Prostaglandin biosynthesis, transport, and signaling in corpus luteum: a basis for autoregulation of luteal function.

The corpus luteum (CL) is a transient ovarian endocrine gland formed from the ovulated follicle. Progesterone is the primary secretory product of CL and is essential for establishment of pregnancy in mammals. In the cyclic female, the life span of CL is characterized by luteal development, maintenance, and regression regulated by complex interactions between luteotrophic and luteolytic mediators. It is universally accepted that prostaglandin (PG) F(2a) is the luteolysin whereas PGE(2) is considered as a luteotropin in most mammals. New emerging concepts emphasize the autocrine and paracrine actions of luteal PGs in CL function. However, there is no report on selective biosynthesis and cellular transport of luteal PGE(2) and PGF(2alpha) in the CL of any species. We have studied the expression of enzymes involved in the metabolism of PGE(2) and PGF(2alpha), cyclooxygenase (COX)-1 and -2, PGE and F synthases, PG 15-dehydrogenase, and PG transporter as well as receptors (EP2, EP3, and FP) throughout the CL life span using a bovine model. COX-1, PGF synthase, and PG 15-dehydrogenase are expressed at constant levels whereas COX-2, PGE synthase, PG transporter, EP2, EP3, and FP are highly modulated during different phases of the CL life span. The PG components are preferentially expressed in large luteal cells. The results indicate that PGE(2) biosynthesis, transport, and signaling cascades are selectively activated during luteal maintenance. By contrast the PGF(2alpha) system is activated during luteal regression. Collectively, our results suggest an integrated role for luteal PGE(2) and PGF(2alpha) in autoregulation of CL function.

[1]  S. Banu,et al.  Temporal and tissue-specific expression of prostaglandin receptors EP2, EP3, EP4, FP, and cyclooxygenases 1 and 2 in uterus and fetal membranes during bovine pregnancy. , 2004, Endocrinology.

[2]  S. Banu,et al.  Molecular cloning and spatio-temporal expression of the prostaglandin transporter: A basis for the action of prostaglandins in the bovine reproductive system , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[3]  S. Banu,et al.  Molecular cloning and characterization of bovine prostaglandin E2 receptors EP2 and EP4: expression and regulation in endometrium and myometrium during the estrous cycle and early pregnancy. , 2003, Endocrinology.

[4]  Ralf Morgenstern,et al.  Human Microsomal Prostaglandin E Synthase-1 , 2003, Journal of Biological Chemistry.

[5]  J. Regan,et al.  Prostaglandin F2α stimulation of cyclooxygenase-2 promoter activity by the FPB prostanoid receptor , 2003 .

[6]  J. A. Arosh,et al.  An Aldose Reductase with 20α-Hydroxysteroid Dehydrogenase Activity Is Most Likely the Enzyme Responsible for the Production of Prostaglandin F2α in the Bovine Endometrium* , 2003, The Journal of Biological Chemistry.

[7]  J. Kotwica,et al.  Role of prostaglandin E2 in basal and noradrenaline-induced progesterone secretion by the bovine corpus luteum. , 2003, Prostaglandins & other lipid mediators.

[8]  B. Berisha,et al.  Changes in prostaglandin secretion by the regressing bovine corpus luteum. , 2003, Prostaglandins & other lipid mediators.

[9]  J. Regan,et al.  Prostaglandin F(2alpha) stimulation of cyclooxygenase-2 promoter activity by the FP(B) prostanoid receptor. , 2003, European journal of pharmacology.

[10]  B. Rueda,et al.  The corpus luteum: an ovarian structure with maternal instincts and suicidal tendencies. , 2002, Frontiers in bioscience : a journal and virtual library.

[11]  P. Bridges,et al.  Effect of mifepristone on pregnancy, pregnancy-specific protein B (PSPB), progesterone, estradiol-17β, prostaglandin F2α (PGF2α) and prostaglandin E (PGE) in ovariectomized 90-day pregnant ewes , 2002 .

[12]  I. Song,et al.  The enzymology of prostaglandin endoperoxide H synthases-1 and -2. , 2002, Prostaglandins & other lipid mediators.

[13]  H. Tai,et al.  Prostaglandin catabolizing enzymes. , 2002, Prostaglandins & other lipid mediators.

[14]  J. A. Arosh,et al.  Expression of Cyclooxygenases 1 and 2 and Prostaglandin E Synthase in Bovine Endometrial Tissue During the Estrous Cycle1 , 2002, Biology of reproduction.

[15]  Y. Sugimoto,et al.  Prostaglandin receptors: advances in the study of EP3 receptor signaling. , 2002, Journal of biochemistry.

[16]  S. Tsai,et al.  Regulation of progesterone and prostaglandin F2α production in the CL , 2002, Molecular and Cellular Endocrinology.

[17]  G. Niswender Molecular control of luteal secretion of progesterone. , 2002, Reproduction.

[18]  K. Sakamoto,et al.  Cloning and Characterization of the Novel Isoforms for PGF 2α Receptor in the Bovine Corpus Luteum , 2002 .

[19]  P. Bridges,et al.  Effect of mifepristone on pregnancy, pregnancy-specific protein B (PSPB), progesterone, estradiol-17beta, prostaglandin F2alpha (PGF2alpha) and prostaglandin E (PGE) in ovariectomized 90-day pregnant ewes. , 2002, Prostaglandins & other lipid mediators.

[20]  S. Tsai,et al.  Regulation of progesterone and prostaglandin F2alpha production in the CL. , 2002, Molecular and cellular endocrinology.

[21]  V. Schuster Prostaglandin transport. , 2002, Prostaglandins & other lipid mediators.

[22]  R. Anderson,et al.  Expression of COX-2 and PGE synthase and synthesis of PGE2 in endometrial adenocarcinoma: a possible autocrine/paracrine regulation of neoplastic cell function via EP2/EP4 receptors , 2001, British Journal of Cancer.

[23]  J. Lussier,et al.  Molecular Cloning and Induction of Bovine Prostaglandin E Synthase by Gonadotropins in Ovarian Follicles Prior to Ovulationin Vivo * , 2001, The Journal of Biological Chemistry.

[24]  R. Millar,et al.  Cyclooxygenase-2 expression and prostaglandin E(2) synthesis are up-regulated in carcinomas of the cervix: a possible autocrine/paracrine regulation of neoplastic cell function via EP2/EP4 receptors. , 2001, The Journal of clinical endocrinology and metabolism.

[25]  S. Tsai,et al.  Prostaglandin F2α Receptor in the Corpus Luteum: Recent Information on the Gene, Messenger Ribonucleic Acid, and Protein1 , 2001, Biology of reproduction.

[26]  P. Bridges,et al.  Effects of indomethacin, luteinizing hormone (LH), prostaglandin E2 (PGE2), trilostane, mifepristone, ethamoxytriphetol (MER-25) on secretion of prostaglandin E (PGE), prostaglandin F2alpha (PGF2alpha) and progesterone by ovine corpora lutea of pregnancy or the estrous cycle. , 2001, Prostaglandins & other lipid mediators.

[27]  M. Zerani,et al.  Prostaglandin receptors and role of G protein-activated pathways on corpora lutea of pseudopregnant rabbit in vitro. , 2001, The Journal of endocrinology.

[28]  J. Lussier,et al.  Molecular cloning and induction of bovine prostaglandin E synthase by gonadotropins in ovarian follicles prior to ovulation in vivo. , 2001, The Journal of biological chemistry.

[29]  L. Lau,et al.  Prostaglandin F2α-induced Expression of 20α-Hydroxysteroid Dehydrogenase Involves the Transcription Factor NUR77* , 2000, The Journal of Biological Chemistry.

[30]  J. Juengel,et al.  Prostaglandin Metabolism in the Ovine Corpus Luteum: Catabolism of Prostaglandin F2α (PGF2α) Coincides with Resistance of the Corpus Luteum to PGF2α1 , 2000 .

[31]  J. Juengel,et al.  Mechanisms controlling the function and life span of the corpus luteum. , 2000, Physiological reviews.

[32]  L. Lau,et al.  Prostaglandin F2alpha-induced expression of 20alpha-hydroxysteroid dehydrogenase involves the transcription factor NUR77. , 2000, The Journal of biological chemistry.

[33]  C. Stocco,et al.  Progesterone receptor is not required for progesterone action in the rat corpus luteum of pregnancy☆ , 1999, Steroids.

[34]  R. Randel,et al.  PGE2 induces its own secretion in vitro by bovine 270-day placenta but not by 200-day placenta. , 1999, Prostaglandins & other lipid mediators.

[35]  J. McCRACKEN,et al.  Luteolysis: a neuroendocrine-mediated event. , 1999, Physiological reviews.

[36]  S. Narumiya,et al.  Prostanoid receptors: structures, properties, and functions. , 1999, Physiological reviews.

[37]  M. Wiltbank,et al.  Regulation of prostaglandin F2α and E receptor mRNA by prostaglandin F2α in ovine corpora lutea , 1998 .

[38]  S. Tsai,et al.  Prostaglandin F2alpha regulates distinct physiological changes in early and mid-cycle bovine corpora lutea. , 1998, Biology of reproduction.

[39]  V. Schuster,et al.  Molecular mechanisms of prostaglandin transport. , 1998, Annual review of physiology.

[40]  S. Tsai,et al.  Prostaglandin F2alpha induces expression of prostaglandin G/H synthase-2 in the ovine corpus luteum: a potential positive feedback loop during luteolysis. , 1997, Biology of reproduction.

[41]  P. Bridges,et al.  PGE1 or PGE2 not LH regulates secretion of progesterone in vitro by the 88-90 day ovine corpus luteum of pregnancy. , 1997, Prostaglandins.

[42]  W. Hansel,et al.  The bovine corupus lutem preface , 1996 .

[43]  R. D. Del Vecchio,et al.  Bovine luteal cell production in vitro of prostaglandin E2, oxytocin and progesterone in response to pregnancy-specific protein B and prostaglandin F2 alpha. , 1996, Journal of reproduction and fertility.

[44]  D. Dewitt,et al.  Prostaglandin endoperoxide H synthases-1 and -2. , 1996, Advances in immunology.

[45]  W. Hansel,et al.  The bovine corpus luteum. , 1996, Theriogenology.

[46]  W. Schlegel,et al.  Prostaglandin-E2 9-reductase from corpus luteum of pseudopregnant rabbit is a member of the aldo-keto reductase superfamily featuring 20 alpha-hydroxysteroid dehydrogenase activity. , 1995, European journal of biochemistry.

[47]  O. J. Ginther,et al.  Prostaglandin F2 alpha receptors in the early bovine corpus luteum. , 1995, Biology of reproduction.

[48]  P. Leung,et al.  Auto/paracrine role of prostaglandins in corpus luteum function , 1994, Molecular and Cellular Endocrinology.

[49]  G. Niswender,et al.  Receptors for prostaglandins F2 alpha and E2 in ovine corpora lutea during maternal recognition of pregnancy. , 1992, Biology of reproduction.

[50]  L. Hamberger,et al.  Luteotropic effects of prostaglandin E2 on the human corpus luteum of the menstrual cycle and early pregnancy. , 1988, The Journal of clinical endocrinology and metabolism.

[51]  W. Walters,et al.  Human luteal tissue prostaglandins, 17β-estradiol, and progesterone in relation to the growth and senescence of the corpus luteum**Supported by the National Health and Medical Research Council of Australia and by a grant-in-aid from the Clive and Vera Ramaciotti Foundations. , 1983 .

[52]  W. Walters,et al.  Human luteal tissue prostaglandins, 17 beta-estradiol, and progesterone in relation to the growth and senescence of the corpus luteum. , 1983, Fertility and sterility.

[53]  R. Magness,et al.  Effect of PGE1 or PGE2 on PGF2α-induced luteolysis in nonbred ewes , 1981 .

[54]  R. Magness,et al.  Effect of chronic ipsilateral or contralateral intrauterine infusion of prostaglandin E2 (PGE2) on luteal function of unilaterally ovariectomized ewes. , 1981, Prostaglandins and medicine.

[55]  R. Magness,et al.  Effect of chronic ipsilateral or contralateral intrauterine infusion of prostaglandin E1 (PGE1) on luteal function of unilaterally ovariectomized ewes. , 1981, Prostaglandins.

[56]  E. Inskeep,et al.  Antiluteolytic effect of the conceptus and of PGE2 in ewes. , 1977, Journal of animal science.

[57]  R. Scaramuzzi,et al.  Simultaneous infusion of prostaglandin E2 antagonizes the luteolytic action of prostaglandin F2alpha in vivo. , 1977, The Journal of endocrinology.

[58]  J. M. Marsh,et al.  Cyclic AMP accumulation and steroidogenesis in the human corpus luteum: effect of gonadotropins and prostaglandins. , 1974, The Journal of clinical endocrinology and metabolism.