DYRK2 and GSK-3 phosphorylate and promote the timely degradation of OMA-1, a key regulator of the oocyte-to-embryo transition in C. elegans

Dev Biol. 2005 Dec 1;288(1):139-49. doi: 10.1016/j.ydbio.2005.09.053. Epub 2005 Nov 11.

Abstract

Oocyte maturation and fertilization initiates a dynamic and tightly regulated process in which a non-dividing oocyte is transformed into a rapidly dividing embryo. We have shown previously that two C. elegans CCCH zinc finger proteins, OMA-1 and OMA-2, have an essential and redundant function in oocyte maturation. Both OMA-1 and OMA-2 are expressed only in oocytes and 1-cell embryos, and need to be degraded rapidly after the first mitotic division for embryogenesis to proceed normally. We report here a distinct redundant function for OMA-1 and OMA-2 in the 1-cell embryo. Depletion of both oma-1 and oma-2 in embryos leads to embryonic lethality. We also show that OMA-1 protein is directly phosphorylated at T239 by the DYRK kinase MBK-2, and that phosphorylation at T239 is required both for OMA-1 function in the 1-cell embryo and its degradation after the first mitosis. OMA-1 phosphorylated at T239 is only detected within a short developmental window of 1-cell embryos, beginning soon after the proposed activation of MBK-2. Phosphorylation at T239 facilitates subsequent phosphorylation of OMA-1 by another kinase, GSK-3, at T339 in vitro. Phosphorylation at both T239 and T339 are essential for correctly-timed OMA-1 degradation in vivo. We propose that a series of precisely-timed phosphorylation events regulates both the activity and the timing of degradation for OMA proteins, thereby allowing restricted and distinct functions of OMA-1 and OMA-2 in the maturing oocyte and 1-cell embryo, ensuring a normal oocyte-to-embryo transition in C. elegans.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / metabolism*
  • Caenorhabditis elegans Proteins / physiology
  • Carrier Proteins / metabolism*
  • Carrier Proteins / physiology
  • Embryo, Nonmammalian / embryology
  • Embryo, Nonmammalian / enzymology
  • Glycogen Synthase Kinase 3 / physiology*
  • Molecular Sequence Data
  • Oocytes / growth & development
  • Oocytes / metabolism*
  • Phosphorylation
  • Protein-Serine-Threonine Kinases / physiology*
  • Protein-Tyrosine Kinases / metabolism
  • Protein-Tyrosine Kinases / physiology*
  • Substrate Specificity / physiology
  • Tyrosine / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Carrier Proteins
  • OMA-1 protein, C elegans
  • oma-2 protein, C elegans
  • Tyrosine
  • Dyrk kinase
  • MBK-2 protein, C elegans
  • Protein-Tyrosine Kinases
  • Protein-Serine-Threonine Kinases
  • Glycogen Synthase Kinase 3