Saving energy for sex

January 14, 2003

Dr. David Greenstein and colleagues at Vanderbilt University School of Medicine (Nashville, Tennessee) have identified a sperm-sensing control mechanism through which worms can coordinate oocyte (egg cell) development with sperm availability. They have found that a receptor called VAB-1 is built into the oocyte cell membrane, and it signals oocyte maturation only when sperm are present. This discovery lends new insight into the molecular basis for energy-efficient reproduction in highly reproducing animals, like the roundworm C. elegans, whose relatives are the culprits in diseases like elephantiasis and river blindness and destroy billions of dollars worth of crops annually.

Like humans, C. elegans worm oocytes arrest during meiosis (the process of cell division in gamete-producing cells) and only resume in response to a specific activating signal. In C. elegans, the sperm signal to the oocyte using a so-called major sperm protein (MSP). The resumption of oocyte meiosis and ovulation are thereby coupled with sperm availability -- when the animal is afforded the best chance for successful fertilization.

Previous work by Dr. Greenstein's group, as well as by others, has identified several components of the oocyte maturation signal transduction pathway in C. elegans. It is known that MSP from the sperm activates a mitogen-activated protein kinase (MAPK) cascade of sequential protein phosphorylation events inside the oocyte, which intimately participate in the completion of meiosis. However, the identity of the oocyte cell surface molecule that receives and transmits the MSP signal to the intracellular MAPK machinery has, until now, remained a mystery.

As published in the January 15 issue of Genes & Development, Dr. Greenstein and colleagues report that MSP binding to the VAB-1 receptor culminates in oocyte maturation in C. elegans. VAB-1 was previously implicated as an ephrin protein receptor involved in mediating cell-to-cell interactions during epidermal morphogenesis. This finding by Dr. Greenstein and colleagues reveals an unexpected role for VAB-1 in reproduction.

C. elegans worms are facultative hermaphrodites, meaning that the species has both males and hermaphrodites, and is therefore capable of self- or cross-fertilization. In C. elegans, developing ooctyes travel along the gonad, or ovary, where the contraction of smooth muscle cells helps promote ovulation. Fertilization occurs when ovulating oocytes enter the sperm storage compartment, called the spermatheca.

Dr. Greenstein and colleagues have found that in the absence of sperm, VAB-1 represses MAPK activity and inhibits oocyte meiotic maturation. However, when sperm are present in the spermatheca, MSP is released and it binds VAB-1 on both the oocyte and sheath cell membranes. The researchers demonstrated that MSP antagonizes VAB-1 inhibition of the MAPK phosphorylation cascade and thereby promotes oocyte maturation. "In the case of sex, two wrongs can sometimes make a right", Greenstein says. VAB-1 also promotes the contraction of the ovarian smooth muscle cells to promote their contraction for ovulation.

Cold Spring Harbor Laboratory

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