A novel mechanism controls the Ca2+ oscillations triggered by activation of ascidian eggs and has an absolute requirement for Cdk1 activity

Levasseur, Mark; Carroll, Michael A.; Jones, Kevin; McDougall, Alex

doi:10.1242/jcs.003012

Cited by 17 publications

(11 citation statements)

References 52 publications

(53 reference statements)

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“…In another ascidian, A. aspersa, DN-cyclin B steadily activates Cdk1 and prolongs the sperm-induced [Ca 2 þ ] i oscillations (Levasseur and McDougall, 2000). Furthermore, it has been shown that Cdk1 activity is both necessary and sufficient for phase II [Ca 2 þ ] i oscillations (Levasseur et al, 2007). In the present study, GST-D85N-cyclin B also maintained ERK activity and prolonged the period of [Ca 2 þ ] i oscillations in the Phallusia eggs; the period of [Ca 2 þ ] i oscillations correlated with both ERK and Cdk1 activities.…”

Section: Effect Of Cdk1 On [Ca 2 þ ] I Oscillationssupporting

confidence: 69%

Role of Mos/MEK/ERK cascade and Cdk1 in Ca2+ oscillations in fertilized ascidian eggs

Sensui

Yoshida

Tachibana

2012

Developmental Biology

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Intracellular calcium ion concentration ([Ca(2+)](i)) transients are observed in the fertilized eggs of all species investigated so far, and are critical for initiating several events related to egg activation and cell cycle control. Here, we investigated the role of the Mos/MEK/ERK cascade and Cdk1 on Ca(2+) oscillations in fertilized ascidian eggs. The egg of the ascidian Phallusia nigra shows [Ca(2+)](i) oscillations after fertilization: Ca(2+) waves immediately following fertilization (phase I), and [Ca(2+)](i) oscillations between the first and second polar body extrusions (phase II). Our results show that in P. nigra eggs, ERK activity peaked just before the extrusion of the first polar body, and decreased gradually, eventually disappearing at the extrusion of the second polar body. Cyclin-dependent protein kinase 1(Cdk1) activity decreased to undetectable levels immediately after fertilization, and then periodically increased according to the meiotic and mitotic cell cycle. When the unfertilized eggs were incubated with U0126, an inhibitor of MEK, before insemination, ERK was immediately inactivated, and the phase II [Ca(2+)](i) oscillations disappeared. Alternatively, when the constitutively active Mos protein (GST-Mos) was injected into the unfertilized eggs, ERK activity was preserved for at least 120 min after fertilization, and the phase II [Ca(2+)](i) oscillations lasted for more than 120 min after the second polar body extrusion. These results suggest that ERK activity is necessary for maintaining [Ca(2+)](i) oscillations. GST-ΔN85-cyclin, which maintains Cdk1 activity, caused ERK activity in the eggs to persist for over 120 min after fertilization, and prolonged [Ca(2+)](i) oscillations. Moreover, the effects of GST-ΔN85-cyclin on the egg were abrogated by the application of U0126. Thus, Cdk1-mediated [Ca(2+)](i) oscillations seem to require ERK activity. However, GST-Mos triggered [Ca(2+)](i) oscillations after the second polar body extrusion, whereas GST-ΔN85-cyclin did not, although it prolongs the duration of [Ca(2+)](i) oscillations. Interestingly, GST-ΔN85-cyclin increased the frequency of [Ca(2+)](i) transients in the Mos-induced [Ca(2+)](i) oscillations after the extrusion of the second polar body. Thus, Cdk1 could maintain, but not activate, ERK and [Ca(2+)](i) oscillations. ERK activity and [Ca(2+)](i) oscillations seem to form a negative feedback loop which may be responsible for maintaining the meiotic period.

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Section: Effect Of Cdk1 On [Ca 2 þ ] I Oscillationssupporting

confidence: 69%

Role of Mos/MEK/ERK cascade and Cdk1 in Ca2+ oscillations in fertilized ascidian eggs

Sensui

Yoshida

Tachibana

2012

Developmental Biology

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“…In C. intestinalis, we firstly demonstrated that MPF kinase activity is significantly high in metaphase-I blocked oocytes and decreases after fertilization and sperm-triggered calcium oscillation (Russo et al, 1996). Other authors confirmed and extended our initial observation (McDougall and Levasseur, 1998;Levasseur and McDougall, 2000;Levasseur et al, 2007). This can be considered an initial and circumstantial evidence on the existence of a CSF activity able to stabilize MPF complex.…”

Section: Presence Of a Csf-like Activity In C Intestinalissupporting

confidence: 82%

Phylogenetic conservation of cytostatic factor related genes in the ascidian Ciona intestinalis

Russo¹,

Bilotto²,

Ciarcia³

et al. 2009

Gene

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“…In analyses of Ca 2+ signals and cell‐cycle kinases during ascidian fertilization, MPF has been shown to upregulate Ca 2+ ‐wave production, given that oscillations occur when MPF activity is normally elevated or artificially raised; conversely, oscillations are blocked when MPF is either naturally deactivated (between meiotic divisions and at the end of meiosis) or experimentally downregulated by MPF inhibitors (Levasseur and McDougall, ; Levasseur et al, ; Sensui et al, ). Based on several lines of evidence, MPF‐mediated stimulation of Ca 2+ signals involves the modulation of IP 3 levels rather than alteration in IP 3 R sensitivity to IP 3 (Levasseur and McDougall, ; Levasseur et al, ).…”

Section: Comparative Biology Of Fertilization‐induced Calcium Signalsmentioning

confidence: 99%

Comparative biology of sperm factors and fertilization‐induced calcium signals across the animal kingdom

Kashir

Deguchi

Jones

et al. 2013

Molecular Reproduction Devel

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SUMMARYFertilization causes mature oocytes or eggs to increase their concentrations of intracellular calcium ions (Ca 2þ ) in all animals that have been examined, and such Ca 2þ elevations, in turn, provide key activating signals that are required for non-parthenogenetic development. Several lines of evidence indicate that the Ca 2þ transients produced during fertilization in mammals and other taxa are triggered by soluble factors that sperm deliver into oocytes after gamete fusion. Thus, for a broad-based analysis of Ca 2þ dynamics during fertilization in animals, this article begins by summarizing data on soluble sperm factors in non-mammalian species, and subsequently reviews various topics related to a sperm-specific phospholipase C, called PLCz, which is believed to be the predominant activator of mammalian oocytes. After characterizing initiation processes that involve sperm factors or alternative triggering mechanisms, the spatiotemporal patterns of Ca 2þ signals in fertilized oocytes or eggs are compared in a taxon-by-taxon manner, and broadly classified as either a single major transient or a series of repetitive oscillations. Both solitary and oscillatory types of fertilization-induced Ca 2þ signals are typically propagated as global waves that depend on Ca 2þ release from the endoplasmic reticulum in response to increased concentrations of inositol 1,4,5-trisphosphate (IP 3 ). Thus, for taxa where relevant data are available, upstream pathways that elevate intraoocytic IP 3 levels during fertilization are described, while other less-common modes of producing Ca 2þ transients are also examined. In addition, the importance of fertilization-induced Ca 2þ signals for activating development is underscored by noting some major downstream effects of these signals in various animals.Mol. Reprod. Dev. 80: 787À815,

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A novel mechanism controls the Ca2+ oscillations triggered by activation of ascidian eggs and has an absolute requirement for Cdk1 activity

Cited by 17 publications

References 52 publications

Role of Mos/MEK/ERK cascade and Cdk1 in Ca2+ oscillations in fertilized ascidian eggs

Role of Mos/MEK/ERK cascade and Cdk1 in Ca2+ oscillations in fertilized ascidian eggs

Phylogenetic conservation of cytostatic factor related genes in the ascidian Ciona intestinalis

Comparative biology of sperm factors and fertilization‐induced calcium signals across the animal kingdom

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