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Endocrinology, Vol 135, 841-848, Copyright © 1994 by Endocrine Society

ARTICLES

Induction of prostaglandin endoperoxide synthase-2 by human chorionic gonadotropin in bovine preovulatory follicles in vivo

J Sirois
Department of Physiology, Cornell University College of Veterinary Medicine, Ithaca, New York 14853.

Gonadotropins have recently been shown to induce prostaglandin endoperoxide synthase-2 (PGHS-2) in rat preovulatory follicles before ovulation, but hormonal induction of this enzyme has not yet been reported in preovulatory follicles of any other species. To determine whether the selective induction of PGHS-2 by the ovulatory gonadotropin surge is a molecular process that has been conserved in other mammalian species with different reproductive cycles, the regulation of PGHS isoforms was studied in bovine preovulatory follicles isolated 0, 6, 12, 18, 20, 22, 24, and 26 h after an ovulatory dose of hCG. Each follicle was dissected into three preparations: the intact follicle wall (i.e. theca interna with attached granulosa cells), theca interna, and isolated granulosa cells. Solubilized cell extracts were obtained from each preparation and analyzed by Western blots, using polyclonal antibodies that selectively recognize PGHS-2 and PGHS-1 isoforms. RNA extracts were prepared and analyzed by Northern blots, using a mouse PGHS-2 complementary DNA. The results indicated that the expression of PGHS-2 messenger RNA (mRNA) and protein, but not that of PGHS-1, was regulated by hCG in bovine preovulatory follicles before ovulation. Levels of PGHS-2 protein (mol wt, 74,000) in the follicle wall were undetectable at 0, 6, and 12 h, but increased dramatically after 18 h to reach maximal levels 24 h post-hCG treatment. Northern blots revealed a similar temporal induction of PGHS-2 mRNA (4.0 kilobases). Analyses of isolated preparations of theca interna and granulosa cells clearly showed that PGHS-2 was expressed exclusively in granulosa cells and not in theca interna. Significant increases in follicular fluid concentrations of prostaglandins E2 and F were associated with the induction of follicular PGHS-2 protein and mRNA. Thus, this study establishes that the induction by gonadotropin of PGHS-2 in granulosa cells before ovulation appears to be a conserved mechanism by which the synthesis of prostaglandins necessary for the ovulation process is regulated in different species. However, the striking difference between the time course of PGHS-2 induction previously reported in rat follicles (4 h post-hCG treatment) and that observed in bovine follicles (18 h post-hCG treatment) suggests that the control of PGHS-2 expression could be one of the determinants involved in dictating the species-specific progression (length) of the ovulation process.


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J. H. Song, J. Sirois, A. Houde, and B. D. Murphy
Cloning, Developmental Expression, and Immunohistochemistry of Cyclooxygenase 2 in the Endometrium during Embryo Implantation and Gestation in the Mink (Mustela vison)
Endocrinology, August 1, 1998; 139(8): 3629 - 3636.
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 J. Pharmacol. Exp. Ther.Home page
D. M. Dirig, P. C. Isakson, and T. L. Yaksh
Effect of COX-1 and COX-2 Inhibition on Induction and Maintenance of Carrageenan-Evoked Thermal Hyperalgesia in Rats
J. Pharmacol. Exp. Ther., June 1, 1998; 285(3): 1031 - 1038.
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C. W. Xiao, J. M. Liu, J. Sirois, and A. K. Goff
Regulation of Cyclooxygenase-2 and Prostaglandin F Synthase Gene Expression by Steroid Hormones and Interferon-{tau} in Bovine Endometrial Cells
Endocrinology, May 1, 1998; 139(5): 2293 - 2299.
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M. Ando, S. Kol, E. Kokia, K. Ruutiainen-Altman, J. Sirois, R. M. Rohan, D. W. Payne, and E. Y. Adashi
Rat Ovarian Prostaglandin Endoperoxide Synthase-1 and -2: Periovulatory Expression of Granulosa Cell-Based Interleukin-1-Dependent Enzymes
Endocrinology, May 1, 1998; 139(5): 2501 - 2508.
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D. Boerboom and J. Sirois
Molecular Characterization of Equine Prostaglandin G/H Synthase-2 and Regulation of Its Messenger Ribonucleic Acid in Preovulatory Follicles
Endocrinology, April 1, 1998; 139(4): 1662 - 1670.
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 J. Clin. Endocrinol. Metab.Home page
J.-C. Huang, D.-Y. Liu, S. Yadollahi, K. K. Wu, and M. Y. Dawood
Interleukin-1{beta} Induces Cyclooxygenase-2 Gene Expression in Cultured Endometrial Stromal Cells
J. Clin. Endocrinol. Metab., February 1, 1998; 83(2): 538 - 541.
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 J. Histochem. Cytochem.Home page
M. Dore, L. C. Cote, A. Mitchell, and J. Sirois
Expression of Prostaglandin G/H Synthase Type 1, but not Type 2, in Human Ovarian Adenocarcinomas
J. Histochem. Cytochem., January 1, 1998; 46(1): 77 - 84.
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M. Shemesh, M. Gurevich, D. Mizrachi, L. Dombrovski, Y. Stram, M. J. Fields, and L. S. Shore
Expression of Functional Luteinizing Hormone (LH) Receptor and Its Messenger Ribonucleic Acid in Bovine Uterine Veins: LH Induction of Cyclooxygenase and Augmentation of Prostaglandin Production in Bovine Uterine Veins
Endocrinology, November 1, 1997; 138(11): 4844 - 4851.
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J. S. Richards
Editorial: Sounding the Alarm--Does Induction of Prostaglandin Endoperoxide Synthase-2 Control the Mammalian Ovulatory Clock?
Endocrinology, October 1, 1997; 138(10): 4047 - 4048.
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J. Sirois and M. Dore
The Late Induction of Prostaglandin G/H Synthase-2 in Equine Preovulatory Follicles Supports Its Role as a Determinant of the Ovulatory Process
Endocrinology, October 1, 1997; 138(10): 4427 - 4434.
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K. Narko, O. Ritvos, and A. Ristimaki
Induction of Cyclooxygenase-2 and Prostaglandin F2{alpha} Receptor Expression by Interleukin-1{beta} in Cultured Human Granulosa-Luteal Cells
Endocrinology, September 1, 1997; 138(9): 3638 - 3644.
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W. X. Wu, X. H. Ma, Q. Zhang, L. Buchwalder, and P. W. Nathanielsz
Regulation of Prostaglandin Endoperoxide H Synthase 1 and 2 by Estradiol and Progesterone in Nonpregnant Ovine Myometrium and Endometrium in Vivo
Endocrinology, September 1, 1997; 138(9): 4005 - 4012.
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G. Charpigny, P. Reinaud, J.-P. Tamby, C. Creminon, J. Martal, J. Maclouf, and M. Guillomot
Expression of Cyclooxygenase-1 and -2 in Ovine Endometrium During the Estrous Cycle and Early Pregnancy
Endocrinology, May 1, 1997; 138(5): 2163 - 2171.
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 J. Biol. Chem.Home page
J. K. Morris and J. S. Richards
An E-box Region within the Prostaglandin Endoperoxide Synthase-2 (PGS-2) Promoter Is Required for Transcription in Rat Ovarian Granulosa Cells
J. Biol. Chem., July 12, 1996; 271(28): 16633 - 16643.
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F. Filion, N. Bouchard, A. K. Goff, J. G. Lussier, and J. Sirois
Molecular Cloning and Induction of Bovine Prostaglandin E Synthase by Gonadotropins in Ovarian Follicles Prior to Ovulation in Vivo
J. Biol. Chem., August 31, 2001; 276(36): 34323 - 34330.
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