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Developmentally regulated cell cycle dependence of swelling-activated anion channel activity in the mouse embryo

Ottawa Health Research Institute, Hormones, Growth and Development Unit and Departments of Obstetrics and Gynecology (Division of Reproductive Medicine), and Cellular and Molecular Medicine, University of Ottawa, Ottawa, Ontario, K1Y 4E9 Canada

*Author for correspondence (e-mail: jbaltz{at}ohri.ca)

Accepted June 18, 2001

Anion channels activated by increased cell volume are a nearly ubiquitous mechanism of cell volume regulation, including in early preimplantation mouse embryos. Here, we show that the swelling-activated anion current (I_Cl,swell) in early mouse embryos is cell-cycle dependent, and also that this dependence is developmentally regulated. I_Cl,swell is present both in first meiotic prophase (germinal vesicle stage) mouse oocytes and in unfertilized mature oocytes in second meiotic metaphase, and it persists after fertilization though the 1-cell and 2-cell stages. I_Cl,swell was found to remain unchanged during metaphase at the end of the 1-cell stage. However, I_Cl,swell decreased during prophase and became nearly undetectable upon entry into metaphase at the end of the 2-cell stage. Entry into prophase/metaphase was required for the decrease in I_Cl,swell at the end of the 2-cell stage, since it persisted indefinitely in 2-cell embryos arrested in late G₂. There is considerable evidence that the channel underlying I_Cl,swell is not only permeable to inorganic anions, but to organic osmolytes as well. We found a similar pattern of cell cycle and developmental dependence in the 1-cell and 2-cell stages for the swelling-induced increase in permeability to the organic osmolyte glycine. Thus, entry into metaphase deactivates I_Cl,swell in embryos, but only after developmental progression through the 2-cell stage.

Key words: Preimplantation embryo, Volume regulation, Cell cycle, Metaphase, Ion channel, Mouse

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