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Published in: Journal of Assisted Reproduction and Genetics 8/2016

01-08-2016 | Epigenetics

Epigenetic alterations of CYP19A1 gene in Cumulus cells and its relevance to infertility in endometriosis

Authors: Elham Hosseini, Fereshteh Mehraein, Maryam Shahhoseini, Leili Karimian, Fatemeh Nikmard, Mahnaz Ashrafi, Parvaneh Afsharian, Reza Aflatoonian

Published in: Journal of Assisted Reproduction and Genetics | Issue 8/2016

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Abstract

Purpose

The purpose of the present study was to investigate the epigenetic mechanisms responsible for the aberrant aromatase expression (CYP19A1) in Cumulus Cells (CCs) of infertile endometriosis patients.

Method

Cumulus cells were obtained from 24 infertile patients with and without endometriosis who underwent ovarian stimulation for intracytoplasmic sperm injection. Expression of CYP19A1 gene was quantified using Reverse Transcription Q-PCR. DNA methylation, histone modifications, and binding of Estrogen Receptor, ERβ to regulatory DNA sequences of CYP19A1 gene were evaluated by Chromatin ImmunoPrecipitation (ChIP) assay.

Results

CYP19A1 gene expression in CCs of endometriosis patients was significantly lower than the control group (P = 0.04). Higher incorporation of MeCP2 (as a marker of DNA methylation) on PII and PI.4 promoters, and hypoacetylation at H3K9 in PII and hypermethylation at H3K9 in PI.4 were observed in CYP19A1 gene in endometriosis patients (P < 0.05). Moreover, a decreased level of ERβ binding to PII and an increased level of its binding to PI.3 and PI.4 promoters of CYP19A1 were observed in endometriosis patients when compared to control.

Conclusion

Significant reduction of CYP19A1 gene expression in CCs of endometriosis patients may be the result of epigenetic alterations in its regulatory regions, either by DNA methylation or histone modifications. These epigenetic changes along with differential binding of ERβ (as a transcription factor) in CYP19A1 promoters may impair follicular steroidogenesis, leading to poor Oocyte and embryo condition in endometriosis patients.
Literature
1.
go back to reference Kennedy S, Bergqvist A, Chapron C, D’Hooghe T, Dunselman G, Greb R, et al. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod. 2005;20(10):2698–704.CrossRefPubMed Kennedy S, Bergqvist A, Chapron C, D’Hooghe T, Dunselman G, Greb R, et al. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod. 2005;20(10):2698–704.CrossRefPubMed
2.
go back to reference Dunselman G, Vermeulen N, Becker C, Calhaz-Jorge C, D’Hooghe T, De Bie B, et al. ESHRE guideline: management of women with endometriosis. Hum Reprod. 2014;29(3):400–12.CrossRefPubMed Dunselman G, Vermeulen N, Becker C, Calhaz-Jorge C, D’Hooghe T, De Bie B, et al. ESHRE guideline: management of women with endometriosis. Hum Reprod. 2014;29(3):400–12.CrossRefPubMed
3.
go back to reference Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A. Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril. 2008;90(2):247–57.CrossRefPubMed Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A. Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril. 2008;90(2):247–57.CrossRefPubMed
4.
go back to reference Garrido Ns, Navarro J, Remohà J, SimÃ3n C, Pellicer A. Follicular hormonal environment and embryo quality in women with endometriosis. Human reproduction update 2000;6(1):67-74. Garrido Ns, Navarro J, Remohí J, SimÃ3n C, Pellicer A. Follicular hormonal environment and embryo quality in women with endometriosis. Human reproduction update 2000;6(1):67-74.
5.
go back to reference Hsu AL, Townsend PM, Oehninger S, Castora FJ. Endometriosis may be associated with mitochondrial dysfunction in cumulus cells from subjects undergoing in vitro fertilization-intracytoplasmic sperm injection, as reflected by decreased adenosine triphosphate production. Fertil Stril. 2015;103(2):347–52. e1.CrossRef Hsu AL, Townsend PM, Oehninger S, Castora FJ. Endometriosis may be associated with mitochondrial dysfunction in cumulus cells from subjects undergoing in vitro fertilization-intracytoplasmic sperm injection, as reflected by decreased adenosine triphosphate production. Fertil Stril. 2015;103(2):347–52. e1.CrossRef
6.
go back to reference Wang J, Shen X, Huang X, Zhao Z. Follicular fluid levels of prostaglandin E2 and the effect of prostaglandin E2 on steroidogenesis in granulosa-lutein cells in women with moderate and severe endometriosis undergoing in vitro fertilization and embryo transfer. Chin Med J. 2012;125(22):3985–90.PubMed Wang J, Shen X, Huang X, Zhao Z. Follicular fluid levels of prostaglandin E2 and the effect of prostaglandin E2 on steroidogenesis in granulosa-lutein cells in women with moderate and severe endometriosis undergoing in vitro fertilization and embryo transfer. Chin Med J. 2012;125(22):3985–90.PubMed
8.
go back to reference Pellicer A, Oliveira N, Ruiz A, Remohí J, Simón C. Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction. Hum Reprod. 1995;10 suppl 2:91–7.CrossRefPubMed Pellicer A, Oliveira N, Ruiz A, Remohí J, Simón C. Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction. Hum Reprod. 1995;10 suppl 2:91–7.CrossRefPubMed
9.
go back to reference Albertini DF, Combelles C, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121(5):647–53.CrossRefPubMed Albertini DF, Combelles C, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121(5):647–53.CrossRefPubMed
10.
go back to reference Huang Z, Wells D. The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Mol Hum Reprod. 2010;16(10):715–25.CrossRefPubMed Huang Z, Wells D. The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Mol Hum Reprod. 2010;16(10):715–25.CrossRefPubMed
11.
go back to reference Egea RR, Puchalt NG, Escrivá MM, Varghese AC. OMICS: current and future perspectives in reproductive medicine and technology. J Hum Reprod Sci. 2014;7(2):73.CrossRefPubMedPubMedCentral Egea RR, Puchalt NG, Escrivá MM, Varghese AC. OMICS: current and future perspectives in reproductive medicine and technology. J Hum Reprod Sci. 2014;7(2):73.CrossRefPubMedPubMedCentral
12.
go back to reference Gasca S, Pellestor F, Assou S, Loup V, Anahory T, Dechaud H, et al. Identifying new human oocyte marker genes: a microarray approach. Reprod Biomed Online. 2007;14(2):175–83.CrossRefPubMedPubMedCentral Gasca S, Pellestor F, Assou S, Loup V, Anahory T, Dechaud H, et al. Identifying new human oocyte marker genes: a microarray approach. Reprod Biomed Online. 2007;14(2):175–83.CrossRefPubMedPubMedCentral
13.
go back to reference Hamel M, Dufort I, Robert C, Gravel C, Leveille M-C, Leader A, et al. Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod. 2008;23(5):1118–27.CrossRefPubMed Hamel M, Dufort I, Robert C, Gravel C, Leveille M-C, Leader A, et al. Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod. 2008;23(5):1118–27.CrossRefPubMed
14.
go back to reference Feuerstein P, Cadoret V, Dalbies-Tran R, Guerif F, Bidault R, Royere D. Gene expression in human cumulus cells: one approach to oocyte competence. Hum Reprod. 2007;22(12):3069–77.CrossRefPubMed Feuerstein P, Cadoret V, Dalbies-Tran R, Guerif F, Bidault R, Royere D. Gene expression in human cumulus cells: one approach to oocyte competence. Hum Reprod. 2007;22(12):3069–77.CrossRefPubMed
15.
go back to reference Lucidi P, BernabÃ2 N, Turriani M, Barboni B, Mattioli M. Cumulus cells steroidogenesis is influenced by the degree of oocyte maturation. Reprod Biol Endocrinol 2003;1:45. Lucidi P, BernabÃ2 N, Turriani M, Barboni B, Mattioli M. Cumulus cells steroidogenesis is influenced by the degree of oocyte maturation. Reprod Biol Endocrinol 2003;1:45.
16.
go back to reference Fisher CR, Graves KH, Parlow AF, Simpson ER. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci. 1998;95(12):6965–70.CrossRefPubMedPubMedCentral Fisher CR, Graves KH, Parlow AF, Simpson ER. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci. 1998;95(12):6965–70.CrossRefPubMedPubMedCentral
17.
go back to reference Pelletier G, El-Alfy M. Immunocytochemical localization of estrogen receptors α and β in the human reproductive organs. J Clin Endocrinol Metab. 2000;85(12):4835–40.PubMed Pelletier G, El-Alfy M. Immunocytochemical localization of estrogen receptors α and β in the human reproductive organs. J Clin Endocrinol Metab. 2000;85(12):4835–40.PubMed
19.
go back to reference Zhuang L-Z, Adashi EY, Hsueh AJ. Direct enhancement of gonadotropin-stimulated ovarian estrogen biosynthesis by estrogen and clomiphene citrate. Endocrinology. 1982;110(6):2219–21.CrossRefPubMed Zhuang L-Z, Adashi EY, Hsueh AJ. Direct enhancement of gonadotropin-stimulated ovarian estrogen biosynthesis by estrogen and clomiphene citrate. Endocrinology. 1982;110(6):2219–21.CrossRefPubMed
20.
go back to reference Katz-Jaffe MG, Surrey ES, Minjarez DA, Gustofson RL, Stevens JM, Schoolcraft WB. Association of abnormal ovarian reserve parameters with a higher incidence of aneuploid blastocysts. Obstet Gynecol. 2013;121(1):71–7.CrossRefPubMed Katz-Jaffe MG, Surrey ES, Minjarez DA, Gustofson RL, Stevens JM, Schoolcraft WB. Association of abnormal ovarian reserve parameters with a higher incidence of aneuploid blastocysts. Obstet Gynecol. 2013;121(1):71–7.CrossRefPubMed
21.
go back to reference Conley A, Mapes S, Corbin C, Greger D, Walters K, Trant J, et al. A comparative approach to structure-function studies of mammalian aromatases. J Steroid Biochem Mol Biol. 2001;79(1):289–97.CrossRefPubMed Conley A, Mapes S, Corbin C, Greger D, Walters K, Trant J, et al. A comparative approach to structure-function studies of mammalian aromatases. J Steroid Biochem Mol Biol. 2001;79(1):289–97.CrossRefPubMed
22.
go back to reference Sebastian S, Bulun SE. A highly complex organization of the regulatory region of the human CYP19 (aromatase) gene revealed by the human genome project. J Clin Endocrinol Metab. 2001;86(10):4600–2.CrossRefPubMed Sebastian S, Bulun SE. A highly complex organization of the regulatory region of the human CYP19 (aromatase) gene revealed by the human genome project. J Clin Endocrinol Metab. 2001;86(10):4600–2.CrossRefPubMed
23.
go back to reference Bulun SE, Lin Z, Imir G, Amin S, Demura M, Yilmaz B, et al. Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol Rev. 2005;57(3):359–83.CrossRefPubMed Bulun SE, Lin Z, Imir G, Amin S, Demura M, Yilmaz B, et al. Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol Rev. 2005;57(3):359–83.CrossRefPubMed
24.
go back to reference Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, et al. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev. 1994;15(3):342–55.PubMed Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, et al. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev. 1994;15(3):342–55.PubMed
25.
26.
go back to reference Barcelos IDE, Donabella FC, Ribas CP, Meola J, Ferriani RA, de Paz CCP, et al. Down-regulation of the CYP19A1 gene in cumulus cells of infertile women with endometriosis. RBM Online. 2015;30(5):532–41.PubMed Barcelos IDE, Donabella FC, Ribas CP, Meola J, Ferriani RA, de Paz CCP, et al. Down-regulation of the CYP19A1 gene in cumulus cells of infertile women with endometriosis. RBM Online. 2015;30(5):532–41.PubMed
27.
go back to reference Magli MC, Jones GM, Lundin K, Van den Abbeel E. Atlas of human embryology: from oocytes to preimplantation embryos. Hum Reprod. 2012;27:1.CrossRef Magli MC, Jones GM, Lundin K, Van den Abbeel E. Atlas of human embryology: from oocytes to preimplantation embryos. Hum Reprod. 2012;27:1.CrossRef
28.
go back to reference Mönkkönen KS, Aflatoonian R, Lee K-F, Yeung WS, Tsao S-W, Laitinen JT, et al. Localization and variable expression of Gαi2 in human endometrium and fallopian tubes. Hum Reprod. 2007;22(5):1224–30.CrossRefPubMed Mönkkönen KS, Aflatoonian R, Lee K-F, Yeung WS, Tsao S-W, Laitinen JT, et al. Localization and variable expression of Gαi2 in human endometrium and fallopian tubes. Hum Reprod. 2007;22(5):1224–30.CrossRefPubMed
29.
go back to reference Mönkkönen KS, Aflatoonian R, Lee K-F, Yeung WS, Tsao S-W, Laitinen JT, et al. Hormonal regulation of Gαi2 and mPRα in immortalized human oviductal cell line OE-E6/E7. MHR. 2007;13(12):845–51.CrossRefPubMed Mönkkönen KS, Aflatoonian R, Lee K-F, Yeung WS, Tsao S-W, Laitinen JT, et al. Hormonal regulation of Gαi2 and mPRα in immortalized human oviductal cell line OE-E6/E7. MHR. 2007;13(12):845–51.CrossRefPubMed
31.
go back to reference Lu X, Wu Y, Gao X-H, Wang Y-W, Wang L, Sun X-X. Effect of letrozole on estradiol production and P450 aromatase messenger RNA expression of cultured luteinized granulosa cells from women with and without endometriosis. Fertil Steril. 2012;98(1):131–5.CrossRefPubMed Lu X, Wu Y, Gao X-H, Wang Y-W, Wang L, Sun X-X. Effect of letrozole on estradiol production and P450 aromatase messenger RNA expression of cultured luteinized granulosa cells from women with and without endometriosis. Fertil Steril. 2012;98(1):131–5.CrossRefPubMed
32.
go back to reference Harlow C, Cahill D, Maile L, Talbot W, Mears J, Wardle P, et al. Reduced preovulatory granulosa cell steroidogenesis in women with endometriosis. J Clin Endocrinol Metab. 1996;81(1):426–9.PubMed Harlow C, Cahill D, Maile L, Talbot W, Mears J, Wardle P, et al. Reduced preovulatory granulosa cell steroidogenesis in women with endometriosis. J Clin Endocrinol Metab. 1996;81(1):426–9.PubMed
33.
go back to reference De Abreu LG, Romã£O GS, Reis RMD, Ferriani RA, de Sã¡ MFS, Moura MD. Reduced aromatase activity in granulosa cells of women with endometriosis undergoing assisted reproduction techniques. Gynecol Endocrinol. 2006;22(8):432–6.CrossRefPubMed De Abreu LG, Romã£O GS, Reis RMD, Ferriani RA, de Sã¡ MFS, Moura MD. Reduced aromatase activity in granulosa cells of women with endometriosis undergoing assisted reproduction techniques. Gynecol Endocrinol. 2006;22(8):432–6.CrossRefPubMed
34.
go back to reference De Abreu LG, Silveira VS, Scrideli CA, Ramos ES, Dos Reis RM, Ferriani RA, et al. Endometriosis does not alter aromatase gene expression (CYP19A1) in mural lutein-granulosa cells of women undergoing assisted reproduction techniques—a pilot study. J Endometriosis. 2011;3(4):177–82. De Abreu LG, Silveira VS, Scrideli CA, Ramos ES, Dos Reis RM, Ferriani RA, et al. Endometriosis does not alter aromatase gene expression (CYP19A1) in mural lutein-granulosa cells of women undergoing assisted reproduction techniques—a pilot study. J Endometriosis. 2011;3(4):177–82.
35.
36.
go back to reference Nan X, Ng H-H, Johnson CA, Laherty CD, Turner BM, Eisenman RN, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature. 1998;393(6683):386–9.CrossRefPubMed Nan X, Ng H-H, Johnson CA, Laherty CD, Turner BM, Eisenman RN, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature. 1998;393(6683):386–9.CrossRefPubMed
37.
go back to reference Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, Klein F, et al. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell. 1992;69(6):905–14.CrossRefPubMed Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, Klein F, et al. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell. 1992;69(6):905–14.CrossRefPubMed
38.
go back to reference Fo F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem. 2003;278(6):4035–40.CrossRef Fo F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem. 2003;278(6):4035–40.CrossRef
39.
40.
go back to reference Fischer JJ, Toedling J, Krueger T, Schueler M, Huber W, Sperling S. Combinatorial effects of four histone modifications in transcription and differentiation. Genomics. 2008;91(1):41–51.CrossRefPubMed Fischer JJ, Toedling J, Krueger T, Schueler M, Huber W, Sperling S. Combinatorial effects of four histone modifications in transcription and differentiation. Genomics. 2008;91(1):41–51.CrossRefPubMed
41.
go back to reference Adashi E, Hsueh A. Estrogens augment the stimulation of ovarian aromatase activity by follicle-stimulating hormone in cultured rat granulosa cells. J Biol Chem. 1982;257(11):6077–83.PubMed Adashi E, Hsueh A. Estrogens augment the stimulation of ovarian aromatase activity by follicle-stimulating hormone in cultured rat granulosa cells. J Biol Chem. 1982;257(11):6077–83.PubMed
43.
go back to reference Bréard E, Roussel H, Lindet Y, Mittre H, Leymarie P. Presence of exon I. 4 mRNA from CYP19 gene in human granulosa cells. Mol Cell Endocrinol. 1999;154(1):187–90.CrossRefPubMed Bréard E, Roussel H, Lindet Y, Mittre H, Leymarie P. Presence of exon I. 4 mRNA from CYP19 gene in human granulosa cells. Mol Cell Endocrinol. 1999;154(1):187–90.CrossRefPubMed
44.
45.
go back to reference Dago DN, Scafoglio C, Rinaldi A, Memoli D, Giurato G, Nassa G, et al. Estrogen receptor beta impacts hormone-induced alternative mRNA splicing in breast cancer cells. BMC Genomics. 2015;16(1):367.CrossRefPubMedPubMedCentral Dago DN, Scafoglio C, Rinaldi A, Memoli D, Giurato G, Nassa G, et al. Estrogen receptor beta impacts hormone-induced alternative mRNA splicing in breast cancer cells. BMC Genomics. 2015;16(1):367.CrossRefPubMedPubMedCentral
46.
go back to reference Bulun SE, Monsivais D, Kakinuma T, Furukawa Y, Bernardi L, Pavone ME, et al. Molecular biology of endometriosis: from aromatase to genomic abnormalities. Semin Reprod Med. 2015;2015:220–4. Bulun SE, Monsivais D, Kakinuma T, Furukawa Y, Bernardi L, Pavone ME, et al. Molecular biology of endometriosis: from aromatase to genomic abnormalities. Semin Reprod Med. 2015;2015:220–4.
47.
go back to reference Mahdian S, Aflatoonian R, Yazdi RS, Yaghmaei P, Ramazanali F, Afsharian P, et al. Macrophage migration inhibitory factor as a potential biomarker of endometriosis. Fertil Steril. 2015;103(1):153–9. e3.CrossRefPubMed Mahdian S, Aflatoonian R, Yazdi RS, Yaghmaei P, Ramazanali F, Afsharian P, et al. Macrophage migration inhibitory factor as a potential biomarker of endometriosis. Fertil Steril. 2015;103(1):153–9. e3.CrossRefPubMed
48.
go back to reference Simon C, Gutierrez A, Vidal A, De los Santos M, Tarin J, Remohi J, et al. Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod. 1994;9(4):725–9.PubMed Simon C, Gutierrez A, Vidal A, De los Santos M, Tarin J, Remohi J, et al. Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod. 1994;9(4):725–9.PubMed
49.
go back to reference Pellicer A, Navarro J, Bosch E, Garrido N, Garcia‐Velasco JA, Remohí J, et al. Endometrial quality in infertile women with endometriosis. Ann N Y Acad Sci. 2001;943(1):122–30.CrossRefPubMed Pellicer A, Navarro J, Bosch E, Garrido N, Garcia‐Velasco JA, Remohí J, et al. Endometrial quality in infertile women with endometriosis. Ann N Y Acad Sci. 2001;943(1):122–30.CrossRefPubMed
50.
go back to reference Hammes SR. Steroids and oocyte maturation—a new look at an old story. Mol Endocrinol. 2004;18(4):769–75.CrossRefPubMed Hammes SR. Steroids and oocyte maturation—a new look at an old story. Mol Endocrinol. 2004;18(4):769–75.CrossRefPubMed
51.
go back to reference Tesarik J, Mendoza C. Nongenomic effects of 17 beta-estradiol on maturing human oocytes: relationship to oocyte developmental potential. J Clin Endocrinol Metab. 1995;80(4):1438–43.PubMed Tesarik J, Mendoza C. Nongenomic effects of 17 beta-estradiol on maturing human oocytes: relationship to oocyte developmental potential. J Clin Endocrinol Metab. 1995;80(4):1438–43.PubMed
52.
go back to reference Dumesic DA, Meldrum DR, Katz-Jaffe MG, Krisher RL, Schoolcraft WB. Oocyte environment: follicular fluid and cumulus cells are critical for oocyte health. Fertil Stril. 2015;103(2):303–16.CrossRef Dumesic DA, Meldrum DR, Katz-Jaffe MG, Krisher RL, Schoolcraft WB. Oocyte environment: follicular fluid and cumulus cells are critical for oocyte health. Fertil Stril. 2015;103(2):303–16.CrossRef
53.
go back to reference Neal MS, Younglai EV, Holloway AC, Foster WG. Aromatase activity in granulosa cells as a predictor of pregnancy potential. International Congress Series; 2004: Elsevier B.V.; 2004. p. 139–42. doi:10.1016/j.ics 2004.05.022. Neal MS, Younglai EV, Holloway AC, Foster WG. Aromatase activity in granulosa cells as a predictor of pregnancy potential. International Congress Series; 2004: Elsevier B.V.; 2004. p. 139–42. doi:10.​1016/​j.​ics 2004.​05.​022.
54.
go back to reference Peña JE, Chang PL, Chan L-K, Zeitoun K, Thornton MH, Sauer MV. Supraphysiological estradiol levels do not affect oocyte and embryo quality in oocyte donation cycles. Hum Reprod. 2002;17(1):83–7.CrossRefPubMed Peña JE, Chang PL, Chan L-K, Zeitoun K, Thornton MH, Sauer MV. Supraphysiological estradiol levels do not affect oocyte and embryo quality in oocyte donation cycles. Hum Reprod. 2002;17(1):83–7.CrossRefPubMed
55.
go back to reference Brizek CL, Schlaff S, Pellegrini VA, Frank JB, Worrilow KC. Increased incidence of aberrant morphological phenotypes in human embryogenesis—an association with endometriosis. J Assist Reprod Genet. 1995;12(2):106–12.CrossRefPubMed Brizek CL, Schlaff S, Pellegrini VA, Frank JB, Worrilow KC. Increased incidence of aberrant morphological phenotypes in human embryogenesis—an association with endometriosis. J Assist Reprod Genet. 1995;12(2):106–12.CrossRefPubMed
56.
go back to reference Sanchez AM, Somigliana E, Vercellini P, Pagliardini L, Candiani M, Vigano P. Endometriosis as a detrimental condition for granulosa cell steroidogenesis and development: from molecular alterations to clinical impact. J Steroid Biochem Mol Biol. 2016;155:35–46.CrossRefPubMed Sanchez AM, Somigliana E, Vercellini P, Pagliardini L, Candiani M, Vigano P. Endometriosis as a detrimental condition for granulosa cell steroidogenesis and development: from molecular alterations to clinical impact. J Steroid Biochem Mol Biol. 2016;155:35–46.CrossRefPubMed
Metadata
Title
Epigenetic alterations of CYP19A1 gene in Cumulus cells and its relevance to infertility in endometriosis
Authors
Elham Hosseini
Fereshteh Mehraein
Maryam Shahhoseini
Leili Karimian
Fatemeh Nikmard
Mahnaz Ashrafi
Parvaneh Afsharian
Reza Aflatoonian
Publication date
01-08-2016
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 8/2016
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-016-0727-z

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