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

Mary Kosinki, Kent McDonald, Joel Schwartz, Ikuko Yamamoto, David Greenstein

Research output: Contribution to journalArticlepeer-review

76 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)3357-3369
Number of pages13
JournalDevelopment
Volume132
Issue number15
DOIs
StatePublished - Aug 2005

Keywords

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

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