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Endocrinology Vol. 140, No. 6 2685-2695
Copyright © 1999 by The Endocrine Society

ARTICLES

Anovulation in Cyclooxygenase-2-Deficient Mice Is Restored by Prostaglandin E2 and Interleukin-1ß1

Barbara J. Davis, David E. Lennard, Christopher A. Lee, Howard F. Tiano, Scott G. Morham, William C. Wetsel and Robert Langenbach

Laboratory of Experimental Pathology (B.J.D., D.E.L.) and Laboratory of Environmental Carcinogenesis/Mutagenesis (C.A.L., H.F.T., R.L.), National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709; Myriad Genetics, Inc. (S.G.M.), Salt Lake City, Utah 84108; and the Department of Psychiatry and Behavioral Sciences, Duke University Medical Center (W.C.W.), Durham, North Carolina 27710

Address all correspondence and requests for reprints to: Dr. Barbara J. Davis, Laboratory of Experimental Pathology, National Institute of Environmental Health Sciences, Box 12233, Research Triangle Park, North Carolina 27709. E-mail: davis1{at}niehs.nih.gov

Mice carrying a null mutation for either of the two cyclooxygenase (COX) isoenzymes, necessary for prostanoid production, exhibit several isotype-specific reproductive abnormalities. Mice deficient in COX-1 are fertile but have decreased pup viability, whereas mice deficient in COX-2 fail to ovulate and have abnormal implantation and decidualization responses. The present study identifies the specific contribution of each COX isoenzyme in hypothalamic, pituitary, and ovarian function and establishes the pathology and rescue of the anovulatory syndrome in the COX-2-deficient mouse. In both COX-1- and COX-2-deficient mice, pituitary gonadotropins were selectively increased, whereas hypothalamic LHRH and serum gonadotropin levels were similar to those in wild-type animals (+/+). No significant differences in serum estrogen or progesterone were noted among the three genotypes. Exogenous gonadotropin stimulation with PMSG and hCG produced a comparable 4-fold increase in ovarian PGE2 levels in wild-type and COX-1-/- mice. COX-2-/- mice had no increase in PGE2 over PMSG-stimulated levels. Wild-type and COX-1-/- mice ovulated in response to PMSG/hCG; very few COX-2-/- animals responded to this regimen. The defect in ovulation in COX-2 mutants was attributed to both an abnormal cumulus oophorum expansion and subsequent stigmata formation. Gonadotropin stimulation and concurrent treatment with PGE2 or interleukin-1ß resulted in ovulation of COX-2-/- mice comparable to that in COX-2+/+, whereas treatment with PGF2{alpha} was less effective. Collectively, these data demonstrate that COX-2, but not COX-1, is required for the gonadotropin induction of ovarian PG levels; that COX-2-related prostanoids are required for stabilization of the cumulus oophorum during ovulation; and that ovulation can be restored in the COX-2-/- animals by simultaneous treatment with gonadotropins and PGE2 or interleukin-1ß.




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T. Sakurai, K. Tamura, S. Okamoto, T. Hara, and H. Kogo
Possible Role of Cyclooxygenase II in the Acquisition of Ovarian Luteal Function in Rodents
Biol Reprod, September 1, 2003; 69(3): 835 - 842.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
T. E. Curry Jr. and K. G. Osteen
The Matrix Metalloproteinase System: Changes, Regulation, and Impact throughout the Ovarian and Uterine Reproductive Cycle
Endocr. Rev., August 1, 2003; 24(4): 428 - 465.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
F. Gaytan, C. Bellido, M. Gaytan, C. Morales, and J. E. Sanchez-Criado
Differential Effects of RU486 and Indomethacin on Follicle Rupture During the Ovulatory Process in the Rat
Biol Reprod, July 1, 2003; 69(1): 99 - 105.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
J.-Y. Park, F. Richard, S.-Y. Chun, J.-H. Park, E. Law, K. Horner, S-L C. Jin, and M. Conti
Phosphodiesterase Regulation Is Critical for the Differentiation and Pattern of Gene Expression in Granulosa Cells of the Ovarian Follicle
Mol. Endocrinol., June 1, 2003; 17(6): 1117 - 1130.
[Abstract] [Full Text] [PDF]

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 Ann Rheum DisHome page
J Martel-Pelletier, D Lajeunesse, P Reboul, and J-P Pelletier
Therapeutic role of dual inhibitors of 5-LOX and COX, selective and non-selective non-steroidal anti-inflammatory drugs
Ann Rheum Dis, June 1, 2003; 62(6): 501 - 509.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
C. M. Milner and A. J. Day
TSG-6: a multifunctional protein associated with inflammation
J. Cell Sci., May 15, 2003; 116(10): 1863 - 1873.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
S. A. Ochsner, D. L. Russell, A. J. Day, R. M. Breyer, and J. S. Richards
Decreased Expression of Tumor Necrosis Factor-{alpha}-Stimulated Gene 6 in Cumulus Cells of the Cyclooxygenase-2 and EP2 Null Mice
Endocrinology, March 1, 2003; 144(3): 1008 - 1019.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
D. L. Russell, S. A. Ochsner, M. Hsieh, S. Mulders, and J. S. Richards
Hormone-Regulated Expression and Localization of Versican in the Rodent Ovary
Endocrinology, March 1, 2003; 144(3): 1020 - 1031.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
E. Segi, K. Haraguchi, Y. Sugimoto, M. Tsuji, H. Tsunekawa, S. Tamba, K. Tsuboi, S. Tanaka, and A. Ichikawa
Expression of Messenger RNA for Prostaglandin E Receptor Subtypes EP4/EP2 and Cyclooxygenase Isozymes in Mouse Periovulatory Follicles and Oviducts During Superovulation
Biol Reprod, March 1, 2003; 68(3): 804 - 811.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
J.-G. Cheng and C. L. Stewart
Loss of Cyclooxygenase-2 Retards Decidual Growth but Does Not Inhibit Embryo Implantation or Development to Term
Biol Reprod, February 1, 2003; 68(2): 401 - 404.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
L. L. Espey and J. S. Richards
Temporal and Spatial Patterns of Ovarian Gene Transcription Following an Ovulatory Dose of Gonadotropin in the Rat
Biol Reprod, December 1, 2002; 67(6): 1662 - 1670.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
D. M. Duffy and R. L. Stouffer
Follicular administration of a cyclooxygenase inhibitor can prevent oocyte release without alteration of normal luteal function in rhesus monkeys
Hum. Reprod., November 1, 2002; 17(11): 2825 - 2831.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
F. Gaytan, E. Tarradas, C. Bellido, C. Morales, and J. E. Sanchez-Criado
Prostaglandin E1 Inhibits Abnormal Follicle Rupture and Restores Ovulation in Indomethacin-Treated Rats
Biol Reprod, October 1, 2002; 67(4): 1140 - 1147.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
L. Koumas and R. P. Phipps
Differential COX localization and PG release in Thy-1+ and Thy-1- human female reproductive tract fibroblasts
Am J Physiol Cell Physiol, August 1, 2002; 283(2): C599 - C608.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
S. Varani, J. A. Elvin, C. Yan, J. DeMayo, F. J. DeMayo, H. F. Horton, M. C. Byrne, and M. M. Matzuk
Knockout of Pentraxin 3, a Downstream Target of Growth Differentiation Factor-9, Causes Female Subfertility
Mol. Endocrinol., June 1, 2002; 16(6): 1154 - 1167.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
Y.-L. Wu and M. C. Wiltbank
Transcriptional Regulation of the Cyclooxygenase-2 Gene Changes from Protein Kinase (PK) A- to PKC-Dependence after Luteinization of Granulosa Cells
Biol Reprod, May 1, 2002; 66(5): 1505 - 1514.
[Abstract] [Full Text]

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 J. Physiol.Home page
C. G Egan, J. C Lockhart, W. R Ferrell, S. M Day, and J. S McLean
Pathophysiological basis of acute inflammatory hyperaemia in the rat knee: roles of cyclo-oxygenase-1 and -2
J. Physiol., March 1, 2002; 539(2): 579 - 587.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
B. Hinz and K. Brune
Cyclooxygenase-2---10 Years Later
J. Pharmacol. Exp. Ther., February 1, 2002; 300(2): 367 - 375.
[Abstract] [Full Text] [PDF]

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 Recent Prog Horm ResHome page
J. S. Richards, D. L. Russell, S. Ochsner, M. Hsieh, K. H. Doyle, A. E. Falender, Y. K. Lo, and S. C. Sharma
Novel Signaling Pathways That Control Ovarian Follicular Development, Ovulation, and Luteinization
Recent Prog. Horm. Res., January 1, 2002; 57(1): 195 - 220.
[Abstract] [Full Text] [PDF]

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 Mol Hum ReprodHome page
D. M. Duffy and R. L. Stouffer
The ovulatory gonadotrophin surge stimulates cyclooxygenase expression and prostaglandin production by the monkey follicle
Mol. Hum. Reprod., August 1, 2001; 7(8): 731 - 739.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
I. M. Joyce, F. L. Pendola, M. O'Brien, and J. J. Eppig
Regulation of Prostaglandin-Endoperoxide Synthase 2 Messenger Ribonucleic Acid Expression in Mouse Granulosa Cells during Ovulation
Endocrinology, July 1, 2001; 142(7): 3187 - 3197.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. Reese, X. Zhao, W.-G. Ma, N. Brown, T. J. Maziasz, and S. K. Dey
Comparative Analysis of Pharmacologic and/or Genetic Disruption of Cyclooxygenase-1 and Cyclooxygenase-2 Function in Female Reproduction in Mice
Endocrinology, July 1, 2001; 142(7): 3198 - 3206.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
M. D. Calder, A. N. Caveney, M. E. Westhusin, and A. J. Watson
Cyclooxygenase-2 and Prostaglandin E2(PGE2) Receptor Messenger RNAs Are Affected by Bovine Oocyte Maturation Time and Cumulus-Oocyte Complex Quality, and PGE2 Induces Moderate Expansion of the Bovine Cumulus In Vitro
Biol Reprod, July 1, 2001; 65(1): 135 - 140.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. S. Richards
Perspective: The Ovarian Follicle--A Perspective in 2001
Endocrinology, June 1, 2001; 142(6): 2184 - 2193.
[Full Text] [PDF]

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 Biol. Reprod.Home page
H. Matsumoto, W.-g. Ma, W. Smalley, J. Trzaskos, R. M. Breyer, and S. K. Dey
Diversification of Cyclooxygenase-2-Derived Prostaglandins in Ovulation and Implantation
Biol Reprod, May 1, 2001; 64(5): 1557 - 1565.
[Abstract] [Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
C. D. Loftin, D. B. Trivedi, H. F. Tiano, J. A. Clark, C. A. Lee, J. A. Epstein, S. G. Morham, M. D. Breyer, M. Nguyen, B. M. Hawkins, et al.
Failure of ductus arteriosus closure and remodeling in neonatal mice deficient in cyclooxygenase-1 and cyclooxygenase-2
PNAS, January 23, 2001; (2001) 31573498.
[Abstract] [Full Text]

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 EndocrinologyHome page
G. A. Dissen, J. A. Parrott, M. K. Skinner, D. F. Hill, M. E. Costa, and S. R. Ojeda
Direct Effects of Nerve Growth Factor on Thecal Cells from Antral Ovarian Follicles
Endocrinology, December 1, 2000; 141(12): 4736 - 4750.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
A. Kirschenbaum, D. R. Liotta, S. Yao, X.-H. Liu, A. P. Klausner, P. Unger, E. Shapiro, I. Leav, and A. C. Levine
Immunohistochemical Localization of Cyclooxygenase-1 and Cyclooxygenase-2 in the Human Fetal and Adult Male Reproductive Tracts
J. Clin. Endocrinol. Metab., September 1, 2000; 85(9): 3436 - 3441.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
T.-L. Erkinheimo, K. Saukkonen, K. Narko, J. Jalkanen, O. Ylikorkala, and A. Ristimäki
Expression of Cyclooxygenase-2 and Prostanoid Receptors by Human Myometrium
J. Clin. Endocrinol. Metab., September 1, 2000; 85(9): 3468 - 3475.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
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.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
C. D. Loftin, D. B. Trivedi, H. F. Tiano, J. A. Clark, C. A. Lee, J. A. Epstein, S. G. Morham, M. D. Breyer, M. Nguyen, B. M. Hawkins, et al.
Failure of ductus arteriosus closure and remodeling in neonatal mice deficient in cyclooxygenase-1 and cyclooxygenase-2
PNAS, January 30, 2001; 98(3): 1059 - 1064.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
J. A. Elvin, C. Yan, and M. M. Matzuk
Growth differentiation factor-9 stimulates progesterone synthesis in granulosa cells via a prostaglandin E2/EP2 receptor pathway
PNAS, August 29, 2000; 97(18): 10288 - 10293.
[Abstract] [Full Text] [PDF]

Home page
 J. Physiol.Home page
C. G. Egan, J. C. Lockhart, W. R. Ferrell, S. M. Day, and J. S. McLean
Pathophysiological basis of acute inflammatory hyperaemia in the rat knee: roles of cyclo-oxygenase-1 and -2
J. Physiol., January 25, 2002; (2002) 200101347.
[Abstract] [PDF]


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