C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes

Mary Kosinski,David Greenstein,Kent Mcdonald,Ikuko Yamamoto,Joel Schwartz

doi:10.1242/dev.01916

Mary Kosinski, David Greenstein + Show 3 more

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https://doi.org/10.1242/dev.01916

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Abstract

The major sperm protein (MSP) is the central cytoskeletal element required for actin-independent motility of nematode spermatozoa. MSP has a dual role in Caenorhabditis elegans reproduction, functioning as a hormone for both oocyte meiotic maturation and ovarian muscle contraction. The identification of the signaling function of MSP raised the question, how do spermatozoa, which are devoid of ribosomes, ER and Golgi, release a cytoplasmic protein lacking a signal sequence? Here, we provide evidence that MSP export occurs by the budding of novel vesicles that have both inner and outer membranes with MSP sandwiched in between. MSP vesicles are apparently labile structures that generate long-range MSP gradients for signaling at the oocyte cell surface. Both spermatozoa and non-motile spermatids bud MSP vesicles, but their stability and signaling properties differ. Budding protrusions from the cell body contain MSP, but not the MSD proteins, which counteract MSP filament assembly. We propose that MSP generates the protrusive force for its own vesicular export.

Highlights

Intercellular communication between sperm and oocyte is fundamental for sexual reproduction (Hardy, 2002)
Spermatozoa are only observed in the spermatheca and uterus; we observed major sperm protein (MSP) extending past the distal constriction into the proximal gonad arm
This staining represents MSP that is extracellular to spermatozoa

Summary

Introduction

Intercellular communication between sperm and oocyte is fundamental for sexual reproduction (Hardy, 2002). Long- and short-range signaling mechanisms control a medley of essential reproductive processes, including sperm chemotaxis, oocyte meiotic maturation, gamete recognition, cell fusion and egg activation. Sperm chemotaxis occurs in the mammalian female reproductive tract (Eisenbach and Tur-Kaspa, 1999) and may involve the function of conserved olfactory receptors (Spehr et al, 2003). Egg surface components, such as the ZP3 glycoprotein in mammals and the fucose sulfate polymer in sea urchins, mediate short-range signaling that induces the acrosome reaction, a highly specialized exocytic event needed for zona penetration and gamete fusion (Wassarman et al, 2001; Neill and Vacquier, 2004)

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