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DOI: 10.1055/s-2005-861022
Oxytocin-induced Prostaglandin E2 (PGE2) Synthesis is Regulated by Progesterone via Oxytocinase in Ishikawa Cells
Publication History
Received 17 February 2004
Accepted after Revision 20 July 2004
Publication Date:
09 February 2005 (online)
Abstract
Cell-surface oxytocinase inactivates oxytocin and regulates oxytocin stimulation. We reported that oxytocinase in human endometrial epithelial cells was secreted from the cell membrane in the mid-secretory phase and disappeared from the cell surface. On the other hand, the production in human endometrium of prostaglandins, which play important roles in the reproductive process, has been reported to be upregulated by oxytocin. We investigated whether progesterone affects cell-surface oxytocinase and oxytocin-induced prostaglandin E2 (PGE2) production in vitro. Progesterone induced secretion of oxytocinase into the culture medium, which resulted in a decrease in cell-surface oxytocinase. Production of PGE2 was increased slightly by oxytocin without progesterone, and significantly with progesterone. The inhibition of oxytocinase activity by amastatin had a similar effect to the loss of cell-surface oxytocinase caused by progesterone. It is therefore likely that the cell-surface oxytocinase of endometrial epithelial cells modified by progesterone plays an important role in the function of the human endometrium through PGE2.
Key words
Oxytocinase - Progesterone - Prostaglandins - PGE2 - Oxytocin - Endometrium
References
- 1 Poyser N L. The control of prostaglandin production by the endometrium in relation to luteolysis and menstruation. Prostaglandins Leukot Essent Fatty Acids. 1995; 53 147-195
- 2 Song H, Lim H, Paria B C, Matsumoto H, Swift L L, Morrow J, Bonventre J V, Dey S K. Cytosolic phospholipase A2alpha is crucial [correction of A2alpha deficiency is crucial] for ”on-time" embryo implantation that directs subsequent development. Development. 2002; 129 2879-2889
- 3 Lim H, Gupta R A, Ma W G, Paria B C, Moller D E, Morrow J D, DuBois R N, Trzaskos J M, Dey S K. Cyclo-oxygenase-2-derived prostacyclin mediates embryo implantation in the mouse via PPARdelta. Genes Dev. 1999; 13 1561-1574
- 4 Parent J, Chapdelaine P, Sirois J, Fortier M A. Expression of microsomal prostaglandin E synthase in bovine endometrium: coexpression with cyclooxygenase type 2 and regulation by interferon-tau. Endocrinology. 2002; 143 2936-2943
- 5 Bennegard B, Hahlin M, Wennberg E, Noren H. Local luteolytic effect of prostaglandin F2 alpha in the human corpus luteum. Fertil Steril. 1991; 56 1070-1076
- 6 Pratt B R, Butcher R L, Inskeep E K. Antiluteolytic effect of the conceptus and of PGE2 in ewes. J Anim Sci. 1977; 45 784-791
- 7 Hahlin M, Dennefors B, Johanson C, Hamberger L. Luteotropic effects of prostaglandin E2 on the human corpus luteum of the menstrual cycle and early pregnancy. J Clin Endocrinol Metab. 1988; 66 909-914
- 8 Parent J, Villeneuve C, Alexenko A P, Ealy A D, Fortier M A. Influence of different isoforms of recombinant trophoblastic interferons on prostaglandin production in cultured bovine endometrial cells. Biol Reprod. 2003; 68 1035-1043
- 9 Kawano Y, Nakamura S, Fukuda J, Miyakawa I. Synergistic effect of interleukin-1alpha and ceramide analogue on production of prostaglandin E2 and F2alpha by endometrial stromal cells. Am J Reprod Immunol. 2001; 46 393-398
- 10 Xiao C W, Murphy B D, Sirois J, Goff A K. Down-regulation of oxytocin-induced cyclooxygenase-2 and prostaglandin F synthase expression by interferon-tau in bovine endometrial cells. Biol Reprod. 1999; 60 656-663
- 11 Zlatnik M G, Copland J A, Ives K, Soloff M S. Functional oxytocin receptors in a human endometrial cell line. Am J Obstet Gynecol. 2000; 182 850-855
- 12 Toda S, Ando H, Nagasaka T, Tsukahara S, Nomura M, Kotani Y, Nomura S, Kikkawa F, Tsujimoto M, Mizutani S. Existence of placental leucine aminopeptidase/oxytocinase/insulin-regulated membrane aminopeptidase in human endometrial epithelial cells. J Clin Endocrinol Metab. 2002; 87 1384-1389
- 13 Lessey B A, Ilesanmi A O, Castelbaum A J, Yuan L, Somkuti S G, Chwalisz K, Satyaswaroop P G. Characterization of the functional progesterone receptor in an endometrial adenocarcinoma cell line (Ishikawa): progesterone-induced expression of the alpha1 integrin. J Steroid Biochem Mol Biol. 1996; 59 31-39
- 14 Ando H, Nagasaka T, Nomura M, Tsukahara S, Kotani Y, Toda S, Murata Y, Itakura A, Mizutani S. Premenstrual disappearance of aminopeptidase A in endometrial stromal cells around endometrial spiral arteries/arterioles during the decidual change. J Clin Endocrinol Metab. 2002; 87 2303-2309
- 15 Arnold J T, Kaufman D G, Seppala M, Lessey B A. Endometrial stromal cells regulate epithelial cell growth in vitro: a new co-culture model. Hum Reprod. 2001; 16 836-845
- 16 Satyaswaroop P G, Bressler R S, de la Pena M M, Gurpide E. Isolation and culture of human endometrial glands. J Clin Endocrinol Metab. 1979; 48 639-641
- 17 Iwase A, Nomura S, Mizutani S. Characterization of a secretase activity for placental leucine aminopeptidase. Arch Biochem Biophys. 2001; 393 163-169
- 18 Nakamura H, Itakuara A, Okamura M, Ito M, Iwase A, Nakanishi Y, Okada M, Nagasaka T, Mizutani S. Oxytocin stimulates the translocation of oxytocinase of human vascular endothelial cells via activation of oxytocin receptors. Endocrinology. 2000; 141 4481-4485
- 19 Tokunaga K, Nakamura Y, Sakata K, Fujimori K, Ohkubo M, Sawada K, Sakiyama S. Enhanced expression of a glyceraldehyde-3-phosphate dehydrogenase gene in human lung cancers. Cancer Res. 1987; 47 5616-5619
- 20 Matsumoto H, Rogi T, Yamashiro K, Kodama S, Tsuruoka N, Hattori A, Takio K, Mizutani S, Tsujimoto M. Characterization of a recombinant soluble form of human placental leucine aminopeptidase/oxytocinase expressed in Chinese hamster ovary cells. Eur J Biochem. 2000; 267 46-52
- 21 Ross S A, Scott H M, Morris N J, Leung W Y, Mao F, Lienhard G E, Keller S R. Characterization of the insulin-regulated membrane aminopeptidase in 3T3-L1 adipocytes. J Biol Chem. 1996; 271 3328-3332
- 22 Thurmond D C, Ceresa B P, Okada S, Elmendorf J S, Coker K, Pessin J E. Regulation of insulin-stimulated GLUT4 translocation by Munc18c in 3T3L1 adipocytes. J Biol Chem. 1998; 273 33 876-33 883
- 23 Keller S R. The insulin-regulated aminopeptidase: a companion and regulator of GLUT4. Front Biosci. 2003; 8 410-420
- 24 Dawood M Y, Lau M, Khan-Dawood F S. Localization and expression of oxytocin receptor and its messenger ribonucleic acid in peri-implantation phase human endometrium during control and clomiphene-treated cycles. Am J Obstet Gynecol. 1999; 181 50-56
- 25 Imai K, Kanzaki H, Mori T. Cell surface peptidases in human endometrium. Mol Hum Reprod. 1996; 2 425-431
- 26 Nayak N R, Sengupta J, Ghosh D. Antinidatory effect of luteal phase administration of mifepristone (RU486) is associated with changes in endometrial prostaglandins during the implantation window. Contraception. 1998; 58 111-117
- 27 Lala P K, Kearns M, Parhar R S, Scodras J, Johnson S. Immunological role of the cellular constituents of the decidua in the maintenance of semiallogeneic pregnancy. Ann N Y Acad Sci. 1986; 476 183-205
- 28 Frank G R, Brar A K, Cedars M I, Handwerger S. Prostaglandin E2 enhances human endometrial stromal cell differentiation. Endocrinology. 1994; 134 258-263
- 29 Jacobs A L, Carson D D. Uterine epithelial cell secretion of interleukin-1 alpha induces prostaglandin E2 (PGE2) and PGF2 alpha secretion by uterine stromal cells in vitro. Endocrinology. 1993; 132 300-308
- 30 Ribeiro M L, Perez Martinez S, Farina M, Ogando D, Gimeno M, Franchi A. The effect of epidermal growth factor on prostaglandin synthesis of oestrogenized rat uterus is mediated by nitric oxide. Prostaglandins Leukot Essent Fatty Acids. 1999; 61 353-358
- 31 Wijayagunawardane M P, Miyamoto A, Cerbito W A, Acosta T J, Takagi M, Sato K. Local distributions of oviductal estradiol, progesterone, prostaglandins, oxytocin and endothelin-1 in the cyclic cow. Theriogenology. 1998; 49 607-618
- 32 Wijayagunawardane M P, Miyamoto A, Taquahashi Y, Gabler C, Acosta T J, Nishimura M, Killian G, Sato K. In vitro regulation of local secretion and contraction of the bovine oviduct: stimulation by luteinizing hormone, endothelin-1 and prostaglandins, and inhibition by oxytocin. J Endocrinol. 2001; 168 117-130
- 33 Grazzini E, Guillon G, Mouillac B, Zingg H H. Inhibition of oxytocin receptor function by direct binding of progesterone. Nature. 1998; 392 509-512
Akira Iwase, M. D.
Department of Obstetrics and Gynecology, Nagoya University Graduate School of Medicine
65 Tsurumai-cho · Showa-ku · Nagoya 466-8550 · Japan
Phone: +81 (52) 744-2261
Fax: +81 (52) 744-2268
Email: akiwase@med.nagoya-u.ac.jp