An electrical block is required to prevent polyspermy in eggs fertilized by natural mating of Xenopus laevis

Grey, Robert D.; Bastiani, Michael J.; Webb, Dennis J.; Schertel, Eric R.

doi:10.1016/0012-1606(82)90335-9

Cited by 140 publications

(84 citation statements)

References 33 publications

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“…I Cl, Ca is required for the fast electrical block to polyspermy at fertilization (24). It is therefore critical that this current remains active in eggs.…”

Section: Resultsmentioning

confidence: 99%

Store-operated Calcium Entry Inactivates at the Germinal Vesicle Breakdown Stage of Xenopus Meiosis

Machaca

Haun

2000

Journal of Biological Chemistry

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Store-operated calcium entry (SOCE) is the predominant Ca2؉ influx pathway in non-excitable cells and is activated in response to depletion of intracellular Ca 2؉ stores. We have studied SOCE regulation during Xenopus oocyte meiosis. SOCE can be measured readily in stage VI Xenopus oocytes arrested at the G 2 -M transition of the cell cycle, either by Ca 2؉ imaging or by recording the SOCE current. However, following meiotic maturation, SOCE can no longer be activated by store depletion. We have characterized the time course of SOCE inactivation during oocyte maturation, and show that SOCE inactivates almost completely, in a very short time period, at the germinal vesicle breakdown stage of meiosis. This acute inactivation offers an opportunity to better understand SOCE regulation.Ionic calcium (Ca 2ϩ ) is a universal second messenger important for many cellular responses ranging from gene expression to fertilization (1). Ca 2ϩ signaling is mediated by a rise in cytoplasmic Ca 2ϩ , either by Ca 2ϩ release from intracellular stores or Ca 2ϩ influx from the extracellular space. In nonexcitable cells the primary Ca 2ϩ influx pathway is store-operated calcium entry (SOCE) 1 (2). SOCE is activated in response to depletion of intracellular calcium stores and has been implicated in several cellular processes, including T-cell activation (3, 4) and regulation of exocytosis (5-7). However the mechanism(s) coupling store depletion to SOCE activation remain unknown. The following three models have been proposed: "physical coupling," "diffusible messenger," and "vesicle fusion." The physical coupling hypothesis proposes that SOCE channels couple directly to a Ca 2ϩ sensor on the endoplasmic reticulum membrane, possibly the IP 3 receptor, in analogy to the dihydropyridine-ryanodine receptor interaction in skeletal muscle (8 -10). Whereas the diffusible messenger hypothesis argues that store depletion results in the generation of a diffusible messenger that opens SOCE channels (11-13), the vesicle fusion model proposes that SOCE channels are inserted in the plasma membrane following store depletion (14). Although there is some evidence for each model (2), it is not yet clear what the coupling mechanism is and whether SOCE is activated by the same mechanism in different cell types.Despite the importance and ubiquitous nature of Ca 2ϩ signaling pathways, their role and regulation during the cell cycle remain controversial. Probably the clearest example of a Ca 2ϩ requirement during the cell cycle is at fertilization, where a Ca 2ϩ signal is necessary and sufficient for egg activation and the initiation of embryonic development (15, 16). Oocytes of both Xenopus and mammals are arrested at the G 2 -M transition of the cell cycle (15, 17). Before such oocytes become competent to be fertilized and able to support embryonic development, they undergo a maturation process called meiotic (or oocyte) maturation. During this maturation period oocytes enter meiosis, complete the first meiotic division with the extrusion of a polar body,...

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“…I Cl, Ca is required for the fast electrical block to polyspermy at fertilization (24). It is therefore critical that this current remains active in eggs.…”

Section: Resultsmentioning

confidence: 99%

Store-operated Calcium Entry Inactivates at the Germinal Vesicle Breakdown Stage of Xenopus Meiosis

Machaca

Haun

2000

Journal of Biological Chemistry

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“…In the amphibian oocyte recent experiments have suggested that variations in Cl permeability may be involved in a number of processes associated with the cell membrane. These include responses to acetylcholine (Xenopu8: Kusano, Miledi & Stinnakre, 1977, to adenosine (Xenopwu: Lotan, Dascal, Cohen & Lass, 1982), and to fertilization and activation (Bufo: Maeno, 1959;Ito, 1972;Rana: Cross & Elinson, 1980; Xenopws: Grey, Bastiani, Webb & Schertel, 1982), and a standing electrical current found in immature oocytes (Xenopuw: Robinson, 1979).…”

Section: Introductionmentioning

confidence: 99%

A transient calcium‐dependent chloride current in the immature Xenopus oocyte.

Barish¹

1983

The Journal of Physiology

598

384

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SUMMARY1. Ionic currents were studied in immature full-grown Xenopus oocytes using the two-micro-electrode voltage-clamp technique.2. Recordings of total membrane current showed a transient outward peak during depolarizations from the approximate resting voltage (-70 or -80 mV) to voltages more positive than -20 mV. The current-voltage relation for peak outward current was nl-shaped, with a maximum at about 0 mV. 7. Increasing the external Ca concentration increased the amplitude of the transient outward current without affecting the amplitude of the steady-state current.8. It was concluded that the outward peak in records of total membrane current represented the contribution of a transient outward current carried by C1 ions which was dependent on the entry of external Ca. It will be noted as ICi(Ca)* 9. Decay of ICI(Ca) could be described at the normal Ca concentration by a single exponential function whose time constant showed a shallow U-shaped voltage dependence.10. ICI(ca) was maximally activatable by depolarizations from a holding potential of about -100 mV, but could not be activated by depolarizations from -40 mV.11. The amplitude of Icl(Ca) showed a large temperature dependence as compared to the steady-state current, suggesting complex control of its activation.

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“…The fertilization potential has a duration of 10-20 min and provides a fast, transient block to polyspermy (Cross & Elinson, 1980;Grey, Bastiani, Webb & Schertel, 1982;Jaffe, Cross & Picheral, 1983). The positive shift is caused by an increase in Cl-permeability (Maeno, 1959;Cross, 1981) and the presence of a Cl-gradient (44 mm inside, Jaffe & Schlichter, 1985, and a few millimolar outside).…”

Section: Introductionmentioning

confidence: 99%

Propagating potassium and chloride conductances during activation and fertilization of the egg of the frog, Rana pipiens.

Jaffe¹,

Kado²,

L³

1985

The Journal of Physiology

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SUMMARY1. Fertilization or artificial activation of the frog egg (Rana pipiens) elicits a positive-going shift in membrane potential which results from an opening of Cl-and K+ channels in the egg membrane. We examined the spatial localization of the currents produced by the opening of these channels, using large patch electrodes (tip diameters 3-10 ,um). We also used small patch electrodes (tip diameters about 1 /Im) to study the single K+ channel currents.2. After activation, with the patch electrode at any position on the egg surface, we observed a transient current, with a main peak lasting several seconds. This activation current occurred after a variable delay of 0-3 min following the rise of the activation potential. With 10 % Ringer solution in the bath and pipette, the current was usually outward, although it sometimes had an inward component.3. With one patch electrode on the animal surface of the egg and another patch electrode on the vegetal surface, we observed that the activation current propagated over the egg surface. In experiments where the egg was activated by applying a hyperpolarizing pulse, the response in the animal half preceded that in the vegetal half by an average of about 1 min. The amplitude of the peak outward current was similar for animal and vegetal recordings (1-2 mA/cm2).4. Tetraethylammonium (11 mM) in the patch pipette blocked most ofthe outward component of the activation current and revealed an underlying inward component.5. The inward component of the activation current was carried by Cl-, since it could be reversed by raising the Cl-concentration in the pipette.6. The Cl-component of the activation current propagated over the egg surface, with timing similar to that of the total current. 7. The average amplitude of the peak Cl-current was six or more times larger at the animal than the vegetal surface.8. Fertilization caused a current to propagate from the animal to the vegetal surface, like the current observed during activation.9. With a small patch electrode, single channel currents of the K+ component of the activation current could be seen. The probability that the channels were open increased at more positive potentials. The single channel conductance was estimated 8-2 228 L. A. JAFFE, R. T. KADO AND L. MUNCY to be 25 pS, and the reversal potential to be -150 mV. Single Cl-channel currents have not yet been seen.10. Activation or fertilization of the frog egg resulted in a wave-like opening of Cl-and K+ channels, which spread from the animal to the vegetal half of the egg. The Cl-conductance was larger on the animal half.

show abstract

An electrical block is required to prevent polyspermy in eggs fertilized by natural mating of Xenopus laevis

Cited by 140 publications

References 33 publications

Store-operated Calcium Entry Inactivates at the Germinal Vesicle Breakdown Stage of Xenopus Meiosis

Store-operated Calcium Entry Inactivates at the Germinal Vesicle Breakdown Stage of Xenopus Meiosis

A transient calcium‐dependent chloride current in the immature Xenopus oocyte.

Propagating potassium and chloride conductances during activation and fertilization of the egg of the frog, Rana pipiens.

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