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March 22, 2016

Embryo Viability Teeters on Mother-Daughter Split

  • The first complete, real-time recording of an egg cell eliminating its centrioles shows the starfish egg cell handles mature ‘mother’ centrioles (green) differently from immature ‘daughter’ centrioles (purple). [EMBL/Joana Borrego-Pinto]

     

  • While much of what is known about the earliest stages of fertilization and embryo development has been revealed through molecular evidence, scientists still have a number of questions about the process that remain unanswered. Moreover, researchers have yet to visualize many steps in the embryo development process from beginning to end—for instance, how egg cells discard their centrioles to ensure the proper cell division after fertilization.

    On the surface, the cell biology of sexual reproduction is straightforward: Sperm and egg unite to create an embryo. However, once that process is over, the complexities begin to mount exponentially. Simply combining the genetic content of two cells would lead to disaster because every generation would carry twice as much DNA as its parents. To prevent this, egg and sperm cells halve their genetic content before fusing.

    A similar issue arises with structures in the nucleus called centrioles. Centrioles serve as anchors for the spindle apparatus, which pulls genetic material apart during cell division. If a fertilized egg has centrioles from both the egg cell and the sperm, its genetic material would be pulled in too many directions and shared unevenly between the resulting cells, making the embryo unviable or heavily mutated. So in animals, before an egg cell is fertilized by a sperm, its centrioles are eliminated, ensuring that the resulting embryo receives only the sperm's centrioles.     

    Now, researchers at the European Molecular Biology Laboratory (EMBL) in Heidelberg have been able to capture the entire process visually, in real time, of how egg cells eject their centrioles. The findings from this study were published recently in the Journal of Cell Biology in an article entitled “Distinct Mechanisms Eliminate Mother and Daughter Centrioles in Meiosis of Starfish Oocytes.”

    During the cell division process, each anchor point is a pair of centrioles—a mature mother centriole and an immature daughter centriole.

    "Mother centrioles are known to be very, very stable," explained senior study author Péter Lénárt, Ph.D., group leader at EMBL. "In the worm C. elegans, people have tagged a mother centriole in the sperm, and found it still intact in the late embryo!"

    To investigate how egg cells manage to rid themselves of such resilient structures, the EMBL team developed fluorescent tags for mother and daughter centrioles in a starfish egg cell and recorded the entire process of eliminating them.

    Interestingly, the investigators found that egg cells expel the two mother centrioles, ditching them into the two polar bodies, which also serve as dumps for excess genetic material. One daughter centriole is also dragged into a polar body, leaving the other daughter centriole alone in the egg cell.

    “This only happens in egg cell formation," noted lead study author Joana Borrego-Pinto, Ph.D., who is currently a postdoctoral researcher at the Crick Institute. "In a normal division, a single daughter centriole is never left alone. It seems that if this daughter is alone, it is unstable, and will be degraded, but if we make a mother centriole stay in the cell, it doesn't get destroyed, so the fertilized egg ends up with a tripolar spindle and can't divide."

    Upon further examination by electron microscopy, the scientists found that mother centrioles are expelled into polar bodies thanks to little appendages that centrioles acquire as they mature—suggesting that these appendages direct mother centrioles to the cell membrane, ready for ejection.

    The EMBL team was excited by their findings and are looking to probe deeper into how mother centrioles are transported and ejected, and investigate how and why isolated daughter centrioles break down.

    "Eggs are incredibly diverse—think of chickens, frogs, and starfish—so I doubt that this is exactly the same in all animals," remarked Dr. Lénárt. "But underlying that diversity are conserved modules like the centrioles. By understanding the molecular logic of how those modules can be combined in different ways, we can begin to reconstruct how this diversity evolved."

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