Large P body-like RNPs form in C. elegans oocytes in response to arrested ovulation, heat shock, osmotic stress, and anoxia and are regulated by the major sperm protein pathway

Molly C. Jud, Michael J. Czerwinski, Megan P. Wood, Rachel A. Young, Christopher M. Gallo, Jeremy S. Bickel, Emily L. Petty, Jennifer M. Mason, Brent A. Little, Pamela A. Padilla, Jennifer A. Schisa

Research output: Contribution to journalArticlepeer-review

85 Scopus citations

Abstract

As Caenorhabditis elegans hermaphrodites age, sperm become depleted, ovulation arrests, and oocytes accumulate in the gonad arm. Large ribonucleoprotein (RNP) foci form in these arrested oocytes that contain RNA-binding proteins and translationally masked maternal mRNAs. Within 65 min of mating, the RNP foci dissociate and fertilization proceeds. The majority of arrested oocytes with foci result in viable embryos upon fertilization, suggesting that foci are not deleterious to oocyte function. We have determined that foci formation is not strictly a function of aging, and the somatic, ceh-18, branch of the major sperm protein pathway regulates the formation and dissociation of oocyte foci. Our hypothesis for the function of oocyte RNP foci is similar to the RNA-related functions of processing bodies (P bodies) and stress granules; here, we show three orthologs of P body proteins, DCP-2, CAR-1 and CGH-1, and two markers of stress granules, poly (A) binding protein (PABP) and TIA-1, appear to be present in the oocyte RNP foci. Our results are the first in vivo demonstration linking components of P bodies and stress granules in the germ line of a metazoan. Furthermore, our data demonstrate that formation of oocyte RNP foci is inducible in non-arrested oocytes by heat shock, osmotic stress, or anoxia, similar to the induction of stress granules in mammalian cells and P bodies in yeast. These data suggest commonalities between oocytes undergoing delayed fertilization and cells that are stressed environmentally, as to how they modulate mRNAs and regulate translation.

Original languageEnglish
Pages (from-to)38-51
Number of pages14
JournalDevelopmental Biology
Volume318
Issue number1
DOIs
StatePublished - Jun 1 2008

Keywords

  • Anoxia
  • C. elegans
  • Fertility
  • Heat shock
  • Major sperm protein
  • Oocyte
  • Osmotic stress
  • Ovulation
  • Processing body
  • RNP
  • Stress granule

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