QUICK SEARCH:   [advanced] Author: Keyword(s):
Home     Help     Feedback     Subscriptions     Archive     Search     Table of Contents

First published online June 5, 2009
doi: 10.1242/10.1242/dev.034595

This Article Figures Only Full Text Full Text (PDF) Supplementary Material Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Related articles in Development Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Google Scholar Articles by Govindan, J. A. Articles by Greenstein, D. PubMed Articles by Govindan, J. A. Articles by Greenstein, D. Social Bookmarking                         What's this?

Somatic cAMP signaling regulates MSP-dependent oocyte growth and meiotic maturation in C. elegans

J. Amaranath Govindan^*, Saravanapriah Nadarajan^*, Seongseop Kim, Todd A. Starich and David Greenstein

Department of Genetics, Cell Biology and Development, University of Minnesota, 6-160 Jackson Hall, 321 Church Street SE, Minneapolis, MN 55455, USA.

Author for correspondence (e-mail: green959{at}umn.edu)

Accepted 22 April 2009

Soma-germline interactions control fertility at many levels, including stem cell proliferation, meiosis and gametogenesis, yet the nature of these fundamental signaling mechanisms and their potential evolutionary conservation are incompletely understood. In C. elegans, a sperm-sensing mechanism regulates oocyte meiotic maturation and ovulation, tightly coordinating sperm availability and fertilization. Sperm release the major sperm protein (MSP) signal to trigger meiotic resumption (meiotic maturation) and to promote contraction of the follicle-like gonadal sheath cells that surround oocytes. Using genetic mosaic analysis, we show that all known MSP-dependent meiotic maturation events in the germline require G_s-adenylate cyclase signaling in the gonadal sheath cells. We show that the MSP hormone promotes the sustained actomyosin-dependent cytoplasmic streaming that drives oocyte growth. Furthermore, we demonstrate that efficient oocyte production and cytoplasmic streaming require G_s-adenylate cyclase signaling in the gonadal sheath cells, thereby providing a somatic mechanism that coordinates oocyte growth and meiotic maturation with sperm availability. We present genetic evidence that MSP and G_s-adenylate cyclase signaling regulate oocyte growth and meiotic maturation in part by antagonizing gap-junctional communication between sheath cells and oocytes. In the absence of MSP or G_s-adenylate cyclase signaling, MSP binding sites are enriched and appear clustered on sheath cells. We discuss these results in the context of a model in which the sheath cells function as the major initial sensor of MSP, potentially via multiple classes of G-protein-coupled receptors. Our findings highlight a remarkable similarity between the regulation of meiotic resumption by soma-germline interactions in C. elegans and mammals.

Key words: MSP signaling, Meiosis, Meiotic maturation, Adenylate cyclase signaling, Oogenesis, Cytoplasmic streaming, Caenorhabditis elegans

CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

Related articles in Development:

Opposing signalling centres balance oocyte growth

Development 2009 136: e1304. [Full Text]  

This article has been cited by other articles:

				S. Nadarajan, J. A. Govindan, M. McGovern, E. J. A. Hubbard, and D. Greenstein MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth in C. elegans Development, July 1, 2009; 136(13): 2223 - 2234. [Abstract] [Full Text] [PDF]