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Title: GLUTATHIONE (GSH) CONCENTRATIONS VARY WITH THE CELL CYCLE IN MATURING HAMSTER OOCYTES, ZYGOTES AND PRE-IMPLANTATION STAGE EMBRYOS

Author
item Zuelke, Kurt
item JEFFAY, SUSAN - US EPA
item ZUCKER, ROBERT - US EPA
item PERREAULT, SALLY - US EPA

Submitted to: Journal of Molecular Reproduction and Development
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/2/2002
Publication Date: 1/1/2003
Citation: Zuelke, K.A., Jeffay, S.C., Zucker, R.M., Perreault, S.D. 2003. Glutathione (gsh) concentrations vary with the cell cycle in maturing hamster oocytes, zygotes and pre-implantation stage embryos. Journal of Molecular Reproduction and Development 64:106-112.

Interpretive Summary: Glutathione (GSH) is an ubiquitous intracellular molecule that mediates oxidative stress within cells. In mammalian oocytes, GSH is thought to play critical roles in oocyte function including spindle maintenance and providing the intracellular environment needed to initiate remodelling of the sperm nucleus in the oocyte after fertilization. Previous observations suggested that GSH synthesis may be associated with early cell cycle events associated with the oocyte maturation and fertilization processes. Using Golden hamster oocytes and zygotes as a model for gametes from livestock species, we measured the concentrations of glutathione (GSH) at specific stages of oocyte maturation and at intervals during the first complete embryonic cell cycle. Between 2 and 4 hours after the hormonal induction of oocyte maturation, GSH concentrations increased significantly (~ doubling) in both oocytes and the associated cumulus cells that typically provide the oocyte with nutritive support during the maturation process. This increase was concurrent with early, maturation-related, changes in the oocyte nucleus. GSH remained high in ovulated, mature oocytes, but then declined significantly, by about 50%, shortly after fertilization, as the early embryo developed. GSH concentrations then plummeted by the two-cell embryo stage and remained at only 10% of those in mature oocytes throughout the first 4 days of development. These results demonstrate that oocyte GSH concentrations fluctuate dramatically to already achieve maximal concentrations already during the first 4 hours of oocyte maturation. This increase in GSH coincided with critical developmental processes such as meiotic spindle formation and preparation for sperm chromatin remodeling after fertilization. These observations suggest that GSH synthesis in maturing oocytes is regulated by the hormones that initiate the maturation process, and suggest that GSH is more important during fertilization than during post-fertilization embryo development.

Technical Abstract: Glutathione (GSH) is thought to play critical roles in oocyte function including spindle maintenance and provision of reducing power needed to initiate sperm chromatin decondensation. Previous observations that GSH concentrations are higher in mature than immature oocytes and decline after fertilization, suggest that GSH synthesis may be associated with cell cycle events. To explore this possibility, we measured the concentrations of glutathione (GSH) in Golden hamster oocytes and zygotes at specific stages of oocyte maturation and at intervals during the first complete embryonic cell cycle. Between 2 and 4 hours after the hormonal induction of oocyte maturation, GSH concentrations increased significantly (~ doubling) in both oocytes and their associated cumulus cells. This increase was concurrent with germinal vesicle breakdown and the condensation of metaphase I chromosomes in the oocyte. GSH remained high in ovulated, metaphase II oocytes, but then declined significantly, by about 50%, shortly after fertilization, as the zygote progressed back into interphase (the pronucleus stage). GSH concentrations then plummeted by the two-cell embryo stage and remained at only 10% of those in metaphase II oocytes throughout pre-implantation development. These results demonstrate that oocyte GSH concentrations fluctuate with the cell cycle, being highest during meiotic metaphase, the critical period for spindle growth and development and for sperm chromatin remodeling. These observations raise the possibility that GSH synthesis in maturing oocytes is regulated by gonadotropins, and suggest that GSH is more important during fertilization than during pre-implantation embryo development.