Sperm and oocytes communicate and, in some organisms, such as Caenorhabditis elegans, sperm promote oocyte maturation through resumption of meiosis. Major sperm protein (MSP) serves a cytoskeletal role within spermatozoa and also serves as a hormone signaling oocyte meiotic maturation and ovarian muscle contraction in C. elegans. Kosinski et al. used immunofluorescence microscopy to show that MSP appears inside the spermatozoa and extracellularly in the proximal gonad arm (the site of the unfertilized oocytes) and in the uterus. Transmission electron microscopy (TEM), combined with immunohistochemistry, of samples prepared by high-pressure freezing and freeze substitution revealed the presence of a novel class of MSP-positive extracellular double-membrane vesicles in the spermatheca, in the uterine lumen, and between embryos. In wild-type hermaphrodites, oocyte maturation ceases and activation of mitogen-activated protein kinase (MAPK) decreases as sperm are depleted. MSP also becomes undetectable following sperm depletion. In mutant worms defective in spermiogenesis (they make spermatids, but these do not mature), oocyte maturation and MAPK activation persisted after spermatids were no longer present. MSP was also faintly detectable, suggesting that spermatids and spermatozoa release distinct MSP signals. Spermatid-released MSP is more stable than spermatozoa-released MSP. Thus, vesicle budding through a nontraditional secretory pathway (sperm lack endoplasmic reticulum and Golgi) appears to provide a mechanism of sperm-egg communication.
M. Kosinski, K. McDonald, J. Schwartz, I. Yamamoto, D. Greenstein, C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes. Development 132, 3357-3369 (2005). [Abstract] [Full Text]