Eph and NMDA receptors control Ca2+/calmodulin-dependent protein kinase II activation during C-elegans oocyte meiotic maturation

C Corrigan, R Subramanian, M A Miller

Research output: Contribution to journalArticlepeer-review

42 Citations (Scopus)

Abstract

Fertilization in the female reproductive tract depends on intercellular signaling mechanisms that coordinate sperm presence with oocyte meiotic progression. To achieve this coordination in Caenorhabditis elegans, sperm release an extracellular signal, the major sperm protein (MSP), to induce oocyte meiotic maturation and ovulation. MSP binds to multiple receptors, including the VAB-1 Eph receptor protein-tyrosine kinase on oocyte and ovarian sheath cell surfaces. Canonical VAB-1 ligands called ephrins negatively regulate oocyte maturation and MPK-1 mitogen-activated protein kinase (MAPK) activation. Here, we show that MSP and VAB-1 regulate the signaling properties of two Ca2+ channels that are encoded by the NMR-1 N-methyl D-aspartate type glutamate receptor subunit and ITR-1 inositol 1,4,5-triphosphate receptor. Ephrin/VAB-1 signaling acts upstream of ITR-1 to inhibit meiotic resumption, while NMR-1 prevents signaling by the UNC-43 Ca2+/calmodulin-dependent protein kinase II (CaMKII). MSP binding to VAB-1 stimulates NMR-1-dependent UNC-43 activation, and UNC-43 acts redundantly in oocytes to promote oocyte maturation and MAPK activation. Our results support a model in which VAB-1 switches from a negative regulator into a redundant positive regulator of oocyte maturation upon binding to MSP NMR-1 mediates this switch by controlling UNC-43 CaMKII activation at the oocyte cortex.

Original languageEnglish
Pages (from-to)5225-5237
Number of pages13
JournalDevelopment (Cambridge): for advances in developmental biology and stem cells
Volume132
Issue number23
DOIs
Publication statusPublished - 1 Dec 2005

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