Spatiotemporal dynamics of intracellular [Ca2+](i) oscillations during the growth and meiotic maturation of mouse oocytes

J. Carroll, K. Swann, D. Whittingham, M. Whitaker

Research output: Contribution to journalArticleResearchpeer-review

153 Citations (Scopus)

Abstract

Calcium oscillations occur during meiotic maturation of mouse oocytes. They also trigger activation at fertilization. We have monitored [Ca2+](i) in oocytes at different stages of growth and maturation to examine how the calcium release mechanisms alter during oogenesis. Spontaneous calcium oscillations occur every 2-3 minutes in the majority of fully grown (but immature) mouse oocytes released from antral follicles and resuming meiosis. The oscillations last for 2-4 hours after release from the follicle and take the form of global synchronous [Ca2+](i) increases throughout the cell. Rapid image acquisition or cooling the bath temperature from 28°C to 16°C did not reveal any wave-like spatial heterogeneity in the [Ca2+](i) signal. Calcium appears to reach highest levels in the germinal vesicle but this apparent difference of [Ca2+] in nucleus and cytoplasm is an artifact of dye loading. Smaller, growing immature oocytes are less competent: about 40% are able to resume meiosis and a similar proportion of these oocytes show spontaneous calcium oscillations. [Ca2+](i) transients are not seen in oocytes that do not resume meiosis spontaneously in vitro. Nonetheless, these oocytes are capable of [Ca2+](i) oscillations since they show them in response to the addition of carbachol or thimerosal. To examine how the properties of calcium release change during meiotic maturation, a calcium-releasing factor from sperm was microinjected into fully grown immature and mature oocytes. The sperm-factor-induced oscillations were about two-fold larger and longer in mature oocytes compared to immature oocytes. Calcium waves travelling at 40-60 μm/second were generated in mature oocytes, but not in immature oocytes. In some mature oocytes, successive calcium waves had different sites of origin. The modifications in the size and spatial organization of calcium transients during oocyte maturation may be a necessary prerequisite for normal fertilization.

Original languageEnglish
Pages (from-to)3507-3517
Number of pages11
JournalDevelopment
Volume120
Issue number12
Publication statusPublished - 1 Jan 1994
Externally publishedYes

Keywords

  • Calcium
  • Confocal
  • Meiotic maturation
  • Mouse
  • Oocyte

Cite this