Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Subscribe

Logo for

Genes & Dev. 17 (2): 187-200

Copyright © 2003 by Cold Spring Harbor Laboratory Press.

Vol. 17, No. 2, pp. 187-200, January 15, 2003

RESEARCH PAPER
An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans

Michael A. Miller, Paul J. Ruest, Mary Kosinski, Steven K. Hanks, and David Greenstein1

Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee 37232, USA

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.

[Key Words: Meiosis; meiotic maturation; Eph receptor; soma-germline interactions; major sperm protein; ephrin]

1 Corresponding author.

GENES & DEVELOPMENT 17:187-200 © 2003 by Cold Spring Harbor Laboratory Press  ISSN 0890-9369/03 $5.00

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
SACY-1 DEAD-Box Helicase Links the Somatic Control of Oocyte Meiotic Maturation to the Sperm-to-Oocyte Switch and Gamete Maintenance in Caenorhabditis elegans.
S. Kim, J. A. Govindan, Z. J. Tu, and D. Greenstein (2012)
Genetics 192, 905-928
   Abstract »    Full Text »    PDF »
Sperm Status Regulates Sexual Attraction in Caenorhabditis elegans.
N. S. Morsci, L. A. Haas, and M. M. Barr (2011)
Genetics 189, 1341-1346
   Abstract »    Full Text »    PDF »
Developmental Control of Oocyte Maturation and Egg Activation in Metazoan Models.
J. R. Von Stetina and T. L. Orr-Weaver (2011)
Cold Spring Harb Perspect Biol 3, a005553
   Abstract »    Full Text »    PDF »
The EGR family gene egrh-1 functions non-autonomously in the control of oocyte meiotic maturation and ovulation in C. elegans.
L. M. Clary and P. G. Okkema (2010)
Development 137, 3129-3137
   Abstract »    Full Text »    PDF »
A practical, bioinformatic workflow system for large data sets generated by next-generation sequencing.
C. Cantacessi, A. R. Jex, R. S. Hall, N. D. Young, B. E. Campbell, A. Joachim, M. J. Nolan, S. Abubucker, P. W. Sternberg, S. Ranganathan, et al. (2010)
Nucleic Acids Res. 38, e171
   Abstract »    Full Text »    PDF »
Caenorhabditis elegans FOS-1 and JUN-1 Regulate plc-1 Expression in the Spermatheca to Control Ovulation.
S. M. Hiatt, H. M. Duren, Y. J. Shyu, R. E. Ellis, N. Hisamoto, K. Matsumoto, K.-i. Kariya, T. K. Kerppola, and C.-D. Hu (2009)
Mol. Biol. Cell 20, 3888-3895
   Abstract »    Full Text »    PDF »
Somatic cAMP signaling regulates MSP-dependent oocyte growth and meiotic maturation in C. elegans.
J. A. Govindan, S. Nadarajan, S. Kim, T. A. Starich, and D. Greenstein (2009)
Development 136, 2211-2221
   Abstract »    Full Text »    PDF »
MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth in C. elegans.
S. Nadarajan, J. A. Govindan, M. McGovern, E. J. A. Hubbard, and D. Greenstein (2009)
Development 136, 2223-2234
   Abstract »    Full Text »    PDF »
Reduction in ovulation or male sex phenotype increases long-term anoxia survival in a daf-16-independent manner in Caenorhabditis elegans.
A. R. Mendenhall, M. G. LeBlanc, D. P. Mohan, and P. A. Padilla (2009)
Physiol Genomics 36, 167-178
   Abstract »    Full Text »    PDF »
Regulation of EphB2 activation and cell repulsion by feedback control of the MAPK pathway.
A. Poliakov, M. L. Cotrina, A. Pasini, and D. G. Wilkinson (2008)
J. Cell Biol. 183, 933-947
   Abstract »    Full Text »    PDF »
Studying gene function in Caenorhabditis elegans using RNA-mediated interference.
E. M. Maine (2008)
Briefings in Functional Genomics 7, 184-194
   Abstract »    Full Text »    PDF »
The Mood Stabilizer Valproate Inhibits both Inositol- and Diacylglycerol-signaling Pathways in Caenorhabditis elegans.
S. M. Tokuoka, A. Saiardi, and S. J. Nurrish (2008)
Mol. Biol. Cell 19, 2241-2250
   Abstract »    Full Text »    PDF »
Eph, a Protein Family Coming of Age: More Confusion, Insight, or Complexity?.
M. Lackmann and A. W. Boyd (2008)
Science Signaling 1, re2
   Abstract »    Full Text »    PDF »
Eph/ephrin signaling: networks.
D. Arvanitis and A. Davy (2008)
Genes & Dev. 22, 416-429
   Abstract »    Full Text »    PDF »
Acrylamide-Responsive Genes in the Nematode Caenorhabditis elegans.
K. Hasegawa, S. Miwa, K. Isomura, K. Tsutsumiuchi, H. Taniguchi, and J. Miwa (2008)
Toxicol. Sci. 101, 215-225
   Abstract »    Full Text »    PDF »
Multiple Functions and Dynamic Activation of MPK-1 Extracellular Signal-Regulated Kinase Signaling in Caenorhabditis elegans Germline Development.
M.-H. Lee, M. Ohmachi, S. Arur, S. Nayak, R. Francis, D. Church, E. Lambie, and T. Schedl (2007)
Genetics 177, 2039-2062
   Abstract »    Full Text »    PDF »
Ephrin-Eph signalling drives the asymmetric division of notochord/neural precursors in Ciona embryos.
V. Picco, C. Hudson, and H. Yasuo (2007)
Development 134, 1491-1497
   Abstract »    Full Text »    PDF »
Proteasomal Ubiquitin Receptor RPN-10 Controls Sex Determination in Caenorhabditis elegans.
M. Shimada, K. Kanematsu, K. Tanaka, H. Yokosawa, and H. Kawahara (2006)
Mol. Biol. Cell 17, 5356-5371
   Abstract »    Full Text »    PDF »
A Genomewide Screen for Suppressors of par-2 Uncovers Potential Regulators of PAR Protein-Dependent Cell Polarity in Caenorhabditis elegans.
J.-C. Labbe, A. Pacquelet, T. Marty, and M. Gotta (2006)
Genetics 174, 285-295
   Abstract »    Full Text »    PDF »
Genetic redundancy masks diverse functions of the tumor suppressor gene PTEN during C. elegans development..
Y. Suzuki and M. Han (2006)
Genes & Dev. 20, 423-428
   Abstract »    Full Text »    PDF »
The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation.
A. E. Burrows, B. K. Sceurman, M. E. Kosinski, C. T. Richie, P. L. Sadler, J. M. Schumacher, and A. Golden (2006)
Development 133, 697-709
   Abstract »    Full Text »    PDF »
Eph and NMDA receptors control Ca2+/calmodulin-dependent protein kinase II activation during C. elegans oocyte meiotic maturation.
C. Corrigan, R. Subramanian, and M. A. Miller (2005)
Development 132, 5225-5237
   Abstract »    Full Text »    PDF »
Analysis of the Female Gametophyte Transcriptome of Arabidopsis by Comparative Expression Profiling.
H.-J. Yu, P. Hogan, and V. Sundaresan (2005)
Plant Physiology 139, 1853-1869
   Abstract »    Full Text »    PDF »
C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes.
M. Kosinski, K. McDonald, J. Schwartz, I. Yamamoto, and D. Greenstein (2005)
Development 132, 3357-3369
   Abstract »    Full Text »    PDF »
The Caenorhabditis elegans spe-38 gene encodes a novel four-pass integral membrane protein required for sperm function at fertilization.
I. Chatterjee, A. Richmond, E. Putiri, D. C. Shakes, and A. Singson (2005)
Development 132, 2795-2808
   Abstract »    Full Text »    PDF »
Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis.
J. Holmberg, A. Armulik, K.-A. Senti, K. Edoff, K. Spalding, S. Momma, R. Cassidy, J. G. Flanagan, and J. Frisen (2005)
Genes & Dev. 19, 462-471
   Abstract »    Full Text »    PDF »
PAR-3 is required for epithelial cell polarity in the distal spermatheca of C. elegans.
S. Aono, R. Legouis, W. A. Hoose, and K. J. Kemphues (2004)
Development 131, 2865-2874
   Abstract »    Full Text »    PDF »
Tropomyosin and Troponin Are Required for Ovarian Contraction in the Caenorhabditis elegans Reproductive System.
K. Ono and S. Ono (2004)
Mol. Biol. Cell 15, 2782-2793
   Abstract »    Full Text »    PDF »
Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans.
V. Reinke, I. S. Gil, S. Ward, and K. Kazmer (2004)
Development 131, 311-323
   Abstract »    Full Text »    PDF »
Talin loss-of-function uncovers roles in cell contractility and migration in C. elegans.
E. J. Cram, S. G. Clark, and J. E. Schwarzbauer (2003)
J. Cell Sci. 116, 3871-3878
   Abstract »    Full Text »    PDF »
Multiple roles of ephrins in morphogenesis, neuronal networking, and brain function.
A. Palmer and R. Klein (2003)
Genes & Dev. 17, 1429-1450
   Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882