Regulated trafficking of the MSP/Eph receptor during oocyte meiotic maturation in C. elegans

Curr Biol. 2008 May 20;18(10):705-714. doi: 10.1016/j.cub.2008.04.043. Epub 2008 May 8.


Background: In C. elegans, a sperm-sensing mechanism regulates oocyte meiotic maturation and ovulation, tightly coordinating sperm availability and embryo production; sperm release the major sperm protein (MSP) signal to trigger meiotic resumption. Meiotic arrest depends on the parallel function of the oocyte VAB-1 MSP/Eph receptor and somatic G protein signaling. MSP promotes meiotic maturation by antagonizing Eph receptor signaling and counteracting inhibitory inputs from the gonadal sheath cells.

Results: Here, we present evidence suggesting that in the absence of the MSP ligand, the VAB-1 Eph receptor inhibits meiotic maturation while either in or in transit to the endocytic-recycling compartment. VAB-1::GFP localization to the RAB-11-positive endocytic-recycling compartment is independent of ephrins but is antagonized by MSP signaling. Two negative regulators of oocyte meiotic maturation, DAB-1/Disabled and RAN-1, interact with the VAB-1 receptor and are required for its accumulation in the endocytic-recycling compartment in the absence of MSP or sperm (hereafter referred to as MSP/sperm). Inactivation of the endosomal recycling regulators rme-1 or rab-11.1 causes a vab-1-dependent reduction in the meiotic-maturation rate in the presence of MSP/sperm. Further, we show that Galpha(s) signaling in the gonadal sheath cells, which is required for meiotic maturation in the presence of MSP/sperm, affects VAB-1::GFP trafficking in oocytes.

Conclusions: Regulated endocytic trafficking of the VAB-1 MSP/Eph receptor contributes to the control of oocyte meiotic maturation in C. elegans. Eph receptor trafficking in other systems may be influenced by the conserved proteins DAB-1/Disabled and RAN-1 and by crosstalk with G protein signaling in neighboring cells.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adaptor Proteins, Vesicular Transport / metabolism
  • Animals
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Cycle Proteins / metabolism*
  • Endocytosis
  • Female
  • GTP-Binding Protein alpha Subunits, Gs / metabolism
  • Green Fluorescent Proteins / metabolism
  • Helminth Proteins / metabolism*
  • Male
  • Meiosis / physiology*
  • Nuclear Proteins / metabolism
  • Oocytes / cytology
  • Oocytes / physiology*
  • Ovulation
  • Receptor Protein-Tyrosine Kinases / metabolism*
  • Signal Transduction
  • Spermatozoa / physiology
  • rab GTP-Binding Proteins / metabolism


  • Adaptor Proteins, Vesicular Transport
  • Caenorhabditis elegans Proteins
  • Cell Cycle Proteins
  • DAB-1 protein, C elegans
  • Helminth Proteins
  • Nuclear Proteins
  • major sperm protein, nematode
  • ran-binding protein 1
  • Green Fluorescent Proteins
  • Receptor Protein-Tyrosine Kinases
  • vab-1 protein, C elegans
  • rab11 protein
  • GTP-Binding Protein alpha Subunits, Gs
  • rab GTP-Binding Proteins