Editors' ChoiceReproduction

Traffic Control for Oocytes

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Science Signaling  27 May 2008:
Vol. 1, Issue 21, pp. ec198
DOI: 10.1126/stke.121ec198

The nematode C. elegans, not wanting to waste its resources, produces mature oocytes through meiotic maturation only when the presence of sperm is detected. The detection system consists of a transmembrane receptor protein, VAB-1, which recognizes a secreted sperm protein known as MSP (major sperm protein). Constitutive signaling through VAB-1 appears to hold oocytes in check, and the signal from sperm decreases such signaling to allow the oocyte to mature. VAB-1 occurs on both the oocytes themselves and gonadal sheath cells. Cheng et al. used a fusion protein of green fluorescent protein (GFP) linked to VAB-1 to monitor the receptor’s location and report that regulation of endocytic trafficking of the receptor might provide a critical control point for the regulation of oocyte maturation. In the absence of sperm, VAB-1::GFP was localized with a marker of recycling endosomes at the cortex. In hermaphrodites (which make their own sperm), VAB-1 was found instead in larger cytoplasmic vesicles. In a mutant in which vesicle transport from the recycling compartment to the plasma membrane is inhibited, VAB-1::GFP accumulated in the endocytic recycling compartment and maturation was inhibited. A search for proteins that interacted with the intracellular domain of VAB-1 yielded RAN-1, which was previously genetically identified as a negative regulator of oocyte maturation but is better known for its role in controlling nuclear transport. Depletion of RAN-1 with RNAi reduced the abundance of VAB-1::GFP in the cortex and enhanced accumulation in the larger cytoplasmic vesicles. The sheath cells do their part through signaling that requires a heterotrimeric guanine nucleotide-binding protein (G protein) and gap-junction channels. Disruption of these elements with RNAi appeared to diminish the signals required to inhibit maturation in the absence of sperm and led exclusion of VAB-1::GFP from the recycling endosome compartment. Although cause and effect remain to be formally established, the authors propose that the gonadal sheath cells may have a primary role in sensing MSP and then influence trafficking in the oocyte and, thus, its ability to respond directly to MSP. As Hang et al. note in commentary, why the double layer of regulation is required and exactly how VAB-1 trafficking regulates signaling by the receptor are among a series of new directions for study that are brought into focus by the new results.

H. Cheng, J. A. Govindan, D. Greenstein, Regulated trafficking of the MSP/Eph receptor during oocyte meiotic maturation in C. elegans. Curr. Biol. 18, 705-714 (2008). [PubMed]

J. S. Hang, B. D. Grant, A. Singson, Meiotic maturation: Receptor trafficking is the key. Curr. Biol. 18, R416-R418 (2008). [PubMed]

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