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Published in: Reproductive Biology and Endocrinology 1/2014

Open Access 01-12-2014 | Research

The effect of hormonal estrus induction on maternal effect and apoptosis-related genes expression in porcine cumulus-oocyte complexes

Authors: Marek Bogacki, Marta Wasielak, Anna Kitewska, Iwona Bogacka, Beenu Moza Jalali

Published in: Reproductive Biology and Endocrinology | Issue 1/2014

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Abstract

Background

The effect of hormonal estrus induction on maternal effect (MATER - maternal antigen that embryo requires, ZAR-1 - zygote arrest 1, and BMP15 - bone morphogenetic protein 15) and apoptosis-related genes expression (BCL-2 and BAX) in porcine cumulus-oocyte complexes (COCs) and selected follicular parameters was investigated in this study.

Methods

Gilts were divided into three groups: (I) with natural estrus; (II) stimulated with PMSG/hCG; and (III) with PMSG/hCG + PGF2alpha. Analysis of maternal effect and apoptosis-related transcripts expression in COCs, and progesterone synthesis pathway genes expression (P450scc and 3betaHSD) in granulosa cells was performed by qPCR. BMP15 protein expression in follicular fluid (FF) was analyzed by western blot. Oocyte nuclear maturation was assessed by aceto-orcein staining. Progesterone (P4) and estradiol (E2) concentrations in FF and serum were measured by ELISA. Data were analyzed with the one-way ANOVA and Bonferroni post-test or Kruskal-Wallis test and Dunns post-test.

Results

The highest expression of MATER, ZAR-1, and BMP15 genes was found in COCs recovered from gilts treated with PMSG/hCG when compared to PMSG/hCG + PGF2alpha-stimulated or non-stimulated gilts. Hormonal treatment did not affect the BMP15 protein expression in FF, but increased the expression of genes participating in P4 synthesis in granulosa cells. The higher percentage of immature oocytes was found in PMSG/hCG-treated when compared to the non-stimulated gilts. The expression of BCL-2 and BAX mRNA, and BCL-2/BAX mRNA ratio was significantly higher in COCs derived from PMSG/hCG-treated when compared to PMSG/hCG + PGF2alpha-treated or non-stimulated subjects. The level of P4 in serum was similar in animals from all experimental groups, while its concentration in FF was greater in gilts subjected to PMSG/hCG treatment than in PMSG/hCG + PGF2alpha-stimulated and non-stimulated gilts. The concentration of E2 did not differ in the serum or FF between the control group and the hormonally stimulated groups.

Conclusions

Hormonal induction of estrus affected maternal effect gene transcripts levels in COCs and and oocyte nuclear maturation. The inclusion of PGF2alpha into the stimulation protocol enabled maintaining of physiological concentration of P4 in FF. Additionally, both hormonal treatments seem to be beneficial for apoptosis prevention through increasing BCL-2/BAX transcript ratio.
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Literature
1.
go back to reference Więsak T, Hunter MG, Foxcroft GR: Differences in follicular morphology, steroidogenesis and oocyte maturation in naturally cyclic and PMSG/hCG-treated prepubertal gilts. J Reprod Fertil. 1990, 89: 633-641. 10.1530/jrf.0.0890633.CrossRefPubMed Więsak T, Hunter MG, Foxcroft GR: Differences in follicular morphology, steroidogenesis and oocyte maturation in naturally cyclic and PMSG/hCG-treated prepubertal gilts. J Reprod Fertil. 1990, 89: 633-641. 10.1530/jrf.0.0890633.CrossRefPubMed
2.
go back to reference Zięcik AJ, Białłowicz M, Kaczmarek M, Demianowicz W, Rioperez J, Wasielak M, Bogacki M: Influence of estrous synchronization of prepubertal gilts on embryo quality. J Reprod Dev. 2005, 51: 379-384. 10.1262/jrd.17008.CrossRefPubMed Zięcik AJ, Białłowicz M, Kaczmarek M, Demianowicz W, Rioperez J, Wasielak M, Bogacki M: Influence of estrous synchronization of prepubertal gilts on embryo quality. J Reprod Dev. 2005, 51: 379-384. 10.1262/jrd.17008.CrossRefPubMed
3.
go back to reference Blitek A, Kaczmarek MM, Kiewisz J, Zięcik AJ: Endometrial and conceptus expression of HoxA10, transforming growth factor beta 1, leukemia inhibitory factor, and prostaglandin H synthase-2 in early pregnant pigs with gonadotropin-induced estrus. Domest Anim Endocrinol. 2010, 38: 222-234. 10.1016/j.domaniend.2009.11.001.CrossRefPubMed Blitek A, Kaczmarek MM, Kiewisz J, Zięcik AJ: Endometrial and conceptus expression of HoxA10, transforming growth factor beta 1, leukemia inhibitory factor, and prostaglandin H synthase-2 in early pregnant pigs with gonadotropin-induced estrus. Domest Anim Endocrinol. 2010, 38: 222-234. 10.1016/j.domaniend.2009.11.001.CrossRefPubMed
4.
go back to reference Martinat-Botté F, Venturi E, Guillouet P, Driancourt MA, Terqui M: Induction and synchronization of ovulations of nulliparous and multiparous sows with an injection of gonadotropin-releasing hormone agonist (receptal). Theriogenology. 2010, 73: 332-42. 10.1016/j.theriogenology.2009.09.017.CrossRefPubMed Martinat-Botté F, Venturi E, Guillouet P, Driancourt MA, Terqui M: Induction and synchronization of ovulations of nulliparous and multiparous sows with an injection of gonadotropin-releasing hormone agonist (receptal). Theriogenology. 2010, 73: 332-42. 10.1016/j.theriogenology.2009.09.017.CrossRefPubMed
5.
go back to reference Tong Z-B, Gold L, DePol A, Vanevski K, Dorward H, Sena P, Palumbo C, Bondy CA, Nelson NM: Developmental expression and subcellular localization of mouse MATER, an oocyte-specific protein essential for early development. Endocrinology. 2004, 145: 1427-1434. 10.1210/en.2003-1160.CrossRefPubMed Tong Z-B, Gold L, DePol A, Vanevski K, Dorward H, Sena P, Palumbo C, Bondy CA, Nelson NM: Developmental expression and subcellular localization of mouse MATER, an oocyte-specific protein essential for early development. Endocrinology. 2004, 145: 1427-1434. 10.1210/en.2003-1160.CrossRefPubMed
6.
go back to reference Pisani LF, Ramelli P, Lazzari B, Braglia S, Ceciliani F, Mariani P: Characterization of maternal antigen that embryos require (MATER/NLRP5) gene and protein in pig somatic tissues and germ cells. J Reprod Dev. 2010, 56: 41-48. 10.1262/jrd.09-098A.CrossRefPubMed Pisani LF, Ramelli P, Lazzari B, Braglia S, Ceciliani F, Mariani P: Characterization of maternal antigen that embryos require (MATER/NLRP5) gene and protein in pig somatic tissues and germ cells. J Reprod Dev. 2010, 56: 41-48. 10.1262/jrd.09-098A.CrossRefPubMed
7.
go back to reference Uzbekova S, Roy-Sabau M, Dalbiès-Tran R, Perreau C, Papillier P, Mompart F, Thelie A, Pennetier S, Cognie J, Cadoret V, Royere D, Monget P, Mermillod P: Zygote arrest 1 gene in the pig, cattle and human: evidence of different transcripts variants in male and female germ cells. Reprod Biol Endocrinol. 2006, 4: 12-10.1186/1477-7827-4-12.PubMedCentralCrossRefPubMed Uzbekova S, Roy-Sabau M, Dalbiès-Tran R, Perreau C, Papillier P, Mompart F, Thelie A, Pennetier S, Cognie J, Cadoret V, Royere D, Monget P, Mermillod P: Zygote arrest 1 gene in the pig, cattle and human: evidence of different transcripts variants in male and female germ cells. Reprod Biol Endocrinol. 2006, 4: 12-10.1186/1477-7827-4-12.PubMedCentralCrossRefPubMed
8.
go back to reference Tong Z-B, Gold L, Pfeifer KE, Dorward H, Lee E, Bondy CA, Dean J, Nelson NM: Mater, a maternal effect gene required for early embryonic development in mice. Nat Genet. 2000, 26: 267-268. 10.1038/81547.CrossRefPubMed Tong Z-B, Gold L, Pfeifer KE, Dorward H, Lee E, Bondy CA, Dean J, Nelson NM: Mater, a maternal effect gene required for early embryonic development in mice. Nat Genet. 2000, 26: 267-268. 10.1038/81547.CrossRefPubMed
9.
go back to reference Zheng P, Dean J: Role of Filia, a maternal effect gene, in maintaining euploidy during cleavage-stage mouse embryogenesis. Proc Natl Acad Sci U S A. 2009, 106: 7473-7478. 10.1073/pnas.0900519106.PubMedCentralCrossRefPubMed Zheng P, Dean J: Role of Filia, a maternal effect gene, in maintaining euploidy during cleavage-stage mouse embryogenesis. Proc Natl Acad Sci U S A. 2009, 106: 7473-7478. 10.1073/pnas.0900519106.PubMedCentralCrossRefPubMed
10.
go back to reference Sena P, Riccio M, Marzona L, Nicoli A, Marsella T, Marmiroli S, Bertacchini , Fano RA, La Salsa GB, De Pol A: Human MATER localization in specific cell domains of oocyte and follicular cells. Reprod Biomed Online. 2009, 2: 226-234.CrossRef Sena P, Riccio M, Marzona L, Nicoli A, Marsella T, Marmiroli S, Bertacchini , Fano RA, La Salsa GB, De Pol A: Human MATER localization in specific cell domains of oocyte and follicular cells. Reprod Biomed Online. 2009, 2: 226-234.CrossRef
11.
go back to reference Moore RK, Otsuka F, Shimasaki S: Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J Biol Chem. 2003, 278: 304-310.CrossRefPubMed Moore RK, Otsuka F, Shimasaki S: Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J Biol Chem. 2003, 278: 304-310.CrossRefPubMed
12.
go back to reference Zhu G, Bingran G, Pan D, Mu Y, Feng S: Expression of bone morphogenetic proteins and receptors in porcine cumulus-oocyte complexes during in vitro maturation. Anim Reprod Sci. 2008, 104: 275-283. 10.1016/j.anireprosci.2007.02.011.CrossRefPubMed Zhu G, Bingran G, Pan D, Mu Y, Feng S: Expression of bone morphogenetic proteins and receptors in porcine cumulus-oocyte complexes during in vitro maturation. Anim Reprod Sci. 2008, 104: 275-283. 10.1016/j.anireprosci.2007.02.011.CrossRefPubMed
13.
go back to reference Su YQ, Wu X, O’Brien MJ, Pendola FL, Denegre JN, Matzuk MM, Eppig JJ: Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev Biol. 2004, 276: 64-73. 10.1016/j.ydbio.2004.08.020.CrossRefPubMed Su YQ, Wu X, O’Brien MJ, Pendola FL, Denegre JN, Matzuk MM, Eppig JJ: Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev Biol. 2004, 276: 64-73. 10.1016/j.ydbio.2004.08.020.CrossRefPubMed
14.
go back to reference Kathirvel M, Soundian E, Kumanan V: Differential expression dynamic of growth differentiation factor 9 (GDF9) and bone morphogenetic factor 15 (BMP15) mRNA transcripts during in vitro maturation of buffalo (Bubalus bubalis) cumulus-oocyte complexes. SpringerPlus. 2013, 2: 206-10.1186/2193-1801-2-206.PubMedCentralCrossRefPubMed Kathirvel M, Soundian E, Kumanan V: Differential expression dynamic of growth differentiation factor 9 (GDF9) and bone morphogenetic factor 15 (BMP15) mRNA transcripts during in vitro maturation of buffalo (Bubalus bubalis) cumulus-oocyte complexes. SpringerPlus. 2013, 2: 206-10.1186/2193-1801-2-206.PubMedCentralCrossRefPubMed
15.
go back to reference Wu YT, Tang L, Cai J, Lu XE, Xu J, Zhu XM, Luo Q, Huang H-F: High bone morphogenetic protein-15 level in follicular fluid is associated with high quality oocyte and subsequent embryonic development. Hum Reprod. 2007, 22: 1526-1531. 10.1093/humrep/dem029.CrossRefPubMed Wu YT, Tang L, Cai J, Lu XE, Xu J, Zhu XM, Luo Q, Huang H-F: High bone morphogenetic protein-15 level in follicular fluid is associated with high quality oocyte and subsequent embryonic development. Hum Reprod. 2007, 22: 1526-1531. 10.1093/humrep/dem029.CrossRefPubMed
16.
go back to reference Gode F, Gulekli B, Dogan E, Korhan P, Dogan S, Bige O, Cimrin D, Atabey N: Influence of follicular fluid GDF9 and BMP15 on embryo quality. Fertil Steril. 2011, 95: 2274-2278. 10.1016/j.fertnstert.2011.03.045.CrossRefPubMed Gode F, Gulekli B, Dogan E, Korhan P, Dogan S, Bige O, Cimrin D, Atabey N: Influence of follicular fluid GDF9 and BMP15 on embryo quality. Fertil Steril. 2011, 95: 2274-2278. 10.1016/j.fertnstert.2011.03.045.CrossRefPubMed
17.
go back to reference Li HK, Kuo TY, Yang HS, Chen LR, Li SS, Huang HW: Differential gene expression of bone morphogenetic protein 15 and growth differentiation factor 9 during in vitro maturation of porcine oocytes and early embryos. Anim Reprod Sci. 2008, 103: 312-322. 10.1016/j.anireprosci.2006.12.017.CrossRefPubMed Li HK, Kuo TY, Yang HS, Chen LR, Li SS, Huang HW: Differential gene expression of bone morphogenetic protein 15 and growth differentiation factor 9 during in vitro maturation of porcine oocytes and early embryos. Anim Reprod Sci. 2008, 103: 312-322. 10.1016/j.anireprosci.2006.12.017.CrossRefPubMed
18.
go back to reference Thelie A, Papillier P, Perreau C, Uzbekova S, Hennequet-Antier C, Dalbies-Tran R: Regulation of bovine oocyte-specific transcripts during in vitro oocyte maturation and after maternal embryonic transition analyzed using a transcriptome approach. Mol Reprod Dev. 2009, 76: 773-782. 10.1002/mrd.21031.CrossRefPubMed Thelie A, Papillier P, Perreau C, Uzbekova S, Hennequet-Antier C, Dalbies-Tran R: Regulation of bovine oocyte-specific transcripts during in vitro oocyte maturation and after maternal embryonic transition analyzed using a transcriptome approach. Mol Reprod Dev. 2009, 76: 773-782. 10.1002/mrd.21031.CrossRefPubMed
19.
go back to reference Romar R, De Santis T, Papillier P, Perreau C, Thélie A, Dell’Aquila , Mermillod P, Dalbiés-Tran R: Expression of maternal transcripts during bovine oocyte in vitro maturation is affected be donor age. Reprod Domest Anim. 2011, 46: 23-30.CrossRef Romar R, De Santis T, Papillier P, Perreau C, Thélie A, Dell’Aquila , Mermillod P, Dalbiés-Tran R: Expression of maternal transcripts during bovine oocyte in vitro maturation is affected be donor age. Reprod Domest Anim. 2011, 46: 23-30.CrossRef
20.
go back to reference Sommer JR, Collins EB, Estrada JL, Petters RM: Synchronization and superovulation of mature cycling gilts for the collection of pronuclear stage embryos. Anim Reprod Sci. 2007, 100: 402-410. 10.1016/j.anireprosci.2006.10.010.PubMedCentralCrossRefPubMed Sommer JR, Collins EB, Estrada JL, Petters RM: Synchronization and superovulation of mature cycling gilts for the collection of pronuclear stage embryos. Anim Reprod Sci. 2007, 100: 402-410. 10.1016/j.anireprosci.2006.10.010.PubMedCentralCrossRefPubMed
21.
go back to reference Kuijk EW, du Puy L, van Tol HT, Haagsman HP, Colenbrander B, Roelen BA: Validation of reference genes for quantitative RT-PCR studies in porcine oocytes and preimplantation embryos. BMC Dev Biol. 2007, 7: 58-65. 10.1186/1471-213X-7-58.PubMedCentralCrossRefPubMed Kuijk EW, du Puy L, van Tol HT, Haagsman HP, Colenbrander B, Roelen BA: Validation of reference genes for quantitative RT-PCR studies in porcine oocytes and preimplantation embryos. BMC Dev Biol. 2007, 7: 58-65. 10.1186/1471-213X-7-58.PubMedCentralCrossRefPubMed
22.
go back to reference Wasielak M, Fujii T, Ohsaki T, Hashizume T, Bogacki M, Sawai K: Transcript abundance and apoptosis in day-7 porcine blastocyst cultured with exogenous insulin-like growth factor-I. Reprod Biol. 2013, 13: 58-65.CrossRefPubMed Wasielak M, Fujii T, Ohsaki T, Hashizume T, Bogacki M, Sawai K: Transcript abundance and apoptosis in day-7 porcine blastocyst cultured with exogenous insulin-like growth factor-I. Reprod Biol. 2013, 13: 58-65.CrossRefPubMed
23.
go back to reference Ju S, Rui R, Lu Q, Lin P, Guo H: Analysis of apoptosis and methyltransferase mRNA expression in porcine cloned embryos cultured in vitro. J Assist Reprod Genet. 2010, 27: 49-59. 10.1007/s10815-009-9378-7.PubMedCentralCrossRefPubMed Ju S, Rui R, Lu Q, Lin P, Guo H: Analysis of apoptosis and methyltransferase mRNA expression in porcine cloned embryos cultured in vitro. J Assist Reprod Genet. 2010, 27: 49-59. 10.1007/s10815-009-9378-7.PubMedCentralCrossRefPubMed
24.
go back to reference Walzel H, Brock J, Pöhland R, Vanselow J, Tomek W, Schneider F, Tiemann U: Effects of galectin-1 on regulation of progesterone production in granulosa cells from pig ovaries in vitro. Glycobiology. 2004, 14: 871-881. 10.1093/glycob/cwh101.CrossRefPubMed Walzel H, Brock J, Pöhland R, Vanselow J, Tomek W, Schneider F, Tiemann U: Effects of galectin-1 on regulation of progesterone production in granulosa cells from pig ovaries in vitro. Glycobiology. 2004, 14: 871-881. 10.1093/glycob/cwh101.CrossRefPubMed
25.
go back to reference Paradis F, Novak S, Murdoch GK, Dyck MK, Dixon WT, Foxcroft GR: Temporal regulation of BMP2, BMP6, BMP15, GDF9, BMPR1A, BMPR1B, BMPR2 and TGFBR1 mRNA expression in the oocyte, granulosa and theca cells of developing preovulatory follicles in the pig. Reproduction. 2009, 138: 115-129. 10.1530/REP-08-0538.CrossRefPubMed Paradis F, Novak S, Murdoch GK, Dyck MK, Dixon WT, Foxcroft GR: Temporal regulation of BMP2, BMP6, BMP15, GDF9, BMPR1A, BMPR1B, BMPR2 and TGFBR1 mRNA expression in the oocyte, granulosa and theca cells of developing preovulatory follicles in the pig. Reproduction. 2009, 138: 115-129. 10.1530/REP-08-0538.CrossRefPubMed
26.
go back to reference Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976, 72: 248-254. 10.1016/0003-2697(76)90527-3.CrossRefPubMed Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976, 72: 248-254. 10.1016/0003-2697(76)90527-3.CrossRefPubMed
27.
go back to reference Kiewisz J, Kaczmarek MM, Morawska E, Blitek A, Kapelański W, Zięcik AJ: Estrus synchronization affects WNT signaling in the porcine reproductive tract and embryos. Theriogenology. 2011, 76: 954-966. 10.1016/j.theriogenology.2011.05.002.CrossRefPubMed Kiewisz J, Kaczmarek MM, Morawska E, Blitek A, Kapelański W, Zięcik AJ: Estrus synchronization affects WNT signaling in the porcine reproductive tract and embryos. Theriogenology. 2011, 76: 954-966. 10.1016/j.theriogenology.2011.05.002.CrossRefPubMed
28.
go back to reference Guéripel X, Brun V, Gougeon A: Oocyte bone morphogenetic protein 15, but not growth differentiation factor 9, is increased during gonadotropin-induced follicular development in the immature mouse and is associated with cumulus oophorus expansion. Biol Reprod. 2006, 75: 836-843. 10.1095/biolreprod.106.055574.CrossRefPubMed Guéripel X, Brun V, Gougeon A: Oocyte bone morphogenetic protein 15, but not growth differentiation factor 9, is increased during gonadotropin-induced follicular development in the immature mouse and is associated with cumulus oophorus expansion. Biol Reprod. 2006, 75: 836-843. 10.1095/biolreprod.106.055574.CrossRefPubMed
29.
go back to reference Isom CS, Li RF, Whitworth KM, Prather RS: Timing of first embryonic cleavage is a positive indicator of the in vitro developmental potential of porcine embryos derived from in vitro fertilization, somatic cell nuclear transfer and parthenogenesis. Mol Reprod Dev. 2012, 79: 197-207. 10.1002/mrd.22013.CrossRefPubMed Isom CS, Li RF, Whitworth KM, Prather RS: Timing of first embryonic cleavage is a positive indicator of the in vitro developmental potential of porcine embryos derived from in vitro fertilization, somatic cell nuclear transfer and parthenogenesis. Mol Reprod Dev. 2012, 79: 197-207. 10.1002/mrd.22013.CrossRefPubMed
30.
go back to reference Shimada M, Terada T: FSH and LH induce progesterone production and progesterone receptor synthesis in cumulus cells: a requirement for meiotic resumption in porcine oocytes. Mol Hum Reprod. 2002, 8: 612-618. 10.1093/molehr/8.7.612.CrossRefPubMed Shimada M, Terada T: FSH and LH induce progesterone production and progesterone receptor synthesis in cumulus cells: a requirement for meiotic resumption in porcine oocytes. Mol Hum Reprod. 2002, 8: 612-618. 10.1093/molehr/8.7.612.CrossRefPubMed
31.
go back to reference Aparicio IM, Garcia-Herreros M, O’Shea LC, Hensey C, Lonergan P, Fair T: Expression, regulation, and function of progesterone receptors in bovine cumulus oocyte complexes during in vitro maturation. Biol Reprod. 2011, 84: 910-921. 10.1095/biolreprod.110.087411.CrossRefPubMed Aparicio IM, Garcia-Herreros M, O’Shea LC, Hensey C, Lonergan P, Fair T: Expression, regulation, and function of progesterone receptors in bovine cumulus oocyte complexes during in vitro maturation. Biol Reprod. 2011, 84: 910-921. 10.1095/biolreprod.110.087411.CrossRefPubMed
32.
go back to reference Dode MA, Graves C: Involvement of steroid hormones on in vitro maturation of pig oocytes. Theriogenology. 2002, 57: 811-821. 10.1016/S0093-691X(01)00700-2.CrossRefPubMed Dode MA, Graves C: Involvement of steroid hormones on in vitro maturation of pig oocytes. Theriogenology. 2002, 57: 811-821. 10.1016/S0093-691X(01)00700-2.CrossRefPubMed
33.
go back to reference Silva CC, Knight PG: Effects of androgens, progesterone and their antagonists on the developmental competence of in vitro matured bovine oocytes. J Reprod Fertil. 2000, 119: 261-269.CrossRefPubMed Silva CC, Knight PG: Effects of androgens, progesterone and their antagonists on the developmental competence of in vitro matured bovine oocytes. J Reprod Fertil. 2000, 119: 261-269.CrossRefPubMed
34.
go back to reference Abayasekara DR, Michael AE, Webley GE, Flint AP: Mode of action of prostaglandin F2 alpha in human luteinized granulosa cells: role of protein kinase C. Mol Cell Endocrinol. 1993, 97: 81-91. 10.1016/0303-7207(93)90213-4.CrossRefPubMed Abayasekara DR, Michael AE, Webley GE, Flint AP: Mode of action of prostaglandin F2 alpha in human luteinized granulosa cells: role of protein kinase C. Mol Cell Endocrinol. 1993, 97: 81-91. 10.1016/0303-7207(93)90213-4.CrossRefPubMed
35.
go back to reference Blitek A, Morawska-Pucinska E, Szymanska M, Krawczynski K, Ziecik A: Effect of estrus synchronization on luteal P4 synthesis in early pregnant gilts. Reprod Domest Anim. 2013, 48 (Suppl. 1): 72-124. Blitek A, Morawska-Pucinska E, Szymanska M, Krawczynski K, Ziecik A: Effect of estrus synchronization on luteal P4 synthesis in early pregnant gilts. Reprod Domest Anim. 2013, 48 (Suppl. 1): 72-124.
36.
go back to reference Dode MA, Graves CN: Role of estradiol-17β on nuclear and cytoplasmic maturation of pig oocytes. Anim Reprod Sci. 2003, 78: 99-110. 10.1016/S0378-4320(03)00080-0.CrossRefPubMed Dode MA, Graves CN: Role of estradiol-17β on nuclear and cytoplasmic maturation of pig oocytes. Anim Reprod Sci. 2003, 78: 99-110. 10.1016/S0378-4320(03)00080-0.CrossRefPubMed
37.
go back to reference Wang HF, Isobe N, Kumamoto K, Yamashiro H, Yamashita Y, Terada T: Studies of the role of steroid hormone in the regulation of oocyte maturation in cattle. Reprod Biol Endocrinol. 2006, 4: 4-10.1186/1477-7827-4-4.PubMedCentralCrossRefPubMed Wang HF, Isobe N, Kumamoto K, Yamashiro H, Yamashita Y, Terada T: Studies of the role of steroid hormone in the regulation of oocyte maturation in cattle. Reprod Biol Endocrinol. 2006, 4: 4-10.1186/1477-7827-4-4.PubMedCentralCrossRefPubMed
38.
go back to reference Chun SY, Billig H, Tilly JL, Furuta I, Tsafriri A, Hsueh AJ: Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous insulin-like growth factor I. Endocrinology. 1845–1853, 1994: 135- Chun SY, Billig H, Tilly JL, Furuta I, Tsafriri A, Hsueh AJ: Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous insulin-like growth factor I. Endocrinology. 1845–1853, 1994: 135-
39.
go back to reference Xiao CW, Ash K, Tsang BK: Nuclear factor- B-mediated X-linked inhibitor of apoptosis protein expression prevents rat granulosa cells from tumor necrosis factor-induced apoptosis. Endocrinology. 2001, 142: 557-563.PubMed Xiao CW, Ash K, Tsang BK: Nuclear factor- B-mediated X-linked inhibitor of apoptosis protein expression prevents rat granulosa cells from tumor necrosis factor-induced apoptosis. Endocrinology. 2001, 142: 557-563.PubMed
40.
go back to reference Robles R, Tao XJ, Trbovich AM, Maravel DV, Nahum R, Perez GI, Nahum R, Perez GI, Tilly KI, Tilly JL: Localization, regulation and possible consequences of apoptotic protease-activating factor-1 (Apaf-1) expression in granulosa cells of the mouse ovary. Endocrinology. 1999, 140: 2641-2644. 10.1210/endo.140.6.6931.CrossRefPubMed Robles R, Tao XJ, Trbovich AM, Maravel DV, Nahum R, Perez GI, Nahum R, Perez GI, Tilly KI, Tilly JL: Localization, regulation and possible consequences of apoptotic protease-activating factor-1 (Apaf-1) expression in granulosa cells of the mouse ovary. Endocrinology. 1999, 140: 2641-2644. 10.1210/endo.140.6.6931.CrossRefPubMed
41.
go back to reference Quirk SM, Cowan RG, Harman RM: Progesterone receptor and the cell cycle modulate apoptosis in granulosa cells. Endocrinology. 2004, 145: 5033-5043. 10.1210/en.2004-0140.CrossRefPubMed Quirk SM, Cowan RG, Harman RM: Progesterone receptor and the cell cycle modulate apoptosis in granulosa cells. Endocrinology. 2004, 145: 5033-5043. 10.1210/en.2004-0140.CrossRefPubMed
42.
go back to reference Salhab M, Tosca L, Cabau C, Papillier P, Perreau C, Dupont J, Mermillod P, Uzbekova S: Kinetics of gene expression and signaling in bovine cumulus cells throughout IVM in different mediums in relation to oocyte developmental competence, cumulus apoptosis and progesterone secretion. Theriogenology. 2011, 75: 90-104. 10.1016/j.theriogenology.2010.07.014.CrossRefPubMed Salhab M, Tosca L, Cabau C, Papillier P, Perreau C, Dupont J, Mermillod P, Uzbekova S: Kinetics of gene expression and signaling in bovine cumulus cells throughout IVM in different mediums in relation to oocyte developmental competence, cumulus apoptosis and progesterone secretion. Theriogenology. 2011, 75: 90-104. 10.1016/j.theriogenology.2010.07.014.CrossRefPubMed
43.
go back to reference Hussein TS, Froiland DA, Amato F, Thompson JG, Gilchrist RB: Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J Cell Sci. 2005, 18: 5257-5268.CrossRef Hussein TS, Froiland DA, Amato F, Thompson JG, Gilchrist RB: Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J Cell Sci. 2005, 18: 5257-5268.CrossRef
Metadata
Title
The effect of hormonal estrus induction on maternal effect and apoptosis-related genes expression in porcine cumulus-oocyte complexes
Authors
Marek Bogacki
Marta Wasielak
Anna Kitewska
Iwona Bogacka
Beenu Moza Jalali
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2014
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-12-32

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