Gαo/i and Gαs Signaling Function in Parallel with the MSP/Eph Receptor to Control Meiotic Diapause in C. elegans

J. Amaranath Govindan; Hua Cheng; Jana E. Harris; David Greenstein

doi:10.1016/j.cub.2006.05.020

Gα_o/i and Gα_s Signaling Function in Parallel with the MSP/Eph Receptor to Control Meiotic Diapause in C. elegans

J. Amaranath Govindan, Hua Cheng, Jana E. Harris, David Greenstein

Research output: Contribution to journal › Article › peer-review

88 Scopus citations

Abstract

Background: A conserved biological feature of sexual reproduction in animals is that oocytes arrest in meiotic prophase and resume meiosis in response to extraovarian signals. In C. elegans, sperm trigger meiotic resumption by means of the major sperm protein (MSP) signal. MSP promotes meiotic resumption by functioning as an ephrin-signaling antagonist and by counteracting inhibitory inputs from the somatic gonadal sheath cells. Results: By using a genome-wide RNAi screen in a female-sterile genetic background, we identified 17 conserved genes that maintain meiotic arrest in the absence of the MSP signal. In vitro binding experiments show that MSP promotes oocyte mitogen-activated protein kinase activation and meiotic maturation in part through direct interaction with the VAB-1 Eph receptor. Four conserved proteins, including a disabled protein (DAB-1), a vav family GEF (VAV-1), a protein kinase C (PKC-1), and a STAM homolog (PQN-19), function with the VAB-1 Eph/MSP receptor in oocytes. We show that antagonistic Gα_o/i and Gα_s signaling pathways function in the soma to regulate meiotic maturation in parallel to the VAB-1 pathway. Gα_s activity is necessary and sufficient to promote meiotic maturation, which it does in part by antagonizing inhibitory sheath/oocyte gap-junctional communication. Conclusions: Our findings show that oocyte Eph receptor and somatic cell G protein signaling pathways control meiotic diapause in C. elegans, highlighting contrasts and parallels between MSP signaling in C. elegans and luteinizing hormone signaling in mammals.

Original language	English (US)
Pages (from-to)	1257-1268
Number of pages	12
Journal	Current Biology
Volume	16
Issue number	13
DOIs	https://doi.org/10.1016/j.cub.2006.05.020
State	Published - Jul 11 2006
Externally published	Yes

Bibliographical note

Funding Information:
We are grateful to the Caenorhabditis Genetic Center, Bob Barstead, Jonathan Cooper, Mark Edgley, Darren Kamikura, John Kim, Michael Koelle, Jane Mendel, Shohei Mitani, Gary Molder, Ron Plasterk, Tom Roberts, Gary Ruvkun, and Paul Sternberg for providing strains and reagents. We are indebted to Eric Lambie for sharing his recipe for RNAi-screening media. We thank Todd Starich and Jocelyn Shaw for helpful discussions about innexins. Thanks to Graham Carpenter and Ethan Lee for guidance on receptor biochemistry and to Mary Kosinski, Ikuko Yamamoto, and the anonymous reviewers for helpful suggestions and comments on the manuscript. This work was supported by NIH grants GM65115 and GM57173 (D.G.) and an NIH Training Grant 2T32HD007043-31 (J.E.H.).

Keywords

DEVBIO
SIGNALING

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title = "Gαo/i and Gαs Signaling Function in Parallel with the MSP/Eph Receptor to Control Meiotic Diapause in C. elegans",

abstract = "Background: A conserved biological feature of sexual reproduction in animals is that oocytes arrest in meiotic prophase and resume meiosis in response to extraovarian signals. In C. elegans, sperm trigger meiotic resumption by means of the major sperm protein (MSP) signal. MSP promotes meiotic resumption by functioning as an ephrin-signaling antagonist and by counteracting inhibitory inputs from the somatic gonadal sheath cells. Results: By using a genome-wide RNAi screen in a female-sterile genetic background, we identified 17 conserved genes that maintain meiotic arrest in the absence of the MSP signal. In vitro binding experiments show that MSP promotes oocyte mitogen-activated protein kinase activation and meiotic maturation in part through direct interaction with the VAB-1 Eph receptor. Four conserved proteins, including a disabled protein (DAB-1), a vav family GEF (VAV-1), a protein kinase C (PKC-1), and a STAM homolog (PQN-19), function with the VAB-1 Eph/MSP receptor in oocytes. We show that antagonistic Gαo/i and Gαs signaling pathways function in the soma to regulate meiotic maturation in parallel to the VAB-1 pathway. Gαs activity is necessary and sufficient to promote meiotic maturation, which it does in part by antagonizing inhibitory sheath/oocyte gap-junctional communication. Conclusions: Our findings show that oocyte Eph receptor and somatic cell G protein signaling pathways control meiotic diapause in C. elegans, highlighting contrasts and parallels between MSP signaling in C. elegans and luteinizing hormone signaling in mammals.",

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author = "Govindan, {J. Amaranath} and Hua Cheng and Harris, {Jana E.} and David Greenstein",

note = "Funding Information: We are grateful to the Caenorhabditis Genetic Center, Bob Barstead, Jonathan Cooper, Mark Edgley, Darren Kamikura, John Kim, Michael Koelle, Jane Mendel, Shohei Mitani, Gary Molder, Ron Plasterk, Tom Roberts, Gary Ruvkun, and Paul Sternberg for providing strains and reagents. We are indebted to Eric Lambie for sharing his recipe for RNAi-screening media. We thank Todd Starich and Jocelyn Shaw for helpful discussions about innexins. Thanks to Graham Carpenter and Ethan Lee for guidance on receptor biochemistry and to Mary Kosinski, Ikuko Yamamoto, and the anonymous reviewers for helpful suggestions and comments on the manuscript. This work was supported by NIH grants GM65115 and GM57173 (D.G.) and an NIH Training Grant 2T32HD007043-31 (J.E.H.). ",

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T1 - Gαo/i and Gαs Signaling Function in Parallel with the MSP/Eph Receptor to Control Meiotic Diapause in C. elegans

AU - Govindan, J. Amaranath

AU - Cheng, Hua

AU - Harris, Jana E.

AU - Greenstein, David

N1 - Funding Information: We are grateful to the Caenorhabditis Genetic Center, Bob Barstead, Jonathan Cooper, Mark Edgley, Darren Kamikura, John Kim, Michael Koelle, Jane Mendel, Shohei Mitani, Gary Molder, Ron Plasterk, Tom Roberts, Gary Ruvkun, and Paul Sternberg for providing strains and reagents. We are indebted to Eric Lambie for sharing his recipe for RNAi-screening media. We thank Todd Starich and Jocelyn Shaw for helpful discussions about innexins. Thanks to Graham Carpenter and Ethan Lee for guidance on receptor biochemistry and to Mary Kosinski, Ikuko Yamamoto, and the anonymous reviewers for helpful suggestions and comments on the manuscript. This work was supported by NIH grants GM65115 and GM57173 (D.G.) and an NIH Training Grant 2T32HD007043-31 (J.E.H.).

PY - 2006/7/11

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N2 - Background: A conserved biological feature of sexual reproduction in animals is that oocytes arrest in meiotic prophase and resume meiosis in response to extraovarian signals. In C. elegans, sperm trigger meiotic resumption by means of the major sperm protein (MSP) signal. MSP promotes meiotic resumption by functioning as an ephrin-signaling antagonist and by counteracting inhibitory inputs from the somatic gonadal sheath cells. Results: By using a genome-wide RNAi screen in a female-sterile genetic background, we identified 17 conserved genes that maintain meiotic arrest in the absence of the MSP signal. In vitro binding experiments show that MSP promotes oocyte mitogen-activated protein kinase activation and meiotic maturation in part through direct interaction with the VAB-1 Eph receptor. Four conserved proteins, including a disabled protein (DAB-1), a vav family GEF (VAV-1), a protein kinase C (PKC-1), and a STAM homolog (PQN-19), function with the VAB-1 Eph/MSP receptor in oocytes. We show that antagonistic Gαo/i and Gαs signaling pathways function in the soma to regulate meiotic maturation in parallel to the VAB-1 pathway. Gαs activity is necessary and sufficient to promote meiotic maturation, which it does in part by antagonizing inhibitory sheath/oocyte gap-junctional communication. Conclusions: Our findings show that oocyte Eph receptor and somatic cell G protein signaling pathways control meiotic diapause in C. elegans, highlighting contrasts and parallels between MSP signaling in C. elegans and luteinizing hormone signaling in mammals.

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