Abstract
The molecular underpinnings of the oocyte-to-embryo transition are poorly understood. Here we show that two protein tyrosine phosphatase-like (PTPL) family proteins, EGG-4 and EGG-5, are required for key events of the oocyte-to-embryo transition in Caenorhabditis elegans. The predicted EGG-4 and EGG-5 amino acid sequences are 99% identical and their functions are redundant. In embryos lacking EGG-4 and EGG-5, we observe defects in meiosis, polar body formation, the block to polyspermy, F-actin dynamics, and eggshell deposition. During oogenesis, EGG-4 and EGG-5 assemble at the oocyte cortex with the previously identified regulators or effectors of the oocyte-to-embryo transition EGG-3, CHS-1, and MBK-2 [1, 2]. All of these molecules share a complex interdependence with regards to their dynamics and subcellular localization. Shortly after fertilization, EGG-4 and EGG-5 are required to properly coordinate a redistribution of CHS-1 and EGG-3 away from the cortex during meiotic anaphase I. Therefore, EGG-4 and EGG-5 are not only required for critical events of the oocyte-to-embryo transition but also link the dynamics of the regulatory machinery with the advancing cell cycle.
MeSH Terms
Amino Acid Sequence
Animals
Caenorhabditis elegans/embryology,genetics,metabolism
Caenorhabditis elegans Proteins/analysis,genetics,physiology
Chitin Synthase/analysis,genetics,physiology
Cytoplasm/metabolism
Embryonic Development/genetics
Meiosis/physiology
Molecular Sequence Data
Oocytes/cytology,growth & development,metabolism
Protein Transport
Protein-Tyrosine Kinases/analysis,genetics,physiology
Sequence Alignment
Chemicals
Caenorhabditis elegans Proteins
EGG-4 protein, C elegans
EGG-5 protein, C elegans
Chitin Synthase
MBK-2 protein, C elegans
Protein-Tyrosine Kinases
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Parry Jean M
Waksman Institute and Department of Genetics, Rutgers University, Piscataway, NJ 08854, USA.
Velarde Nathalie V
Lefkovith Ariel J
Zegarek Matthew H
Hang Julie S
Ohm Jonathan
Klancer Richard
Maruyama Rika
Druzhinina Marina K
Grant Barth D
Piano Fabio
Singson Andrew
References (14)
14 references, click to expand
-
EGG-3 regulates cell-surface and cortex rearrangements during egg activation in Caenorhabditis elegans.
Curr Biol. 2007 Sep 18;17(18):1555-60
PMID: 17869112
-
Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C. elegans.
Dev Cell. 2003 Sep;5(3):451-62
PMID: 12967564
-
Regulation of MBK-2/Dyrk kinase by dynamic cortical anchoring during the oocyte-to-zygote transition.
Curr Biol. 2007 Sep 18;17(18):1545-54
PMID: 17869113
-
Fertilization and sperm competition in the nematode Caenorhabditis elegans.
Dev Biol. 1979 Dec;73(2):304-21
PMID: 499670
-
Genes required for the common miracle of fertilization in Caenorhabditis elegans.
Int J Dev Biol. 2008;52(5-6):647-56
PMID: 18649278
-
Two membrane-associated tyrosine phosphatase homologs potentiate C. elegans AKT-1/PKB signaling.
PLoS Genet. 2006 Jul;2(7):e99
PMID: 16839187
-
On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans.
Dev Biol. 1999 Jan 1;205(1):111-28
PMID: 9882501
-
The C. elegans DYRK Kinase MBK-2 Marks Oocyte Proteins for Degradation in Response to Meiotic Maturation.
Curr Biol. 2006 Jan 10;16(1):56-62
PMID: 16338136
-
The Conserved Kinases CDK-1, GSK-3, KIN-19, and MBK-2 Promote OMA-1 Destruction to Regulate the Oocyte-to-Embryo Transition in C. elegans.
Curr Biol. 2006 Jan 10;16(1):47-55
PMID: 16343905
-
Gathering STYX: phosphatase-like form predicts functions for unique protein-interaction domains.
Trends Biochem Sci. 1998 Aug;23(8):301-6
PMID: 9757831
-
Developmental defects observed in hypomorphic anaphase-promoting complex mutants are linked to cell cycle abnormalities.
Development. 2003 Apr;130(8):1605-20
PMID: 12620985
-
Genetic requirements for PIE-1 localization and inhibition of gene expression in the embryonic germ lineage of Caenorhabditis elegans.
Dev Biol. 1998 Aug 15;200(2):212-24
PMID: 9705228
-
Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans.
Dev Biol. 2005 Jun 1;282(1):218-30
PMID: 15936342
-
The Caenorhabditis elegans spe-38 gene encodes a novel four-pass integral membrane protein required for sperm function at fertilization.
Development. 2005 Jun;132(12):2795-808
PMID: 15930110