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PNAS 100 (5): 2231-2236

Copyright © 2003 by the National Academy of Sciences.

From the Cover
Biochemistry
Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes

Yong Zhu*,dagger , Charles D. RiceDagger , Yefei Pang*, Margaret Pace*, and Peter Thomas*,§

* Marine Science Institute, University of Texas at Austin, 750 Channel View Drive, Port Aransas, TX 78373; dagger  Department of Biology, East Carolina University, 1000 East Fifth Street, Greenville, NC 27858; and Dagger  Departments of Environmental Toxicology and Bioscience, Clemson University, 509 Westinghouse Road, Pendleton, SC 29670

Edited by Ronald W. Estabrook, University of Texas Southwestern Medical Center, Dallas, TX, and approved December 17, 2002 (received for review October 9, 2002)

The structures of membrane receptors mediating rapid, nongenomic actions of steroids have not been identified. We describe the cloning of a cDNA from spotted seatrout ovaries encoding a protein that satisfies the following seven criteria for its designation as a steroid membrane receptor: plausible structure, tissue specificity, cellular distribution, steroid binding, signal transduction, hormonal regulation, and biological relevance. For plausible structure, computer modeling predicts that the protein has seven transmembrane domains, typical of G protein-coupled receptors. The mRNA (4.0 kb) is only detected in the brain and reproductive tissues on Northern blots. Antisera only detect the protein (40 kDa) in plasma membranes of reproductive tissues. The recombinant protein produced in an Escherichia coli expression system has a high affinity (Kd = 30 nM), saturable, displaceable, single binding site specific for progestins. Progestins alter signal transduction pathways, activating mitogen-activated protein kinase and inhibiting adenylyl cyclase, in a transfected mammalian cell line. Inhibition of adenylyl cyclase is pertussis toxin sensitive, suggesting the receptor may be coupled to an inhibitory G protein. Progestins and gonadotropin up-regulate both mRNA and protein levels in seatrout ovaries. Changes in receptor abundance in response to hormones and at various stages of oocyte development, its probable coupling to an inhibitory G protein and inhibition of progestin induction of oocyte maturation upon microinjection of antisense oligonucleotides are consistent with the identity of the receptor as an intermediary in oocyte maturation. These characteristics suggest the fish protein is a membrane progestin receptor mediating a "nonclassical" action of progestins to induce oocyte maturation in fish.


§ To whom correspondence should be addressed. E-mail: thomas{at}utmsi.utexas.edu.

www.pnas.org/cgi/doi/10.1073/pnas.0336132100


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   Abstract »    Full Text »    PDF »
Diethylstilbestrol induces fish oocyte maturation.
T. Tokumoto, M. Tokumoto, R. Horiguchi, K. Ishikawa, and Y. Nagahama (2004)
PNAS 101, 3686-3690
   Abstract »    Full Text »    PDF »
Feedback Inhibition of Steroidogenic Acute Regulatory Protein Expression in Vitro and in Vivo by Androgens.
C. P. Houk, E. J. Pearson, N. Martinelle, P. K. Donahoe, and J. Teixeira (2004)
Endocrinology 145, 1269-1275
   Abstract »    Full Text »    PDF »
Brain masculinization requires androgen receptor function.
T. Sato, T. Matsumoto, H. Kawano, T. Watanabe, Y. Uematsu, K. Sekine, T. Fukuda, K.-i. Aihara, A. Krust, T. Yamada, et al. (2004)
PNAS 101, 1673-1678
   Abstract »    Full Text »    PDF »
Making Sense of Cross-Talk between Steroid Hormone Receptors and Intracellular Signaling Pathways: Who Will Have the Last Word?.
C. A. Lange (2004)
Mol. Endocrinol. 18, 269-278
   Abstract »    Full Text »    PDF »
Androgens Promote Maturation and Signaling in Mouse Oocytes Independent of Transcription: A Release of Inhibition Model for Mammalian Oocyte Meiosis.
A. Gill, M. Jamnongjit, and S. R. Hammes (2004)
Mol. Endocrinol. 18, 97-104
   Abstract »    Full Text »    PDF »
Nongenomic Inhibition of Oxytocin Binding by Progesterone in the Ovine Uterus.
K. A. Dunlap and F. Stormshak (2004)
Biol Reprod 70, 65-69
   Abstract »    Full Text »    PDF »
Proteins of Multiple Classes May Participate in Nongenomic Steroid Actions.
C. S. Watson and B. Gametchu (2003)
Experimental Biology and Medicine 228, 1272-1281
   Abstract »    Full Text »    PDF »
Rapid Signaling of Estrogen in Hypothalamic Neurons Involves a Novel G-Protein-Coupled Estrogen Receptor that Activates Protein Kinase C.
J. Qiu, M. A. Bosch, S. C. Tobias, D. K. Grandy, T. S. Scanlan, O. K. Ronnekleiv, and M. J. Kelly (2003)
J. Neurosci. 23, 9529-9540
   Abstract »    Full Text »    PDF »
Non-genomic actions of aldosterone: mechanisms and consequences in kidney cells.
B. Boldyreff and M. Wehling (2003)
Nephrol. Dial. Transplant. 18, 1693-1695
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Androgens and Cardiovascular Disease.
P. Y. Liu, A. K. Death, and D. J. Handelsman (2003)
Endocr. Rev. 24, 313-340
   Abstract »    Full Text »    PDF »
The further redefining of steroid-mediated signaling.
S. R. Hammes (2003)
PNAS 100, 2168-2170
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Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor.
Y. Zhu, J. Bond, and P. Thomas (2003)
PNAS 100, 2237-2242
   Abstract »    Full Text »    PDF »

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