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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*,,
Charles D.
Rice,
Yefei
Pang*,
Margaret
Pace*, and
Peter
Thomas*,§
* Marine Science Institute, University of Texas at
Austin, 750 Channel View Drive, Port Aransas, TX
78373; Department of Biology, East
Carolina University, 1000 East Fifth Street, Greenville,
NC 27858; and 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 describethe cloning of a cDNA from spotted seatrout ovaries encoding aprotein that satisfies the following seven criteria for its designationas a steroid membrane receptor: plausible structure, tissue
specificity,cellular distribution, steroid binding, signal
transduction, hormonalregulation, and biological relevance. For
plausible structure,computer modeling predicts that the protein has
seven transmembranedomains, typical of G protein-coupled
receptors. The mRNA (4.0kb) is only detected in the brain and
reproductive tissues onNorthern blots. Antisera only detect the
protein (40 kDa) in plasmamembranes of reproductive tissues. The
recombinant protein producedin an Escherichia coli
expression system has a high affinity (Kd= 30 nM), saturable, displaceable, single binding site specificfor
progestins. Progestins alter signal transduction pathways,activating
mitogen-activated protein kinase and inhibiting adenylylcyclase, in a
transfected mammalian cell line. Inhibition of adenylylcyclase is
pertussis toxin sensitive, suggesting the receptormay be coupled to an
inhibitory G protein. Progestins and gonadotropinup-regulate both mRNA
and protein levels in seatrout ovaries.Changes in receptor abundance
in response to hormones and at variousstages of oocyte development,
its probable coupling to an inhibitoryG protein and inhibition of
progestin induction of oocyte maturationupon microinjection of
antisense oligonucleotides are consistentwith the identity of the
receptor as an intermediary in oocytematuration. These characteristics
suggest the fish protein isa membrane progestin receptor mediating a
"nonclassical" actionof progestins to induce oocyte maturation
infish.
§
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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