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Development 132 (15): 3357-3369

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

Mary Kosinski1, Kent McDonald2, Joel Schwartz3, Ikuko Yamamoto1, and David Greenstein1,*

1 Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, 465 21st Avenue South, Nashville, TN 37232, USA
2 Electron Microscopy Laboratory, University of California, Berkeley, 26 Giannini Hall, Berkeley, CA 94720-3330, USA
3 Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, 465 21st Avenue South, Nashville, TN 37232, USA

* Author for correspondence (e-mail: david.greenstein{at}vanderbilt.edu)

Accepted for publication 23 May 2005.

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.

Key Words: Oogenesis • Meiotic maturation • Gamete interactions • Major sperm protein signaling • Vesicle budding • Unconventional protein secretion

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