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Published in: Reproductive Biology and Endocrinology 1/2004

Open Access 01-12-2004 | Research

Immature rats show ovulatory defects similar to those in adult rats lacking prostaglandin and progesterone actions

Authors: María Gaytan, Carmen Bellido, Concepcion Morales, Marcelino Gonzalez-Padilla, Jose E Sanchez-Criado, Francisco Gaytan

Published in: Reproductive Biology and Endocrinology | Issue 1/2004

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Abstract

Gonadotropin-primed immature rats (GPIR) constitute a widely used model for the study of ovulation. Although the equivalence between the ovulatory process in immature and adult rats is generally assumed, the morphological and functional characteristics of ovulation in immature rats have been scarcely considered. We describe herein the morphological aspects of the ovulatory process in GPIR and their response to classical ovulation inhibitors, such as the inhibitor of prostaglandin (PG) synthesis indomethacin (INDO) and a progesterone (P) receptor (PR) antagonist (RU486). Immature Wistar rats were primed with equine chorionic gonadotropin (eCG) at 21, 23 or 25 days of age, injected with human chorionic gonadotropin (hCG) 48 h later, and sacrificed 16 h after hCG treatment, to assess follicle rupture and ovulation. Surprisingly, GPIR showed age-related ovulatory defects close similar to those in adult rats lacking P and PG actions. Rats primed with eCG at 21 or 23 days of age showed abnormally ruptured corpora lutea in which the cumulus-oocyte complex (COC) was trapped or had been released to the ovarian interstitum, invading the ovarian stroma and blood and lymphatic vessels. Supplementation of immature rats with exogenous P and/or PG of the E series did not significantly inhibit abnormal follicle rupture. Otherwise, ovulatory defects were practically absent in rats primed with eCG at 25 days of age. GPIR treated with INDO showed the same ovulatory alterations than vehicle-treated ones, although affecting to a higher proportion of follicles. Blocking P actions with RU486 increased the number of COC trapped inside corpora lutea and decreased ovulation. The presence of ovulatory defects in GPIR, suggests that the capacity of the immature ovary to undergo the coordinate changes leading to effective ovulation is not fully established in Wistar rats primed with eCG before 25 days of age.
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Literature
1.
go back to reference Tsafriri A, Chun SY, Reich R: Follicular rupture and ovulation. In: The Ovary. Edited by: Adashi EY, Leung PCK. 1993, New York: Raven Press, 228-243. Tsafriri A, Chun SY, Reich R: Follicular rupture and ovulation. In: The Ovary. Edited by: Adashi EY, Leung PCK. 1993, New York: Raven Press, 228-243.
2.
go back to reference Espey LL, Lipner H: Ovulation. In: The physiology of Reproduction. Edited by: Knobil E, Neill JD. 1994, New York: Raven Press, 1: 725-780. 2 Espey LL, Lipner H: Ovulation. In: The physiology of Reproduction. Edited by: Knobil E, Neill JD. 1994, New York: Raven Press, 1: 725-780. 2
3.
go back to reference Brännström M, Janson PO: The biochemistry of ovulation. In: Ovarian Endocrinology. Edited by: Hillier SG. 1991, Oxford: Blackwell Scientific Publications, 132-166. Brännström M, Janson PO: The biochemistry of ovulation. In: Ovarian Endocrinology. Edited by: Hillier SG. 1991, Oxford: Blackwell Scientific Publications, 132-166.
4.
go back to reference Robker RL, Russell DL, Yoshioka S, Sharma SC, Lydon JP, O'Malley BW, Espey LL, Richards JS: Ovulation: a multi-gene, multi-step process. Steroids. 2000, 65: 559-570. 10.1016/S0039-128X(00)00114-8.CrossRefPubMed Robker RL, Russell DL, Yoshioka S, Sharma SC, Lydon JP, O'Malley BW, Espey LL, Richards JS: Ovulation: a multi-gene, multi-step process. Steroids. 2000, 65: 559-570. 10.1016/S0039-128X(00)00114-8.CrossRefPubMed
5.
go back to reference Ny T, Wahlberg P, Brändström IJM: Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems. Mol Cell Endocrinol. 2002, 187: 29-38. 10.1016/S0303-7207(01)00711-0.CrossRefPubMed Ny T, Wahlberg P, Brändström IJM: Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems. Mol Cell Endocrinol. 2002, 187: 29-38. 10.1016/S0303-7207(01)00711-0.CrossRefPubMed
7.
go back to reference Gaytán F, Tarradas E, Morales C, Bellido C, Sánchez-Criado JE: Morphological evidence for uncontrolled proteolytic activity during the ovulatory process in indomethacin-trated rats. Reproduction. 2002, 123: 639-649. 10.1530/rep.0.1230639.CrossRefPubMed Gaytán F, Tarradas E, Morales C, Bellido C, Sánchez-Criado JE: Morphological evidence for uncontrolled proteolytic activity during the ovulatory process in indomethacin-trated rats. Reproduction. 2002, 123: 639-649. 10.1530/rep.0.1230639.CrossRefPubMed
8.
go back to reference Gaytán F, Tarradas E, Bellido C, Morales C, Sánchez-Criado JE: Prostaglandin E1 inhibits abnormal follicle rupture and restores ovulation in indomethacin-treated rats. Biol Reprod. 2002, 67: 1140-1147.CrossRefPubMed Gaytán F, Tarradas E, Bellido C, Morales C, Sánchez-Criado JE: Prostaglandin E1 inhibits abnormal follicle rupture and restores ovulation in indomethacin-treated rats. Biol Reprod. 2002, 67: 1140-1147.CrossRefPubMed
9.
go back to reference Gaytán F, Bellido C, Gaytán M, Morales C, Sánchez-Criado JE: Differential effects of RU486 and indomethacin on follicle rupture during the ovulatory process in the rat. Biol Reprod. 2003, 69: 99-105.CrossRefPubMed Gaytán F, Bellido C, Gaytán M, Morales C, Sánchez-Criado JE: Differential effects of RU486 and indomethacin on follicle rupture during the ovulatory process in the rat. Biol Reprod. 2003, 69: 99-105.CrossRefPubMed
10.
go back to reference Van der Schoot P, Bakker GH, Kljin JG: of the progesterone antagonist RU486 on ovarian activity in the rat. Endocrinology. 1987, 121: 1375-1382.CrossRefPubMed Van der Schoot P, Bakker GH, Kljin JG: of the progesterone antagonist RU486 on ovarian activity in the rat. Endocrinology. 1987, 121: 1375-1382.CrossRefPubMed
11.
go back to reference Sánchez-Criado JE, Bellido C, Galiot F, López FJ, Gaytán F: A posible dual mechanism of the anovulatory action of antiprogesterone RU486 in the rat. Biol Reprod. 1990, 42: 877-886.CrossRefPubMed Sánchez-Criado JE, Bellido C, Galiot F, López FJ, Gaytán F: A posible dual mechanism of the anovulatory action of antiprogesterone RU486 in the rat. Biol Reprod. 1990, 42: 877-886.CrossRefPubMed
12.
go back to reference Reese J, Zhao X, Ma W, Brown N, Maziasz TJ, Dey SK: Comparative analysis of pharmacologic and/or genetic disruption of cyclooxygenase-1 and cyclooxygenase-2 function in female reproduction in mice. Endocrinology. 2001, 142: 3198-3206. 10.1210/en.142.7.3198.PubMed Reese J, Zhao X, Ma W, Brown N, Maziasz TJ, Dey SK: Comparative analysis of pharmacologic and/or genetic disruption of cyclooxygenase-1 and cyclooxygenase-2 function in female reproduction in mice. Endocrinology. 2001, 142: 3198-3206. 10.1210/en.142.7.3198.PubMed
13.
go back to reference Mori T, Kohda H, Kinoshita Y, Ezaki Y, Morimoto N, Nishimura T: Inhibition by indomethacin of ovulation induced by human chorionic gonadotrophin in immature rats primed with pregnant mare serum gonadotrophin. J Endocrinol. 1980, 84: 333-341.CrossRefPubMed Mori T, Kohda H, Kinoshita Y, Ezaki Y, Morimoto N, Nishimura T: Inhibition by indomethacin of ovulation induced by human chorionic gonadotrophin in immature rats primed with pregnant mare serum gonadotrophin. J Endocrinol. 1980, 84: 333-341.CrossRefPubMed
14.
go back to reference Rao IM, Mahesh VB: Role of progesterone in the modulation of the preovulatory surge of gonadotropins and ovulation in the pregnant mare's serum gonadotropin-primed immature rat and the adult rat. Biol Reprod. 1986, 35: 1154-1161.CrossRefPubMed Rao IM, Mahesh VB: Role of progesterone in the modulation of the preovulatory surge of gonadotropins and ovulation in the pregnant mare's serum gonadotropin-primed immature rat and the adult rat. Biol Reprod. 1986, 35: 1154-1161.CrossRefPubMed
15.
go back to reference Butler TA, Zhu C, Mueller RA, Fuller GC, Lemaire WJ, Woessner JF: Inhibition of ovulation in the perfused rat ovary by the synthetic collagenase inhibitor SC 44463. Biol Reprod. 1991, 44: 1183-1188.CrossRefPubMed Butler TA, Zhu C, Mueller RA, Fuller GC, Lemaire WJ, Woessner JF: Inhibition of ovulation in the perfused rat ovary by the synthetic collagenase inhibitor SC 44463. Biol Reprod. 1991, 44: 1183-1188.CrossRefPubMed
16.
go back to reference Zhu C, Woessner JF: A tissue inhibitor of metalloproteinases and α-macroglobulins in the ovulating rat ovary: possible regulators of collagen matrix breakdown. Biol Reprod. 1991, 45: 334-342.CrossRefPubMed Zhu C, Woessner JF: A tissue inhibitor of metalloproteinases and α-macroglobulins in the ovulating rat ovary: possible regulators of collagen matrix breakdown. Biol Reprod. 1991, 45: 334-342.CrossRefPubMed
17.
go back to reference Chun SY, Popliker M, Reich R, Tsafriri A: Localization of preovulatory expression of plasminogen activator inhibitor type-1 and tissue inhibitor of metalloproteinase type-1 mRNAs in the rat ovary. Biol Reprod. 1992, 47: 245-253.CrossRefPubMed Chun SY, Popliker M, Reich R, Tsafriri A: Localization of preovulatory expression of plasminogen activator inhibitor type-1 and tissue inhibitor of metalloproteinase type-1 mRNAs in the rat ovary. Biol Reprod. 1992, 47: 245-253.CrossRefPubMed
18.
go back to reference Iwamasa J, Shibata S, Tanaka N, Matsuura K, Okamura H: The relationship between ovarian progesterone and proteolytic enzyme activity during ovulation in the gonadotropin-treated immature rat. Biol Reprod. 1992, 46: 309-313.CrossRefPubMed Iwamasa J, Shibata S, Tanaka N, Matsuura K, Okamura H: The relationship between ovarian progesterone and proteolytic enzyme activity during ovulation in the gonadotropin-treated immature rat. Biol Reprod. 1992, 46: 309-313.CrossRefPubMed
19.
go back to reference Mann JS, Kindy MS, Hyde JF, Clark MR, Curry TE: Role of protein synthesis, prostaglandins, and estrogen in rat ovarian metalloproteinase inhibitor production. Biol Reprod. 1993, 48: 1006-1013.CrossRefPubMed Mann JS, Kindy MS, Hyde JF, Clark MR, Curry TE: Role of protein synthesis, prostaglandins, and estrogen in rat ovarian metalloproteinase inhibitor production. Biol Reprod. 1993, 48: 1006-1013.CrossRefPubMed
20.
go back to reference Natraj U, Richards J: Hormonal regulation, localization, and functional activity of the progesterone receptor in granulosa cells of rat preovulatory follicles. Endocrinology. 1993, 133: 761-769. 10.1210/en.133.2.761.PubMed Natraj U, Richards J: Hormonal regulation, localization, and functional activity of the progesterone receptor in granulosa cells of rat preovulatory follicles. Endocrinology. 1993, 133: 761-769. 10.1210/en.133.2.761.PubMed
21.
go back to reference Liu K, Wahlberg P, Ny T: Coordinated and cell-specific regulation of memebrane type matrix metalloproteinase 1 (MT1-MMP) and its substrate matrix metalloproteinase 2 (MMP-2) by physiological signals during follicular development and ovulation. Endocrinology. 1998, 139: 4735-4738. 10.1210/en.139.11.4735.CrossRefPubMed Liu K, Wahlberg P, Ny T: Coordinated and cell-specific regulation of memebrane type matrix metalloproteinase 1 (MT1-MMP) and its substrate matrix metalloproteinase 2 (MMP-2) by physiological signals during follicular development and ovulation. Endocrinology. 1998, 139: 4735-4738. 10.1210/en.139.11.4735.CrossRefPubMed
22.
go back to reference Cooke RG, Nothnick WB, Komar C, Burns P, Curry TE: Collagenase and gelatinase messenger ribonucleic acid expression and activity during follicular development in the rat ovary. Biol Reprod. 1999, 61: 1309-1316.CrossRefPubMed Cooke RG, Nothnick WB, Komar C, Burns P, Curry TE: Collagenase and gelatinase messenger ribonucleic acid expression and activity during follicular development in the rat ovary. Biol Reprod. 1999, 61: 1309-1316.CrossRefPubMed
23.
go back to reference Espey LL, Yoshioka S, Russel D, Ujioka T, Vladu B, Skelsey M, Fujii S, Okamura H, Richards JS: Characterization of ovarian carbonyl reductase gene expression during ovulation in the gonadotropin-primed immature rat. Biol Reprod. 2000, 62: 390-397.CrossRefPubMed Espey LL, Yoshioka S, Russel D, Ujioka T, Vladu B, Skelsey M, Fujii S, Okamura H, Richards JS: Characterization of ovarian carbonyl reductase gene expression during ovulation in the gonadotropin-primed immature rat. Biol Reprod. 2000, 62: 390-397.CrossRefPubMed
24.
go back to reference Curry TE, Song L, Wheeler SE: Cellular localization of gelatinases and tisssue inhibitors of metalloproteinases during follicular growth, ovulation, and early luteal formation in the rat. Biol Reprod. 2001, 65: 855-865.CrossRefPubMed Curry TE, Song L, Wheeler SE: Cellular localization of gelatinases and tisssue inhibitors of metalloproteinases during follicular growth, ovulation, and early luteal formation in the rat. Biol Reprod. 2001, 65: 855-865.CrossRefPubMed
25.
go back to reference Simpson KS, Komar CM, Curry TE: Localization and expression of tissue inhibior of metalloproteinase-4 in the immature gonadotropin-stimulated and adult rat ovary. Biol Reprod. 2003, 68: 214-221.CrossRefPubMed Simpson KS, Komar CM, Curry TE: Localization and expression of tissue inhibior of metalloproteinase-4 in the immature gonadotropin-stimulated and adult rat ovary. Biol Reprod. 2003, 68: 214-221.CrossRefPubMed
26.
go back to reference Tanaka N, Espey LL, Stacy S, Okamura H: Epostane and indomethacin actions on ovarian kalikrein and plasminogen activator activities during ovulation in the gonadotropin-primed immature rat. Biol Reprod. 1992, 46: 665-670.CrossRefPubMed Tanaka N, Espey LL, Stacy S, Okamura H: Epostane and indomethacin actions on ovarian kalikrein and plasminogen activator activities during ovulation in the gonadotropin-primed immature rat. Biol Reprod. 1992, 46: 665-670.CrossRefPubMed
27.
go back to reference Yoshioka S, Fujii S, Richards JS, Espey LL: Gonadotropin-induced expression of pancreatitis-associated protein-III mRNA in the rat ovary at the time of ovulation. J Endocrinol. 2002, 174: 485-492.CrossRefPubMed Yoshioka S, Fujii S, Richards JS, Espey LL: Gonadotropin-induced expression of pancreatitis-associated protein-III mRNA in the rat ovary at the time of ovulation. J Endocrinol. 2002, 174: 485-492.CrossRefPubMed
28.
go back to reference Espey LL, Norris C, Forman J, Siler-Khodr T: Effect of indomethacin, cycloheximide, and aminoglutethimide on ovarian steroid and prostanoid levels during ovulation in the gonadotropin-primed immature rat. Prostaglandins. 1989, 38: 531-539. 10.1016/0090-6980(89)90147-0.CrossRefPubMed Espey LL, Norris C, Forman J, Siler-Khodr T: Effect of indomethacin, cycloheximide, and aminoglutethimide on ovarian steroid and prostanoid levels during ovulation in the gonadotropin-primed immature rat. Prostaglandins. 1989, 38: 531-539. 10.1016/0090-6980(89)90147-0.CrossRefPubMed
29.
go back to reference Zarrow MX, Wilson ED: The influence of age on superovulation in the immature rat and mouse. Endocrinology. 1961, 69: 851-855.CrossRefPubMed Zarrow MX, Wilson ED: The influence of age on superovulation in the immature rat and mouse. Endocrinology. 1961, 69: 851-855.CrossRefPubMed
30.
go back to reference Zarrow MX, Quinn DL: Superovulation in the immature rat following treatment with SG-induced ovulation. J Endocrinol. 1963, 26: 181-188.CrossRefPubMed Zarrow MX, Quinn DL: Superovulation in the immature rat following treatment with SG-induced ovulation. J Endocrinol. 1963, 26: 181-188.CrossRefPubMed
31.
go back to reference Sogn JH, Curry TEJr, Brännström M, LeMaire WJ, Koos RD, Papkoff H, Janson PO: Inhibition of follicle-stimulating hormone-induced ovulation by indomethacin in the perfused rat ovary. Biol Reprod. 1987, 36: 536-542.CrossRefPubMed Sogn JH, Curry TEJr, Brännström M, LeMaire WJ, Koos RD, Papkoff H, Janson PO: Inhibition of follicle-stimulating hormone-induced ovulation by indomethacin in the perfused rat ovary. Biol Reprod. 1987, 36: 536-542.CrossRefPubMed
32.
go back to reference Matsumoto H, Ma W, Smalley W, Trzaskos J, Breyer RM, Dey SK: Diversification of cyclooxygenase-2-derived prostaglandins in ovulation and implantation. Biol Reprod. 2000, 64: 1557-1565.CrossRef Matsumoto H, Ma W, Smalley W, Trzaskos J, Breyer RM, Dey SK: Diversification of cyclooxygenase-2-derived prostaglandins in ovulation and implantation. Biol Reprod. 2000, 64: 1557-1565.CrossRef
33.
go back to reference Mori T, Suzuku A, Nishimura T, Kambegawa A: Inhibition of ovulation in immature rats by antiprogesterone antiserum. J Endocrinol. 1977, 73: 185-186.CrossRefPubMed Mori T, Suzuku A, Nishimura T, Kambegawa A: Inhibition of ovulation in immature rats by antiprogesterone antiserum. J Endocrinol. 1977, 73: 185-186.CrossRefPubMed
34.
go back to reference Snyder B, Beecham G, Schane H: Inhibition of ovulation in rats with epostane, an inhibitor of 3β-hydroxysteroid dehydrogenase. Proc Soc Exp Biol Med. 1984, 176: 238-242.CrossRefPubMed Snyder B, Beecham G, Schane H: Inhibition of ovulation in rats with epostane, an inhibitor of 3β-hydroxysteroid dehydrogenase. Proc Soc Exp Biol Med. 1984, 176: 238-242.CrossRefPubMed
35.
go back to reference Hibbert ML, Stouffer RL, Wolf DP, Zelinski-Wooten MB: Midcycle administration of a progesterone synthesis inhibitor prevents ovulation in primates. Proc Natl Acad Sci USA. 1996, 93: 1897-1901. 10.1073/pnas.93.5.1897.PubMedCentralCrossRefPubMed Hibbert ML, Stouffer RL, Wolf DP, Zelinski-Wooten MB: Midcycle administration of a progesterone synthesis inhibitor prevents ovulation in primates. Proc Natl Acad Sci USA. 1996, 93: 1897-1901. 10.1073/pnas.93.5.1897.PubMedCentralCrossRefPubMed
36.
go back to reference Uilenbroek JTJ: Hormone concentration and ovulatory response in rats treated with antiprogestagens. J Endocrinol. 1991, 129: 423-429.CrossRefPubMed Uilenbroek JTJ: Hormone concentration and ovulatory response in rats treated with antiprogestagens. J Endocrinol. 1991, 129: 423-429.CrossRefPubMed
37.
go back to reference Pall M, Mikuni M, Mitsube K, Brännström M: Time-dependent ovulation inhibition of a selective progesterone-receptor antagonist (Org 31710) and effects on ovulatory mediators in the in vitro perfused rat ovary. Biol Reprod. 2000, 63: 1642-1647.CrossRefPubMed Pall M, Mikuni M, Mitsube K, Brännström M: Time-dependent ovulation inhibition of a selective progesterone-receptor antagonist (Org 31710) and effects on ovulatory mediators in the in vitro perfused rat ovary. Biol Reprod. 2000, 63: 1642-1647.CrossRefPubMed
38.
go back to reference Reich R, Tsafriri A, Mechanic GL: The involvement of collagenase in ovulation in the rat. Endocrinology. 1985, 116: 522-527.CrossRefPubMed Reich R, Tsafriri A, Mechanic GL: The involvement of collagenase in ovulation in the rat. Endocrinology. 1985, 116: 522-527.CrossRefPubMed
39.
go back to reference Woessner JF, Butler T, LeMaire WJ, Morioka N, Mukaida T, Zhu C: The role of collagenase in ovulation in the rat. In: Follicular Development and Ovulation Regulation. Edited by: Tsafriri A, Dekel N. 1989, Serono Symposia: Raven Press, 169-178. Woessner JF, Butler T, LeMaire WJ, Morioka N, Mukaida T, Zhu C: The role of collagenase in ovulation in the rat. In: Follicular Development and Ovulation Regulation. Edited by: Tsafriri A, Dekel N. 1989, Serono Symposia: Raven Press, 169-178.
Metadata
Title
Immature rats show ovulatory defects similar to those in adult rats lacking prostaglandin and progesterone actions
Authors
María Gaytan
Carmen Bellido
Concepcion Morales
Marcelino Gonzalez-Padilla
Jose E Sanchez-Criado
Francisco Gaytan
Publication date
01-12-2004
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2004
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-2-63

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