ homeostasis, we exposed oscillating eggs to an inhibitor of mitochondrial ATP synthase (Wolvetang et al, 1994) ] i levels caused by their exposure to thapsigargin or cyclopiazonic acid (CPA), two SERCA inhibitors; these inhibitors also prevent continuation of [Ca 2+ ] i oscillations in oscillating eggs (Kline and Kline, 1992;Lawrence and Cuthbertson, 1995;Macháty et al, 2002). Nevertheless, the precise rate of change of [Ca 2+ ] ER caused by SERCA inhibition has not been elucidated in these cells.…”

Section: Introductionmentioning

confidence: 99%