Ion currents involved in oocyte maturation, fertilization and early developmental stages of the ascidian Ciona intestinalis

Abstract

SUMMARYElectrophysiological techniques were used to study the role of ion currents in the ascidian Ciona intestinalis oocyte plasma membrane during different stages of growth, meiosis, fertilization and early development. Three stages of immature oocytes were discriminated in the ovary, with the germinal vesicle showing specific different features of growth and maturation. Stage-A (pre-vitellogenic) oocytes exhibited the highest L-type calcium current activity and were incompetent for meiosis resumption. Stage-B (vitellogenic) oocytes showed a progressive disappearance of calcium currents and the first appearance of sodium currents that remained high during the maturation process, up to the postvitellogenic stage-C oocytes. The latter had acquired meiotic competence, undergoing spontaneous in vitro maturation and interacting with the spermatozoon. However, fertilized oocytes did not produce normal larvae, suggesting that cytoplasmic maturation may affect embryo development. In mature oocytes at the metaphase I stage, sodium currents were present and remained high up to the zygote stage. Oocytes fertilized in the absence of sodium showed significant reduction of the fertilization current amplitude and high development of anomalous ''rosette'' embryos. Current amplitudes became negligible in embryos at the 2-and 4-cell stage, whereas resumption of all the current activities occurred at the 8-cell embryo. Taken together, these results suggest: (i) an involvement of L-type calcium currents in initial oocyte meiotic progression and growth; (ii) a role of sodium currents at fertilization; (iii) a role of the fertilization current in ensuring normal embryo development.Mol.

Adverse Effect of Antifouling Compounds on the Reproductive Mechanisms of the Ascidian Ciona intestinalis

“…In particular, the characterization of plasma membrane ionic asset from mature and fertilized oocytes up to the 8-cell embryo, revealed that Na + currents first appear at the MI stage, remaining high up to the zygote stage. After that, Na + currents decrease in the 2- and 4-cell stages up to a second increased activity at the 8-cell stage [28]. …”

“…In ascidians, the impact of organotins on the reproductive processes has been widely studied [22,23,24,25]. In the ascidian Ciona intestinalis , the physiology of reproduction is well known and in particular, the electrical characteristics of the oocyte and embryo plasma membrane and the ions involved in fertilization have been well described [26,27,28]. The mature oocyte is blocked at metaphase I (MI), characterized by the presence of sodium (Na + ) currents and ready to be fertilized.…”

T-Type Ca2+ Current Activity during Oocyte Growth and Maturation in the Ascidian Styela plicata

“…The role of ion currents in the gametes physiology has been well described in many animal species [7], [11], [13]–[16]. A pivotal role in gamete physiology is played by different types of voltage dependent Ca 2+ currents; in particular, it has been shown that the high threshold L-type Ca 2+ currents are either expressed in the immature oocytes and modulate oocyte growth, cytoplasmic maturation and early embryo development in a variety of organisms [9], [10], [17]–[20]. T-type Ca 2+ channels are low voltage-gated channels that contribute to multiple physiological functions.…”

The Ascidian Ciona Intestinalis as Model Organism for Ecotoxicological Bioassays

“…From an experimental point of view, Ciona oocytes are relatively easy to manipulate and microinject, this further advantage has rendered this species a model to study reproductive mechanisms and meiotic regulation [3][4][5][6]. Ciona releases gametes (oocytes and sperm) into sea water where fertilization and embryo development occur.…”