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An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans
Michael A Miller1, Paul J Ruest, Mary Kosinski
1Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee 37232, USA.
Abstract:
During sexual reproduction in most animals, oocytes arrest in meiotic prophase and resume meiosis (meiotic maturation) in response to sperm or somatic cell signals. Despite progress in delineating mitogen-activated protein kinase (MAPK) and CDK/cyclin activation pathways involved in meiotic maturation, it is less clear how these pathways are regulated at the cell surface. The Caenorhabditis elegans major sperm protein (MSP) signals oocytes, which are arrested in meiotic prophase, to resume meiosis and ovulate. We used DNA microarray data and an in situ binding assay to identify the VAB-1 Eph receptor protein-tyrosine kinase as an MSP receptor. We show that VAB-1 and a somatic gonadal sheath cell-dependent pathway, defined by the CEH-18 POU-class homeoprotein, negatively regulate meiotic maturation and MAPK activation. MSP antagonizes these inhibitory signaling circuits, in part by binding VAB-1 on oocytes and sheath cells. Our results define a sperm-sensing control mechanism that inhibits oocyte maturation, MAPK activation, and ovulation when sperm are unavailable for fertilization. MSP-domain proteins are found in diverse animal taxa, where they may regulate contact-dependent Eph receptor signaling pathways.
Insights
Sperm signals oocytes to mature via the VAB-1 Eph receptor, antagonizing inhibitory pathways. This sperm-sensing mechanism ensures oocyte maturation only occurs when fertilization is possible.
Area of Science:
- Reproductive Biology
- Cell Signaling
- Developmental Biology
Background:
- Oocyte maturation is crucial for sexual reproduction, typically arrested in meiotic prophase until triggered by fertilization cues.
- Mitogen-activated protein kinase (MAPK) and CDK/cyclin pathways are key regulators of meiotic maturation, but cell-surface regulation remains less understood.
- In Caenorhabditis elegans, major sperm protein (MSP) signals oocytes to resume meiosis and ovulate.
Purpose of the Study:
- To identify the cell-surface receptor for major sperm protein (MSP) in Caenorhabditis elegans.
- To elucidate the signaling pathways by which MSP regulates oocyte maturation.
- To define the role of the VAB-1 Eph receptor and associated pathways in controlling meiotic maturation and ovulation.
Main Methods:
- Utilized DNA microarray data to identify potential MSP receptors.
- Employed in situ binding assays to confirm VAB-1 as an MSP receptor.
- Investigated the regulatory roles of VAB-1 and the CEH-18 pathway in oocyte maturation and MAPK activation.
Main Results:
- Identified the VAB-1 Eph receptor protein-tyrosine kinase as a direct receptor for MSP on oocytes and gonadal sheath cells.
- Demonstrated that VAB-1 and a pathway involving CEH-18 negatively regulate oocyte meiotic maturation and MAPK activation.
- Showed that MSP antagonizes these inhibitory signals, promoting oocyte maturation and ovulation.
Conclusions:
- Defined a novel sperm-sensing mechanism involving MSP and the VAB-1 Eph receptor that inhibits oocyte maturation when sperm are absent.
- This pathway ensures timely oocyte maturation and ovulation, coordinating reproduction with fertilization.
- MSP-domain proteins likely play conserved roles in regulating contact-dependent Eph receptor signaling across diverse animal taxa.