The onset of activation responsiveness during maturation coincides with the formation of the cortical endoplasmic reticulum in oocytes of Xenopus laevis

Charbonneau, Michel; Grey, Robert D.

doi:10.1016/0012-1606(84)90177-5

Cited by 122 publications

(65 citation statements)

References 24 publications

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“…ER remodeling has been described during maturation of Xenopus (Campanella et al, 1984;Charbonneau and Grey, 1984;Terasaki et al, 2001), mouse (Mehlmann et al, 1996), starfish (Jaffe and Terasaki, 1994), and hamster oocytes (Shiraishi et al, 1995) among others. Early ultrastructural studies in Xenopus show an enrichment of the ER in the cortex during oocyte maturation, where the ER tubules wrap around cortical granules (Gardiner and Grey, 1983;Campanella et al, 1984;Charbonneau and Grey, 1984). This reorganization of the ER brings the Ca 2þ source close to its primary targets in terms of the block to polyspermy: Ca 2þ -activated Cl channels at the cell membrane and cortical granules in the egg's cortex.…”

Section: Er Remodelingmentioning

confidence: 99%

Ca²⁺ signaling differentiation during oocyte maturation

Machaca

2007

Journal Cellular Physiology

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Oocyte maturation is an essential cellular differentiation pathway that prepares the egg for activation at fertilization leading to the initiation of embryogenesis. An integral attribute of oocyte maturation is the remodeling of Ca 2þ signaling pathways endowing the egg with the capacity to produce a specialized Ca 2þ transient at fertilization that is necessary and sufficient for egg activation. Consequently, mechanistic elucidation of Ca 2þ signaling differentiation during oocyte maturation is fundamental to our understanding of egg activation, and offers a glimpse into Ca 2þ signaling regulation during the cell cycle.

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Section: Er Remodelingmentioning

confidence: 99%

Ca²⁺ signaling differentiation during oocyte maturation

Machaca

2007

Journal Cellular Physiology

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“…Although the current data do not exclude the possibility that csp displays additional functions at nerve terminals (where Ca 2ϩ sensing is important for the stimulus-evoked release of transmitter), our results indicate that csp participates in the regulated exocytotic cascade at a step that is independent of Ca 2ϩ . This conclusion is based on the fact that, as reviewed in the Introduction, PMA-triggered cortical granule exocytosis in Xenopus oocytes does not involve changes of cytosolic Ca 2ϩ and proceeds normally even when cytosolic Ca 2ϩ is buffered (5)(6)(7)31). However, cortical granule exocytosis is significantly disrupted by the overexpression of full-length csp, and the remainder of this investigation was aimed at clarifying the basis of this secretory blockade.…”

Section: Discussionmentioning

confidence: 99%

Interaction between Constitutively Expressed Heat Shock Protein, Hsc 70, and Cysteine String Protein Is Important for Cortical Granule Exocytosis in Xenopus Oocytes

Smith

Umbach

Hirano

et al. 2005

Journal of Biological Chemistry

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In many species, binding of sperm to the egg initiates cortical granule exocytosis, an event that contributes to a sustained block of polyspermy. Interestingly, cortical granule exocytosis can be elicited in immature Xenopus oocytes by the protein kinase C activator, phorbol-12-myristate-13-acetate. In this study, we investigated the role of cysteine string protein (csp) in phorbol-12-myristate-13-acetate-evoked cortical granule exocytosis. Prior work indicated that csp is associated with cortical granules of Xenopus oocytes. In oocytes exhibiting >20-fold overexpression of full-length Xenopus csp, cortical granule exocytosis was reduced by ϳ80%. However, csp overexpression did not affect constitutive exocytosis. Subcellular fractionation and confocal fluorescence microscopy revealed that little or none of the overexpressed csp was associated with cortical granules. This accumulation of csp at sites other than cortical granules suggested that mislocalized csp might sequester a protein that is important for regulated exocytosis. Because the NH 2 -terminal region of csp includes a J-domain, which interacts with constitutively expressed 70-kDa heat shock proteins (Hsc 70), we evaluated the effect of overexpressing the J-domain of csp. Although the native J-domain of csp inhibited cortical granule exocytosis, point mutations that interfere with J-domain binding to Hsc 70 eliminated this inhibition. These data indicate that csp interaction with Hsc 70 molecular chaperones is vital for regulated secretion in Xenopus oocytes.Eggs of many species exhibit cortical granule exocytosis, an early postfertilization event that leads to a sustained block of polyspermy (1). Although oocytes of Xenopus laevis must undergo maturation before sperm can elicit cortical granule exocytosis, immature oocytes (and eggs) of Xenopus secrete in response to activators of protein kinase C (2). Somewhat unexpectedly (given that the majority of regulated secretory events are initiated by an increase of cytosolic Ca 2ϩ , Refs. 3 and 4), cortical granule exocytosis in Xenopus oocytes is insensitive to changes of cytosolic Ca 2ϩ . For instance, this secretory event is not triggered by Ca 2ϩ ionophores (using physiological concentrations of Ca 2ϩ ); it cannot be evoked by direct injection of Ca 2ϩ into the cytoplasm, and it is unaffected by removal of extracellular Ca 2ϩ or by buffers that clamp cytosolic Ca 2ϩ below the resting level (5-7). Thus, oocytes offer an empirical avenue for assessing the function of proteins in a secretory pathway where calcium ions play no direct role. This issue is of considerable importance with respect to cysteine string proteins (csp 2 (s)), a class of proteins found associated with a broad range of regulated secretory organelles (8 -10).Csp was originally identified as a novel synaptic antigen in Drosophila (11), and several subsequent investigations indicated that csp might be important as a modulator of presynaptic Ca 2ϩ channels (12-17). However, it also became evident that regulation of presynaptic Ca 2ϩ channe...

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“…As the maturation program unfolds, the cortex of the oocyte, which consists of the oocyte envelope, plasma membrane, and structures immediately underneath the plasma membrane, is greatly altered. Major ultrastructural changes that require new protein synthesis take place (1,7,8) and affect the enzymatic, transport, electrical, and contractile properties of the cortex (1, 9-12). As a result, the oocyte acquires the ability to propagate a wave of cortical granule exocytosis in response to the activation signals and the ability to block polyspermy.…”

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confidence: 99%

“…The fully grown, stage 6 oocyte that is arrested in prophase of meiosis I cannot be fertilized by sperm and fails to be activated when pricked with a needle or exposed to calcium ionophore A23187 (1). In vivo the follicle cells surrounding the oocyte secrete progesterone, which stimulates the oocyte to resume meiosis and undergo germinal vesicle breakdown (GVBD), chromosome condensation, and assembly of the meiosis I spindle.…”

mentioning

confidence: 99%

“…2 and 3). During the process of meiotic maturation, significant increases have been observed in protein synthesis and in posttranslational protein modifications, such as protein phosphorylation and dephosphorylation, which are believed to be necessary for the formation of a fertilizable egg (1,(4)(5)(6). As the maturation program unfolds, the cortex of the oocyte, which consists of the oocyte envelope, plasma membrane, and structures immediately underneath the plasma membrane, is greatly altered.…”

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confidence: 99%

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Xenopus Cdc6 confers sperm binding competence to oocytes without inducing their maturation

Tian

Thomsen

Gong

et al. 1997

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

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Amphibian eggs normally require meiotic maturation to be competent for fertilization. A necessary prerequisite for this event is sperm binding, and we show that under normal physiological conditions this property is acquired at, but not before, meiotic maturation. Immature oocytes do not bind sperm, but injection of total egg poly(A) ؉ mRNA into immature oocytes confers sperm binding in the absence of meiotic maturation. Using an expression cloning approach we have isolated a single cDNA from egg poly(A) ؉ mRNA that can induce sperm binding in immature oocytes. The cDNA was found to encode Xenopus Cdc6, a protein that previously has been shown to function in initiation of DNA replication and cell cycle control. This unanticipated finding provides evidence of a link between a regulator of the cell cycle and alterations in cell surface properties that affect gamete binding.Progesterone-induced meiotic maturation is a crucial step in the development of fertilizability in Xenopus oocytes. The fully grown, stage 6 oocyte that is arrested in prophase of meiosis I cannot be fertilized by sperm and fails to be activated when pricked with a needle or exposed to calcium ionophore A23187 (1). In vivo the follicle cells surrounding the oocyte secrete progesterone, which stimulates the oocyte to resume meiosis and undergo germinal vesicle breakdown (GVBD), chromosome condensation, and assembly of the meiosis I spindle. After a highly asymmetrical cell division that generates the first polar body, the oocyte enters meiosis II and arrests at metaphase (reviewed in refs. 2 and 3). During the process of meiotic maturation, significant increases have been observed in protein synthesis and in posttranslational protein modifications, such as protein phosphorylation and dephosphorylation, which are believed to be necessary for the formation of a fertilizable egg (1, 4-6). As the maturation program unfolds, the cortex of the oocyte, which consists of the oocyte envelope, plasma membrane, and structures immediately underneath the plasma membrane, is greatly altered. Major ultrastructural changes that require new protein synthesis take place (1,7,8) and affect the enzymatic, transport, electrical, and contractile properties of the cortex (1, 9-12). As a result, the oocyte acquires the ability to propagate a wave of cortical granule exocytosis in response to the activation signals and the ability to block polyspermy. The capacity of the oocyte to initiate DNA replication also appears during maturation, possibly as a result of accumulation and posttranslational modifications of components required for this process (13).The meiotic maturation process takes about 5-6 hr after which the mature oocytes are ovulated into the coelomic cavity of the frog. The resulting coelomic eggs can be activated by ionophore or pricking and can be fertilized by sperm to yield normal embryos if the coelomic egg envelope (CE) is removed (14). This removal is required because sperm cannot penetrate the CE (15).The transformation of the CE to the sperm-...

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The onset of activation responsiveness during maturation coincides with the formation of the cortical endoplasmic reticulum in oocytes of Xenopus laevis

Cited by 122 publications

References 24 publications

Ca²⁺ signaling differentiation during oocyte maturation

Ca²⁺ signaling differentiation during oocyte maturation

Interaction between Constitutively Expressed Heat Shock Protein, Hsc 70, and Cysteine String Protein Is Important for Cortical Granule Exocytosis in Xenopus Oocytes

Xenopus Cdc6 confers sperm binding competence to oocytes without inducing their maturation

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The onset of activation responsiveness during maturation coincides with the formation of the cortical endoplasmic reticulum in oocytes of Xenopus laevis

Cited by 122 publications

References 24 publications

Ca2+ signaling differentiation during oocyte maturation

Ca2+ signaling differentiation during oocyte maturation

Interaction between Constitutively Expressed Heat Shock Protein, Hsc 70, and Cysteine String Protein Is Important for Cortical Granule Exocytosis in Xenopus Oocytes

Xenopus Cdc6 confers sperm binding competence to oocytes without inducing their maturation

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Ca²⁺ signaling differentiation during oocyte maturation

Ca²⁺ signaling differentiation during oocyte maturation