Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
Shopping Cart: ( empty )
You are here: Home > Journals > RD > RD03024
RESEARCH ARTICLE
Contents Vol 15(4)

Effect of ovarian steroids on basal and oxytocin-induced prostaglandin F2α secretion from pig endometrial cells

Jianbo Hu A B E , Gheorghe T. Braileanu A C and Mark A. Mirando A D
+ Author Affiliations
- Author Affiliations

A Department of Animal Sciences and Center for Reproductive Biology, Washington State University, Pullman, WA 99164-6353, USA.

B Present address: Department of Animal Science, Texas A&M University, College Station, TX 77843-2471, USA.

C Present address: Department of Pediatrics, School of Medicine, University of Maryland, Baltimore, MD 21201, USA.

D Present address: National Research Initiative Grants Program, 1400 Independence Avenue, S. W. Stop 2241, US Department of Agriculture, Washington, DC 20250-2241, USA.

E To whom correspondence should be addressed. email: jianbo@tamu.edu

Reproduction, Fertility and Development 15(4) 197-205 https://doi.org/10.1071/RD03024
Submitted: 4 March 2003  Accepted: 9 May 2003   Published: 13 August 2003

Abstract

These studies were undertaken to determine how treatment with 100 nM progesterone and/or 10 nM oestradiol-17β acutely (3 h; Experiment 1) or chronically (72 h; Experiments 2–4) influenced basal and oxytocin (OT)-stimulated prostaglandin (PG) F2α secretion, in enriched cultures of pig endometrial luminal epithelial, glandular epithelial and stromal cells obtained on Day 16 (Experiments 1, 2 and 4) or Day 12 (Experiment 3) after oestrus. In Experiment 1, acute treatment with progesterone stimulated PGF2α secretion from each cell type on Day 16, whereas acute oestradiol treatment inhibited the stimulatory action of progesterone on PGF2α secretion only in glandular epithelial cells. In Experiment 2, OT stimulated phospholipase (PL) C activity in luminal epithelial cells on Day 16 only in the presence of chronic oestradiol treatment. For glandular epithelial cells on Day 16, OT stimulated PLC activity only in the presence of chronic treatment with steroid. In stromal cells on Day 16, OT stimulated PLC activity in the absence of steroids and the response to OT was further enhanced by oestradiol. In the absence of chronic treatment with steroid, OT did not stimulate PGF2α secretion from luminal epithelial cells, but oestradiol induced a response to OT. For glandular epithelial cells, OT-induced PGF2α secretion was not altered by steroids, whereas the stimulatory response to OT was inhibited by oestradiol or progesterone in stromal cells. For endometrial cells obtained on Day 12 after oestrus in Experiment 3, OT only stimulated PGF2α release from glandular epithelial and stromal cells. For luminal epithelial cells obtained on Day 16 after oestrus and cultured under polarizing conditions in Experiment 4, secretion of PGF2α occurred preferentially from the basolateral surface and was stimulated by OT more from the basolateral surface than from the apical surface. Oxytocin-induced PGF2α secretion from the apical surface was enhanced by chronic treatment with oestradiol, whereas that from the basolateral surface was enhanced by chronic treatment with progesterone. In summary, oestradiol enhanced OT-induced PGF2α secretion from the apical surface of luminal epithelial cells and reduced the response of stromal cells to OT, actions that may contribute to the reorientation of PGF2α from endocrine secretion (i.e. towards the uterine vasculature) to exocrine secretion (i.e. towards the uterine lumen) during pregnancy recognition in pigs.

Extra keywords: endometrium


Acknowledgments

The authors are indebted to Dr Fuller W. Bazer (Texas A&M University) for critical review of this manuscript and to Dr William W. Thatcher (University of Florida) for supplying the antiserum to PGF2α. The authors are also grateful to the members of M. A. Mirando’s laboratory for assistance with surgery and to the staff of the Washington State University Swine Center and the Experimental Animal Laboratory Building for assistance with the care and handling of animals. This work was supported by National Institutes of Health grant HD30268 to MAM.


References

Armato, U. , and Andreis, P. G. (1983). Prostaglandins of the F series are extremely powerful factors for primary neonatal rat hepatocytes Life Sci. 33, 1745–55.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Asselin, E. , Goff, A. K. , Bergeron, H. R. , and Fortier, M. A. (1996). Influence of sex steroids on the production of prostaglandin F2α and E2 and response to oxytocin in cultured epithelial and stromal cells of the bovine endometrium Biol. Reprod. 54, 371–9..
| PubMed |

Bazer, F. W. , and Thatcher, W. W. (1977). Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2α by the uterine endometrium Prostaglandins 14, 397–400.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Blackwell, D. M. , Speth, R. C. , and Mirando, M. A. (2003). Morphometric analysis of the uterine endometrium of swine on days 12 and 16 postoestrus Anat. Rec. 270, 59–66..
| Crossref | GoogleScholarGoogle Scholar |

Boshier, D. P. , Fairclough, R. J. , and Holloway, H. R. (1987). Assessment of sheep blastocyst effects on neutral lipids in the uterine caruncular epithelium J. Reprod. Fertil. 79, 569–73.
| PubMed |

Boulton, M. I. , McGrath, T. J. , Brown, D. A. , Broad, K. D. , and Gilbert, C. L. (1995). Oxytocin receptor mRNA expression in the porcine uterus J. Reprod. Fertil. Abstr. Ser. 15, 36–7.


Braileanu, G. T. , Simasko, S. M. , Uzumcu, M. , and Mirando, M. A. (1999). Intracellular free calcium in response to oxytocin in pig endometrial cells Mol. Cell. Endocrinol. 155, 77–83.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Braileanu, G. T. , Hu, J. , and Mirando, M. A. (2000). Directional secretion of prostaglandin F2α by polarized luminal epithelial cells from pig endometrium Prostaglandins Other Lipid Mediat. 60, 167–74.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Brinsfield, T. H. , and Hawk, H. W. (1973). Control by progesterone of the concentration of lipid droplets in epithelial cells of the sheep endometrium J. Anim. Sci. 36, 919–22.
| PubMed |

Burton, K. (1956). A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid Biochem. J. 62, 315–22.
| PubMed |

Carnahan, K. G. , Prince, B. C. , and Mirando, M. A. (1996). Exogenous oxytocin stimulates uterine secretion of prostaglandin F2α in cyclic and early pregnant swine Biol. Reprod. 55, 838–43.
| PubMed |

Carnahan, K. G. , Prince, B. C. , Ludwig, T. E. , Uzumcu, M. , Evans, M. A. , and Mirando, M. A. (1999). Effect of oxytocin on concentration of PGF2α in the uterine lumen and subsequent endometrial responsiveness to oxytocin in pigs J. Reprod. Fertil. 117, 207–12.
| PubMed |

Carnahan, K. G. , Uzumcu, M. , Hu, J. , Sample, G. L. , Braileanu, G. T. , and Mirando, M. A. (2002). Oxytocin stimulates secretion of prostaglandin F2α from endometrial cells of swine in the presence of progesterone Domest. Anim. Endocrinol. 23, 435–45.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Charpigny, G. , Reinaud, P. , Tamby, J. P. , Creminon, C. , Martal, J. , Maclouf, J. , and Guillomot, M. (1997). Expression of cyclo-oxygenase-1 and -2 in ovine endometrium during the oestrous cycle and early pregnancy Endocrinology 138, 2163–71.
| PubMed |

Cooke, P. S. , Buchanan, D. L. , Young, P. , Setiawan, T. , Brody, J. , Korach, K. S. , Taylor, J. A. , Lubahn, D. B. , and Cunha, G. R. (1997). Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium Proc. Natl Acad. Sci. USA 94, 6535–40.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Datta, M. C. (1985). Prostaglandin E2 mediated effects on the synthesis of fetal and adult hemoglobin in blood erythroid bursts Prostaglandins 29, 561–77.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Edgerton, L. A , Kaminski, M. A. , and Silvia, W. J. (1996). Changes in uterine secretion of prostaglandin F2α in response to oxytocin during the estrous cycle, early pregnancy, and estrogen-induced pseudopregnancy in swine Biol. Reprod. 55, 657–62.
| PubMed |

Edgerton, L. A. , Kaminski, M. A. , and Silvia, W. J. (2000). Effects of progesterone and oestradiol on uterine secretion of prostaglandin F2α in response to oxytocin in ovariectomized sows Biol. Reprod. 62, 365–9.
| PubMed |

Eggleston, D. L. , Wilken, C. , Van Kirk, E. A. , Slaughter, R. G. , Ji, T. H. , and Murdoch, W. J. (1990). Progesterone induces expression of endometrial messenger RNA encoding for cyclooxygenase (sheep) Prostaglandins 39, 675–83.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Garrett, J. E. , Geisert, R. D. , Zavy, M. T. , Gries, L. K. , Wettemann, R. P. , and Buchanan, D. S. (1988). Effect of exogenous progesterone on prostaglandin F2α release and the interestrous interval in the bovine Prostaglandins 36, 85–96.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Geisert, R. D. , Zavy, M. T. , Moffatt, R. J. , Blair, R. M. , and Yellin, T. (1990). Embryonic steroids and the establishment of pregnancy in pigs J. Reprod. Fertil. 40, 293–305.(Suppl.),


Geisert, R. D. , Pratt, T. N. , Bazer, F. W. , Mayes, J. S. , and Watson, G. H. (1994). Immunocytochemical localization and changes in endometrial progestin receptor protein during the porcine oestrus cycle and early pregnancy Reprod. Fertil. Dev. 6, 749–60.
| PubMed |

Goodwin, R. D. , and Webb, D. R. (1980). Regulation of the immune response by prostaglandins Clin. Immunol. 15, 106–22.


Grazzini, E. , Guillon, G. , Mouillac, B. , and Zingg, H. H. (1998). Inhibition of oxytocin receptor function by direct binding of progesterone Nature 392, 437–8.
| PubMed |

Gross, T. S. , Lacroix, M. C. , Bazer, F. W. , Thatcher, W. W. , and Harney, J. P. (1988). Prostaglandin secretion by perifused porcine endometrium: further evidence for an endocrine versus exocrine secretion of prostaglandins Prostaglandins 35, 327–41.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Hixon, J. E. , and Flint, A. P. F. (1987). Effects of a luteolytic dose of oestradiol benzoate on uterine oxytocin receptor concentrations, phosphoinositide turnover and prostaglandin F2α secretion in sheep J. Reprod. Fertil. 79, 457–67.
| PubMed |

Homanics, G. E. , and Silvia, W. J. (1988). Effects of progesterone and oestradiol-17β on uterine secretion of prostaglandin F2α in response to oxytocin in ovariectomized ewes Biol. Reprod. 38, 804–11.
| PubMed |

Hu, J. B. , Braileanu, Gh. T. , and Mirando, M. A. (2001a). Oxytocin stimulates prostaglandin F2α secretion from porcine endometrial cells through activation of calcium-dependent protein kinase C Prostaglandins Other Lipid Mediat. 65, 85–101.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Hu, J. , Ludwig, T. E. , Salli, U. , Stormshak, F. , and Mirando, M. A. (2001b). Autocrine/paracrine action of oxytocin in pig endometrium Biol. Reprod. 64, 1682–8.
| PubMed |

Jenkin, G. (1992). Interaction between oxytocin and prostaglandin F2α during luteal regression and early pregnancy in sheep Reprod. Fertil. Dev. 4, 321–8.
| PubMed |

Julian, J. , Carson, D. D. , and Glasser, S. R. (1992a). Polarized rat uterine epithelium in vitro: responses to estrogen in defined medium Endocrinology 130, 68–78.
| PubMed |

Julian, J. , Carson, D. D. , and Glasser, S. R. (1992b). Polarized rat uterine epithelium in vitro: constitutive expression of estrogen-induced proteins Endocrinology 130, 79–87.
| PubMed |

Kennedy, T. G. , Martel, D. , and Psychoyos, A. (1983). Endometrial prostaglandin E2 binding: characterization in rats sensitized for the decidual cell reaction and changes during pseudopregnancy Biol. Reprod. 29, 556–64.
| PubMed |

Khurana, N. K. , and Wales, R. G. (1987). Effects of prostaglandins E-2 and F-2α on the metabolism of [U-14C]glucose by mouse morulae-early blastocysts in vitro.  J. Reprod. Fertil. 79, 275–80.
| PubMed |

Lewis, G. S. (1986). Indomethacin inhibits the uptake of 22-sodium by ovine trophoblast tissue in vitro  Prostaglandins 31, 111–22.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Ludwig, T. E. , Sun, B-C. , Carnahan, K. G. , Uzumcu, M. , Yelich, J. V. , Geisert, R. D. , and Mirando, M. A. (1998). Endometrial responsiveness to oxytocin during dioestrus and early pregnancy in pigs is not controlled solely by changes in oxytocin receptor population density Biol. Reprod. 58, 769–77.
| PubMed |

McCracken, J. A. , Custer, E. E. , and Lamsa, J. C. (1999). Luteolysis: a neuroendocrine-mediated event Physiol. Rev. 79, 263–323.
| PubMed |

Mirando, M. A. , Harney, J. P. , Zhou, Y. , Ogle, T. F. , Ott, T. L. , Moffatt, R. J. , and Bazer, F. W. (1993). Changes in progesterone and oestrogen receptor mRNA, progesterone and oestrogen receptor protein, and oxytocin receptors in endometrium of ewes after intrauterine injection of ovine trophoblast interferon J. Mol. Endocrinol. 10, 185–92.
| PubMed |

Mirando, M. A. , Uzumcu, M. , Carnahan, K. G. , and Ludwig, T. E. (1996). A role for oxytocin during luteolysis and early pregnancy in swine Reprod. Domest. Anim. 31, 455–61.


Morgan, G. L. , Geisert, R. D. , McCann, J. P. , Bazer, F. W. , Ott, T. L. , Mirando, M. A. , and Stewart, M. (1993). Failure of luteolysis and extension of the interoestrus interval in sheep treated with the progesterone antagonist mifepristone (RU 486) J. Reprod. Fertil. 98, 451–7.
| PubMed |

Nissenson, R. , Flouret, G. , and Hechter, O. (1978). Opposing effects of oestradiol and progesterone on oxytocin receptor in rabbit uterus Proc. Natl Acad. Sci. USA 75, 2044–8.
| PubMed |

Parhar, R. S. , Yagel, S. , and Lala, P. K. (1989). PGE2-mediated immunosuppression by first trimester human decidual cells blocks activation of maternal leukocytes in the decidua with potential anti-trophoblast activity Cell. Immunol. 120, 61–74.
| PubMed |

Rankin, J. (1976). A role for prostaglandins in the regulation of the placental blood flow Prostaglandins 11, 343–53.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Salamonsen, L. A. , Hampton, A. L. , Clements, J. A. , and Findlay, J. K. (1991). Regulation of gene expression and cellular localization of prostaglandin synthase by oestrogen and progesterone in the ovine uterus J. Reprod. Fertil. 92, 393–406.
| PubMed |

SAS. (1995). PC-SAS, Propriety Software Release 6. 11 System for Windows. (Statistical Analysis System Institute: Cary, NC.)

Schatz, F. , and Gurpide, E. (1983). Effects of oestradiol on prostaglandin F2α levels in primary monolayer cultures of epithelial cells from human proliferative endometrium Endocrinology 113, 1274–9.
| PubMed |

Schatz, F. , Markiewicz, L. , Barg, P. , and Gurpide, E. (1986). In vitro inhibition with antiestrogens of oestradiol effects on prostaglandin F2α production by human endometrium and endometrial epithelial cells Endocrinology 118, 408–12.
| PubMed |

Silvia, W. J. , Lewis, G. S. , McCracken, J. A. , Thatcher, W. W. , and Wilson, L. (1991). Hormonal regulation of uterine secretion of prostaglandin F2α during luteolysis in ruminants Biol. Reprod. 45, 655–63.
| PubMed |

Snedecor, G. W. and  Cochran, W. G. (1980). Factorial experiments. In Statistical Methods 7th edn. edn.  pp. 298–333. (Iowa State University Press: Ames: IA.)

Spencer, T. E. , and Bazer, F. W. (1995). Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe Biol. Reprod. 53, 1527–43.
| PubMed |

Spencer, T. E. , Becker, W. C. , George, P. , Mirando, M. A. , Ogle, T. F. , and Bazer, F. W. (1995). Ovine interferon-tau inhibits estrogen receptor up-regulation and estrogen-induced luteolysis in cyclic ewes Endocrinology 136, 4932–44.
| PubMed |

Spencer, T. E. , Mirando, M. A. , Mayes, J. S. , Watson, G. H. , Ott, T. L. , and Bazer, F. W. (1996). Effects of interferon-tau and progesterone on oestrogen-stimulated expression of receptors for oestrogen, progesterone and oxytocin in the endometrium of ovariectomized ewes Reprod. Fertil. Dev. 8, 843–53.
| PubMed |

Uzumcu, M. , Braileanu, G. T. , Carnahan, K. G. , Ludwig, T. E. , and Mirando, M. A. (1998). Oxytocin-stimulated phosphoinositide hydrolysis and prostaglandin F2α secretion by luminal epithelial, glandular epithelial, and stromal cells from pig endometrium. I. Response of cyclic pigs on day 16 post-oestrus Biol. Reprod. 59, 1259–65.
| PubMed |

Uzumcu, M. , Carnahan, K. G. , Braileanu, G. T. , and Mirando, M. A. (2000). Oxytocin-stimulated phosphoinositide hydrolysis and prostaglandin F2α secretion by luminal epithelial, glandular epithelial and stromal cells from pig endometrium. II. Response of cyclic, pregnant and pseudopregnant pigs on days 12 and 16 post-oestrus Reprod. Fertil. Dev. 12, 157–64.
| PubMed |

Vallet, J. L. , and Lamming, G. E. (1991). Ovine conceptus secretory proteins and bovine recombinant interferon α1-1 decrease endometrial oxytocin receptor concentrations in cyclic and progesterone-treated ovariectomized ewes J. Endocrinol. 131, 475–82.
| PubMed |

Vallet, J. L. , Bazer, F. W. , Fliss, M. F. , and Thatcher, W. W. (1988). Effect of ovine conceptus secretory proteins and purified ovine trophoblast protein-1 on interoestrus interval and plasma concentrations of prostaglandins F2α and E and of 13,14-dihydro-15-keto prostaglandin F2α in cyclic ewes J. Reprod. Fertil. 84, 493–504.
| PubMed |

Vallet, J. L. , Lamming, G. E. , and Batten, M. (1990). Control of endometrial oxytocin receptor and uterine response to oxytocin by progesterone and oestradiol in the ewe J. Reprod. Fertil. 90, 625–34.
| PubMed |

Vore, S. J. , Eling, T. E. , Danilowicz, R. M. , Tucker, A. N. , and Luster, M. I. (1989). Regulation of murine hematopoiesis by arachidonic acid metabolism Int. J. Immunopharmacol. 11, 435–42.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Wang, G. , Bazer, F. W. , Ott, T. L. , and Glasser, S. R. (1998). Polarized luminal epithelial cells isolated from pregnant pig uteri are steroid hormone responsive in vitro.  Biol. Reprod. 58, 53.(Abstract.)


Watson, E. D. , Aubrey, E. S. , Zanecosky, H. G. , and Sertich, P. L. (1992). Isolation and culture of glandular epithelial and stromal cells from the endometrium of mares J. Reprod. Fertil. 95, 269–75.
| PubMed |

Watson, C. S. , Campbell, C. H. , and Gametchu, B. (2002). The dynamic and elusive membrane estrogen receptor-alpha Steroids 67, 429–37.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Whiteaker, S. S. , Mirando, M. A. , Becker, W. C. , and Hostetler, C. E. (1994). Detection of functional oxytocin receptors on endometrium of pigs Biol. Reprod. 51, 92–8.
| PubMed |

Woody, C. O. , First, N. L. , and Pope, A. L. (1967). Effect of exogenous progesterone on estrous cycle length J. Anim. Sci. 26, 139–41.
| PubMed |

Zhang, Z. , and Davis, D. L. (1991). Prostaglandin E and F2α secretion by glandular and stromal cells of the pig endometrium in vitro: effects of oestradiol 17β, progesterone, and day of pregnancy Prostaglandins 42, 151–62.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Zhang, Z. , Paria, B. C. , and Davis, D. L. (1991). Pig endometrial cells in primary culture: morphology, secretion of prostaglandins and proteins, and effects of pregnancy J. Anim. Sci. 69, 3005–15.
| PubMed |