Estrogen disorders: Interpreting the abnormal regulation of aromatase in granulosa cells (Review)
- Authors:
- Ting Liu
- Yifei Huang
- Hui Lin
-
Affiliations: Department of Pathophysiology, School of Basic Medicine Sciences, Nanchang University, Nanchang, Jiangxi 330006, P.R. China, First Clinical Medical School, Nanchang University, Nanchang, Jiangxi 330006, P.R. China - Published online on: March 2, 2021 https://doi.org/10.3892/ijmm.2021.4906
- Article Number: 73
-
Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Mendelson CR, Jiang B, Shelton JM, Richardson JA and Hinshelwood MM: Transcriptional regulation of aromatase in placenta and ovary. J Steroid Biochem Mol Biol. 95:25–33. 2005. View Article : Google Scholar : PubMed/NCBI | |
Li J and Gibbs RB: Detection of estradiol in rat brain tissues: Contribution of local versus systemic production. Psychoneuroendocrinology. 102:84–94. 2019. View Article : Google Scholar | |
Lambard S, Silandre D, Delalande C, Denis-Galeraud I, Bourguiba S and Carreau S: Aromatase in testis: Expression and role in male reproduction. J Steroid Biochem Mol Biol. 95:63–69. 2005. View Article : Google Scholar : PubMed/NCBI | |
Mahendroo MS, Mendelson CR and Simpson ER: Tissue-specific and hormonally controlled alternative promoters regulate aromatase cytochrome P450 gene expression in human adipose tissue. J Biol Chem. 268:19463–19470. 1993. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Pan P, Li X, Zhu Q, Huang T and Ge RS: Food components and environmental chemicals of inhibiting human placental aromatase. Food Chem Toxicol. 128:46–53. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ai A, Tang Z, Liu Y, Yu S, Li B, Huang H, Wang X, Cao Y and Zhang W: Characterization and identification of human immortalized granulosa cells derived from ovarian follicular fluid. Exp Ther Med. 18:2167–2177. 2019.PubMed/NCBI | |
Shoham Z, Jacobs HS and Insler V: Luteinizing hormone: Its role, mechanism of action, and detrimental effects when hyper-secreted during the follicular phase. Fertil Steril. 59:1153–1161. 1993. View Article : Google Scholar : PubMed/NCBI | |
Nelson LR and Bulun SE: Estrogen production and action. J Am Acad Dermatol. 45(Suppl 3): pp. S116–S124. 2001, View Article : Google Scholar | |
Slominski A, Zbytek B, Nikolakis G, Manna PR, Skobowiat C, Zmijewski M, Li W, Janjetovic Z, Postlethwaite A, Zouboulis CC and Tuckey RC: Steroidogenesis in the skin: Implications for local immune functions. J Steroid Biochem Mol Biol. 137:107–123. 2013. View Article : Google Scholar : PubMed/NCBI | |
Bulun SE, Chen D, Moy I, Brooks DC and Zhao H: Aromatase, breast cancer and obesity: A complex interaction. Trends Endocrinol Metab. 23:83–89. 2012. View Article : Google Scholar : | |
Zhao H, Zhou L, Shangguan AJ and Bulun SE: Aromatase expression and regulation in breast and endometrial cancer. J Mol Endocrinol. 57:R19–R33. 2016. View Article : Google Scholar : PubMed/NCBI | |
Shozu M, Zhao Y and Simpson ER: TGF-beta1 stimulates expression of the aromatase (CYP19) gene in human osteoblast-like cells and THP-1 cells. Mol Cell Endocrinol. 160:123–133. 2000. View Article : Google Scholar : PubMed/NCBI | |
Stocco C: Aromatase expression in the ovary: Hormonal and molecular regulation. Steroids. 73:473–487. 2008. View Article : Google Scholar : PubMed/NCBI | |
Bulun SE, Chen D, Lu M, Zhao H, Cheng Y, Demura M, Yilmaz B, Martin R, Utsunomiya H, Thung S, et al: Aromatase excess in cancers of breast, endometrium and ovary. J Steroid Biochem Mol Biol. 106:81–96. 2007. View Article : Google Scholar : PubMed/NCBI | |
Bulun SE and Simpson ER: Aromatase expression in women's cancers. Adv Exp Med Biol. 630:112–132. 2008. View Article : Google Scholar : PubMed/NCBI | |
Sharma D, Ghai S and Singh D: Different promoter usage for CYP19 gene expression in buffalo ovary and placenta. Gen Comp Endocrinol. 162:319–328. 2009. View Article : Google Scholar : PubMed/NCBI | |
Solak KA, Wijnolts FMJ, Nijmeijer SM, Blaauboer BJ, van den Berg M and van Duursen MBM: Excessive levels of diverse phytoestrogens can modulate steroidogenesis and cell migration of KGN human granulosa-derived tumor cells. Toxicol Rep. 1:360–372. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ghosh S, Wu Y, Li R and Hu Y: Jun proteins modulate the ovary-specific promoter of aromatase gene in ovarian granulosa cells via a cAMP-responsive element. Oncogene. 24:2236–2246. 2005. View Article : Google Scholar : PubMed/NCBI | |
Li Q, Du X, Pan Z, Zhang L and Li Q: The transcription factor SMAD4 and miR-10b contribute to E2 release and cell apoptosis in ovarian granulosa cells by targeting CYP19A1. Mol Cell Endocrinol. 476:84–95. 2018. View Article : Google Scholar : PubMed/NCBI | |
Andrieu T, Féral C, Joubert M, Benhaim A and Mittre H: The absence of a functional nuclear receptor element A (NREA) in the promoter II of the aromatase P450 gene in rabbit granulosa cells. J Steroid Biochem Mol Biol. 101:127–135. 2006. View Article : Google Scholar : PubMed/NCBI | |
Boerboom D, Kerban A and Sirois J: Dual regulation of promoter II- and promoter 1f-derived cytochrome P450 aromatase transcripts in equine granulosa cells during human chorionic gonadotropin-induced ovulation: A novel model for the study of aromatase promoter switching. Endocrinology. 140:4133–4141. 1999. View Article : Google Scholar : PubMed/NCBI | |
Simpson ER: Sources of estrogen and their importance. J Steroid Biochem Mol Biol. 86:225–230. 2003. View Article : Google Scholar : PubMed/NCBI | |
Miyoshi T, Otsuka F and Shimasaki S: GRK-6 mediates FSH action synergistically enhanced by estrogen and the oocyte in rat granulosa cells. Biochem Biophys Res Commun. 434:401–406. 2013. View Article : Google Scholar : PubMed/NCBI | |
Czajka-Oraniec I and Simpson ER: Aromatase research and its clinical significance. Endokrynol Pol. 61:126–134. 2010.PubMed/NCBI | |
Velthut-Meikas A, Simm J, Tuuri T, Tapanainen JS, Metsis M and Salumets A: Research resource: Small RNA-seq of human granulosa cells reveals miRNAs in FSHR and aromatase genes. Mol Endocrinol. 27:1128–1141. 2013. View Article : Google Scholar : PubMed/NCBI | |
Mlodawska W and Slomczynska M: Immunohistochemical localization of aromatase during the development and atresia of ovarian follicles in prepubertal horses. Theriogenology. 74:1707–1712. 2010. View Article : Google Scholar : PubMed/NCBI | |
Naganuma H, Ohtani H, Harada N and Nagura H: Immunoelectron microscopic localization of aromatase in human placenta and ovary using microwave fixation. J Histochem Cytochem. 38:1427–1432. 1990. View Article : Google Scholar : PubMed/NCBI | |
Shaikh AA: Estrone and estradiol levels in the ovarian venous blood from rats during the estrous cycle and pregnancy. Biol Reprod. 5:297–307. 1971. View Article : Google Scholar : PubMed/NCBI | |
Szymańska K, Kałafut J, Przybyszewska A, Paziewska B, Adamczuk G, Kiełbus M and Rivero-Müller A: FSHR trans-activation and oligomerization. Front Endocrinol (Lausanne). 9:7602018. View Article : Google Scholar | |
Jiang C, Hou X, Wang C, May JV, Butnev VY, Bousfield GR and Davis JS: Hypoglycosylated hFSH has greater bioactivity than fully glycosylated recombinant hFSH in human granulosa cells. J Clin Endocrinol Metab. 100:E852–E860. 2015. View Article : Google Scholar : PubMed/NCBI | |
Hobeika E, Armouti M, Kala H, Fierro MA, Winston NJ, Scoccia B, Zamah AM and Stocco C: Oocyte-secreted factors synergize with FSH to promote aromatase expression in primary human cumulus cells. J Clin Endocrinol Metab. 104:1667–1676. 2019. View Article : Google Scholar : | |
Parakh TN, Hernandez JA, Grammer JC, Weck J, Hunzicker- Dunn M, Zeleznik AJ and Nilson JH: Follicle-stimulating hormone/cAMP regulation of aromatase gene expression requires beta-catenin. Proc Natl Acad Sci USA. 103:12435–12440. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kwintkiewicz J, Cai Z and Stocco C: Follicle-stimulating hormone-induced activation of Gata4 contributes in the up-regulation of Cyp19 expression in rat granulosa cells. Mol Endocrinol. 21:933–947. 2007. View Article : Google Scholar : PubMed/NCBI | |
Hong Y, Li H, Yuan YC and Chen S: Molecular characterization of aromatase. Ann N Y Acad Sci. 1155:112–120. 2009. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Gao D, Xu T, Adur MK, Zhang L, Luo L, Zhu T, Tong X, Zhang D, Wang Y, et al: Anti-Müllerian hormone inhibits luteinizing hormone-induced androstenedione synthesis in porcine theca cells. Theriogenology. 142:421–432. 2020. View Article : Google Scholar | |
Fang Y, Wang B, Lyu S, Zhang K, Cheng Q and Zhu Y: Virus analog decreases estradiol secretion in FSH-treated human ovarian granulosa cells. Gynecol Endocrinol. 36:346–350. 2020. View Article : Google Scholar | |
Kajitani T, Liu S, Maruyama T, Uchida H, Sakurai R, Masuda H, Nagashima T, Ono M, Arase T and Yoshimura Y: Analysis of serum FSH bioactivity in a patient with an FSH-secreting pituitary microadenoma and multicystic ovaries: A case report. Hum Reprod. 23:435–439. 2008. View Article : Google Scholar | |
Shi J, Yoshino O, Osuga Y, Koga K, Hirota Y, Nose E, Nishii O, Yano T and Taketani Y: Bone morphogenetic protein-2 (BMP-2) increases gene expression of FSH receptor and aromatase and decreases gene expression of LH receptor and StAR in human granulosa cells. Am J Reprod Immunol. 65:421–427. 2011. View Article : Google Scholar | |
Shi J, Yoshino O, Osuga Y, Koga K, Hirota Y, Hirata T, Yano T, Nishii O and Taketani Y: Bone morphogenetic protein-6 stimulates gene expression of follicle-stimulating hormone receptor, inhibin/activin beta subunits, and anti-Müllerian hormone in human granulosa cells. Fertil Steril. 92:1794–1798. 2009. View Article : Google Scholar : PubMed/NCBI | |
Shi J, Yoshino O, Osuga Y, Nishii O, Yano T and Taketani Y: Bone morphogenetic protein 7 (BMP-7) increases the expression of follicle-stimulating hormone (FSH) receptor in human granulosa cells. Fertil Steril. 93:1273–1279. 2010. View Article : Google Scholar | |
Overes HW, de Leeuw R and Kloosterboer HJ: Regulation of aromatase activity in FSH-primed rat granulosa cells in vitro by follicle-stimulating hormone and various amounts of human chorionic gonadotrophin. Hum Reprod. 7:191–196. 1992. View Article : Google Scholar : PubMed/NCBI | |
Wu Y, Ghosh S, Nishi Y, Yanase T, Nawata H and Hu Y: The orphan nuclear receptors NURR1 and NGFI-B modulate aromatase gene expression in ovarian granulosa cells: A possible mechanism for repression of aromatase expression upon luteinizing hormone surge. Endocrinology. 146:237–246. 2005. View Article : Google Scholar | |
Du BW, Zhang XJ, Shi N, Peng T, Gao JB, Azimova B, Zhang R, Pu DB, Wang C, Abduvaliev A, et al: Luteolin-7-methylether from Leonurus japonicus inhibits estrogen biosynthesis in human ovarian granulosa cells by suppression of aromatase (CYP19). Eur J Pharmacol. 879:1731542020. View Article : Google Scholar : PubMed/NCBI | |
Lee SY, Kang YJ, Kwon J, Nishi Y, Yanase T, Lee KA and Koong MK: miR-4463 regulates aromatase expression and activity for 17β-estradiol synthesis in response to follicle-stimulating hormone. Clin Exp Reprod Med. 47:194–206. 2020. View Article : Google Scholar : PubMed/NCBI | |
Xu S, Linher-Melville K, Yang BB, Wu D and Li J: Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase. Endocrinology. 152:3941–3951. 2011. View Article : Google Scholar : PubMed/NCBI | |
Liu J, Li X, Yao Y and Li Q, Pan Z and Li Q: miR-1275 controls granulosa cell apoptosis and estradiol synthesis by impairing LRH-1/CYP19A1 axis. Biochim Biophys Acta Gene Regul Mech. 1861:246–257. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wang L, Li C, Li R, Deng Y, Tan Y, Tong C and Qi H: MicroRNA-764-3p regulates 17β-estradiol synthesis of mouse ovarian granulosa cells by targeting steroidogenic factor-1. In Vitro Cell Dev Biol Anim. 52:365–373. 2016. View Article : Google Scholar | |
Chaurasiya V, Kumari S, Onteru SK and Singh D: miR-326 down-regulate CYP19A1 expression and estradiol-17b production in buffalo granulosa cells through CREB and C/EBP-β. J Steroid Biochem Mol Biol. 199:1056082020. View Article : Google Scholar | |
Shi S, Zhou X, Li J, Zhang L, Hu Y, Li Y, Yang G and Chu G: MiR-214-3p promotes proliferation and inhibits estradiol synthesis in porcine granulosa cells. J Anim Sci Biotechnol. 11:942020. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Liu YD, Zhou XY, Chen SL, Chen X, Zhe J, Zhang J, Zhang QY and Chen YX: MiR-29a regulates the proliferation, aromatase expression, and estradiol biosynthesis of human granulosa cells in polycystic ovary syndrome. Mol Cell Endocrinol. 498:1105402019. View Article : Google Scholar : PubMed/NCBI | |
Al-Kawlani B, Murrieta-Coxca JM, Chaiwangyen W, Fröhlich K, Fritzsche A, Winkler S, Markert UR and Morales-Prieto DM: Doxorubicin induces cytotoxicity and miR-132 expression in granulosa cells. Reprod Toxicol. 96:95–101. 2020. View Article : Google Scholar : PubMed/NCBI | |
Ogo Y, Taniuchi S, Ojima F, Hayashi S, Murakami I, Saito Y, Takeuchi S, Kudo T and Takahashi S: IGF-1 gene expression is differentially regulated by estrogen receptors α and β in mouse endometrial stromal cells and ovarian granulosa cells. J Reprod Dev. 60:216–223. 2014. View Article : Google Scholar : | |
Zhou J, Chin E and Bondy C: Cellular pattern of insulin-like growth factor-I (IGF-I) and IGF-I receptor gene expression in the developing and mature ovarian follicle. Endocrinology. 129:3281–3288. 1991. View Article : Google Scholar : PubMed/NCBI | |
Mani AM, Fenwick MA, Cheng Z, Sharma MK, Singh D and Wathes DC: IGF1 induces up-regulation of steroidogenic and apoptotic regulatory genes via activation of phosphatidylinositol-dependent kinase/AKT in bovine granulosa cells. Reproduction. 139:139–151. 2010. View Article : Google Scholar | |
Herrmann M, Scholmerich J and Straub RH: Influence of cytokines and growth factors on distinct steroidogenic enzymes in vitro: A short tabular data collection. Ann NY Acad Sci. 966:166–186. 2002. View Article : Google Scholar : PubMed/NCBI | |
Fang L, Yu Y, Li Y, Wang S, Zhang R, Guo Y, Li Y, Yan Y and Sun YP: Human chorionic gonadotropin-induced amphiregulin stimulates aromatase expression in human granulosa-lutein cells: A mechanism for estradiol production in the luteal phase. Hum Reprod. 34:2018–2026. 2019. View Article : Google Scholar : PubMed/NCBI | |
Mendelson CR, Merrill JC, Steinkampf MP and Simpson ER: Regulation of the synthesis of aromatase cytochrome P-450 in human adipose stromal and ovarian granulosa cells. Steroids. 50:51–59. 1987. View Article : Google Scholar : PubMed/NCBI | |
Mishra SR, Bharati J, Rajesh G, Chauhan VS, Taru Sharma G, Bag S, Maurya VP, Singh G and Sarkar M: Fibroblast growth factor 2 (FGF2) and vascular endothelial growth factor A (VEGFA) synergistically promote steroidogenesis and survival of cultured buffalo granulosa cells. Anim Reprod Sci. 179:88–97. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zachow RJ, Ramski BE and Lee H: Modulation of estrogen production and 17beta-hydroxysteroid dehydrogenase-type 1, cytochrome P450 aromatase, c-met, and protein kinase Balpha messenger ribonucleic acid content in rat ovarian granulosa cells by hepatocyte growth factor and follicle-stimulating hormone. Biol Reprod. 62:1851–1857. 2000. View Article : Google Scholar : PubMed/NCBI | |
Chen YJ, Hsiao PW, Lee MT, Mason JI, Ke FC and Hwang JJ: Interplay of PI3K and cAMP/PKA signaling, and rapamycin-hypersensitivity in TGFbeta1 enhancement of FSH-stimulated steroidogenesis in rat ovarian granulosa cells. J Endocrinol. 192:405–419. 2007. View Article : Google Scholar : PubMed/NCBI | |
Zachow RJ, Weitsman SR and Magoffin DA: Leptin impairs the synergistic stimulation by transforming growth factor-beta of follicle-stimulating hormone-dependent aromatase activity and messenger ribonucleic acid expression in rat ovarian granulosa cells. Biol Reprod. 61:1104–1109. 1999. View Article : Google Scholar : PubMed/NCBI | |
Kwintkiewicz J, Nishi Y, Yanase T and Giudice LC: Peroxisome proliferator-activated receptor-gamma mediates bisphenol A inhibition of FSH-stimulated IGF-1, aromatase, and estradiol in human granulosa cells. Environ Health Perspect. 118:400–406. 2010. View Article : Google Scholar : PubMed/NCBI | |
Bloom MS, Mok-Lin E and Fujimoto VY: Bisphenol A and ovarian steroidogenesis. Fertil Steril. 106:857–863. 2016. View Article : Google Scholar : PubMed/NCBI | |
Dasmahapatra AK, Wimpee BA, Trewin AL and Hutz RJ: 2,3,7,8-Tetrachlorodibenzo-p-dioxin increases steady-state estrogen receptor-beta mRNA levels after CYP1A1 and CYP1B1 induction in rat granulosa cells in vitro. Mol Cell Endocrinol. 182:39–48. 2001. View Article : Google Scholar : PubMed/NCBI | |
Dasmahapatra AK, Wimpee BA, Trewin AL, Wimpee CF, Ghorai JK and Hutz RJ: Demonstration of 2,3,7,8-tetrachloro-dibenzo-p-dioxin attenuation of P450 steroidogenic enzyme mRNAs in rat granulosa cell in vitro by competitive reverse transcriptase-polymerase chain reaction assay. Mol Cell Endocrinol. 164:5–18. 2000. View Article : Google Scholar : PubMed/NCBI | |
Enan E, Moran F, VandeVoort CA, Stewart DR, Overstreet JW and Lasley BL: Mechanism of toxic action of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in cultured human luteinized granulosa cells. Reprod Toxicol. 10:497–508. 1996. View Article : Google Scholar : PubMed/NCBI | |
Baldridge MG, Marks GT, Rawlins RG and Hutz RJ: Very low-dose (femtomolar) 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) disrupts steroidogenic enzyme mRNAs and steroid secretion by human luteinizing granulosa cells. Reprod Toxicol. 52:57–61. 2015. View Article : Google Scholar : PubMed/NCBI | |
Lovekamp TN and Davis BJ: Mono-(2-ethylhexyl) phthalate suppresses aromatase transcript levels and estradiol production in cultured rat granulosa cells. Toxicol Appl Pharmacol. 172:217–224. 2001. View Article : Google Scholar : PubMed/NCBI | |
Reinsberg J, Wegener-Toper P, van der Ven K, van der Ven H and Klingmueller D: Effect of mono-(2-ethylhexyl) phthalate on steroid production of human granulosa cells. Toxicol Appl Pharmacol. 239:116–123. 2009. View Article : Google Scholar : PubMed/NCBI | |
Davis BJ, Weaver R, Gaines LJ and Heindel JJ: Mono-(2-ethylhexyl) phthalate suppresses estradiol production independent of FSH-cAMP stimulation in rat granulosa cells. Toxicol Appl Pharmacol. 128:224–228. 1994. View Article : Google Scholar : PubMed/NCBI | |
Simon V, Avet C, Grange-Messent V, Wargnier R, Denoyelle C, Pierre A, Dairou J, Dupret JM and Cohen-Tannoudji J: Carbon black nanoparticles inhibit aromatase expression and estradiol secretion in human granulosa cells through the ERK1/2 pathway. Endocrinology. 158:3200–3211. 2017. View Article : Google Scholar : PubMed/NCBI | |
Fan G, Zhang Q, Wan Y, Lv F, Chen Y, Ni Y, Zou W, Zhang W and Wang H: Decreased levels of H3K9ac and H3K27ac in the promotor region of ovarian P450 aromatase mediated low estradiol synthesis in female offspring rats induced by prenatal nicotine exposure as well as in human granulosa cells after nicotine treatment. Food Chem Toxicol. 128:256–266. 2019. View Article : Google Scholar : PubMed/NCBI | |
Taupeau C, Poupon J, Treton D, Brosse A, Richard Y and Machelon V: Lead reduces messenger RNA and protein levels of cytochrome p450 aromatase and estrogen receptor beta in human ovarian granulosa cells. Biol Reprod. 68:1982–1988. 2003. View Article : Google Scholar : PubMed/NCBI | |
Morinaga H, Yanase T, Nomura M, Okabe T, Goto K, Harada N and Nawata H: A benzimidazole fungicide, benomyl, and its metabolite, carbendazim, induce aromatase activity in a human ovarian granulose-like tumor cell line (KGN). Endocrinology. 145:1860–1869. 2004. View Article : Google Scholar | |
Zachow R and Uzumcu M: The methoxychlor metabolite, 2,2-bis-(p-hydroxyphenyl)-1,1,1-trichloroethane, inhibits steroidogenesis in rat ovarian granulosa cells in vitro. Reprod Toxicol. 22:659–665. 2006. View Article : Google Scholar : PubMed/NCBI | |
Rice S, Pellatt L, Ramanathan K, Whitehead SA and Mason HD: Metformin inhibits aromatase via an extracellular signal-regulated kinase-mediated pathway. Endocrinology. 150:4794–4801. 2009. View Article : Google Scholar : PubMed/NCBI | |
Fuhrmeister IP, Branchini G, Pimentel AM, Ferreira GD, Capp E, Brum IS and von Eye Corleta H: Human granulosa cells: Insulin and insulin-like growth factor-1 receptors and aromatase expression modulation by metformin. Gynecol Obstet Invest. 77:156–162. 2014. View Article : Google Scholar : PubMed/NCBI | |
Seto-Young D, Avtanski D, Parikh G, Suwandhi P, Strizhevsky M, Araki T, Rosenwaks Z and Poretsky L: Rosiglitazone and pioglitazone inhibit estrogen synthesis in human granulosa cells by interfering with androgen binding to aromatase. Horm Metab Res. 43:250–256. 2011. View Article : Google Scholar : PubMed/NCBI | |
Mu YM, Yanase T, Nishi Y, Waseda N, Oda T, Tanaka A, Takayanagi R and Nawata H: Insulin sensitizer, troglitazone, directly inhibits aromatase activity in human ovarian granulosa cells. Biochem Biophys Res Commun. 271:710–713. 2000. View Article : Google Scholar : PubMed/NCBI | |
Gonzalez-Robayna IJ, Falender AE, Ochsner S, Firestone GL and Richards JS: Follicle-Stimulating hormone (FSH) stimulates phosphorylation and activation of protein kinase B (PKB/Akt) and serum and glucocorticoid-lnduced kinase (Sgk): Evidence for A kinase-independent signaling by FSH in granulosa cells. Mol Endocrinol. 14:1283–1300. 2000. View Article : Google Scholar : PubMed/NCBI | |
Donadeu FX and Ascoli M: The differential effects of the gonado- tropin receptors on aromatase expression in primary cultures of immature rat granulosa cells are highly dependent on the density of receptors expressed and the activation of the inositol phosphate cascade. Endocrinology. 146:3907–3916. 2005. View Article : Google Scholar : PubMed/NCBI | |
Riccetti L, Sperduti S, Lazzaretti C, Casarini L and Simoni M: The cAMP/PKA pathway: Steroidogenesis of the antral follicular stage. Minerva Ginecol. 70:516–524. 2018. View Article : Google Scholar : PubMed/NCBI | |
Alam H, Maizels ET, Park Y, Ghaey S, Feiger ZJ, Chandel NS and Hunzicker-Dunn M: Follicle-stimulating hormone activation of hypoxia-inducible factor-1 by the phosphatidylinositol 3-kinase/AKT/Ras homolog enriched in brain (Rheb)/mammalian target of rapamycin (mTOR) pathway is necessary for induction of select protein markers of follicular differentiation. J Biol Chem. 279:19431–19440. 2004. View Article : Google Scholar : PubMed/NCBI | |
Zhou Y, Zeng C, Li X, Wu PL, Yin L, Yu XL, Zhou YF and Xue Q: IGF-I stimulates ERβ and aromatase expression via IGF1R/PI3K/AKT-mediated transcriptional activation in endometriosis. J Mol Med (Berl). 94:887–897. 2016. View Article : Google Scholar | |
Liu J, Han Y, Tian Y, Weng X, Hu X, Liu W, Heng D, Xu K, Yang Y and Zhang C: Regulation by 3,5,3′-tri-iodothyronine and FSH of cytochrome P450 family 19 (CYP19) expression in mouse granulosa cells. Reprod Fertil Dev. 30:1225–1233. 2018. View Article : Google Scholar : PubMed/NCBI | |
Cottom J, Salvador LM, Maizels ET, Reierstad S, Park Y, Carr DW, Davare MA, Hell JW, Palmer SS, Dent P, et al: Follicle-stimulating hormone activates extracellular signal-regulated kinase but not extracellular signal-regulated kinase kinase through a 100-kDa phosphotyrosine phosphatase. J Biol Chem. 278:7167–7179. 2003. View Article : Google Scholar | |
Huang X, Jin J, Shen S, Xia Y, Xu P, Zou X, Wang H, Yi L, Wang Y and Gao Q: Modulation of expression of 17-Hydroxylase/17,20 lyase (CYP17) and P450 aromatase (CYP19) by inhibition of MEK1 in a human ovarian granulosa-like tumor cell line. Gynecol Endocrinol. 32:201–205. 2016. View Article : Google Scholar | |
Findlay JK: An update on the roles of inhibin, activin, and follistatin as local regulators of folliculogenesis. Biol Reprod. 48:15–23. 1993. View Article : Google Scholar : PubMed/NCBI | |
Nomura M, Sakamoto R, Morinaga H, Wang L, Mukasa C and Takayanagi R: Activin stimulates CYP19A gene expression in human ovarian granulosa cell-like KGN cells via the Smad2 signaling pathway. Biochem Biophys Res Commun. 436:443–448. 2013. View Article : Google Scholar : PubMed/NCBI | |
Yenuganti VR, Ravinder and Singh D: Endotoxin induced TLR4 signaling downregulates CYP19A1 expression through CEBPB in buffalo granulosa cells. Toxicol In Vitro. 42:93–100. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Lu E, Bao R, Xu P, Feng F, Wen W, Dong Q, Hu C, Xiao L, Tang M, et al: Notch signalling regulates steroidogenesis in mouse ovarian granulosa cells. Reprod Fertil Dev. 31:1091–1103. 2019. View Article : Google Scholar : PubMed/NCBI | |
Manna PR, Molehin D and Ahmed AU: Dysregulation of aromatase in breast, endometrial, and ovarian cancers: An overview of therapeutic strategies. Prog Mol Biol Transl Sci. 144:487–537. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kato N, Uchigasaki S, Fukase M and Kurose A: Expression of P450 aromatase in granulosa cell tumors and sertoli-stromal cell tumors of the ovary: Which cells are responsible for estrogenesis? Int J Gynecol Pathol. 35:41–47. 2016. View Article : Google Scholar | |
Kitamura S, Abiko K, Matsumura N, Nakai H, Akimoto Y, Tanimoto H and Konishi I: Adult granulosa cell tumors of the ovary: A retrospective study of 30 cases with respect to the expression of steroid synthesis enzymes. J Gynecol Oncol. 28:e312017. View Article : Google Scholar : PubMed/NCBI | |
Hsueh AJ, Adashi EY, Jones PB and Welsh TH Jr: Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocr Rev. 5:76–127. 1984. View Article : Google Scholar : PubMed/NCBI | |
Cocquet J, Pailhoux E, Jaubert F, Servel N, Xia X, Pannetier M, De Baere E, Messiaen L, Cotinot C, Fellous M and Veitia RA: Evolution and expression of FOXL2. J Med Genet. 39:916–921. 2002. View Article : Google Scholar : PubMed/NCBI | |
Belli M, Iwata N, Nakamura T, Iwase A, Stupack D and Shimasaki S: FOXL2C134W-induced CYP19 expression via cooperation with SMAD3 in HGrC1 cells. Endocrinology. 159:1690–1703. 2018. View Article : Google Scholar : PubMed/NCBI | |
Fleming NI, Knower KC, Lazarus KA, Fuller PJ, Simpson ER and Clyne CD: Aromatase is a direct target of FOXL2: C134W in granulosa cell tumors via a single highly conserved binding site in the ovarian specific promoter. PLoS One. 5:e143892010. View Article : Google Scholar : PubMed/NCBI | |
Leung K: (S)-6-[(4-Chlorophenyl)(1H-1,2,4-triazol-1-yl) methyl]-1-[(11)C]methyl-1H-benzotriazole. Molecular imaging and contrast agent database (MICAD). National Center for Biotechnology Information; Bethesda, MD: 2004 | |
Moro F, Leombroni M, Pasciuto T, Trivellizzi IN, Mascilini F, Ciccarone F, Zannoni GF, Fanfani F, Scambia G and Testa AC: Synchronous primary cancers of endometrium and ovary vs endometrial cancer with ovarian metastasis: An observational study. Ultrasound Obstet Gynecol. 53:827–835. 2019.PubMed/NCBI | |
Michael MD, Kilgore MW, Morohashi K and Simpson ER: Ad4BP/SF-1 regulates cyclic AMP-induced transcription from the proximal promoter (PII) of the human aromatase P450 (CYP19) gene in the ovary. J Biol Chem. 270:13561–13566. 1995. View Article : Google Scholar : PubMed/NCBI | |
Panghiyangani R, Soeharso P, Andrijono, Suryandari DA, Wiweko B, Kurniati M and Pujianto DA: CYP19A1 gene expression in patients with polycystic ovarian syndrome. J Hum Reprod Sci. 13:100–103. 2020. View Article : Google Scholar : PubMed/NCBI | |
Shozu M, Sumitani H, Segawa T, Yang HJ, Murakami K, Kasai T and Inoue M: Overexpression of aromatase P450 in leiomyoma tissue is driven primarily through promoter I.4 of the aromatase P450 gene (CYP19). J Clin Endocrinol Metab. 87:2540–2548. 2002. View Article : Google Scholar : PubMed/NCBI | |
Jamnongjit M and Hammes SR: Ovarian steroids: The good, the bad, and the signals that raise them. Cell Cycle. 5:1178–1183. 2006. View Article : Google Scholar : PubMed/NCBI | |
Yang F, Ruan YC, Yang YJ, Wang K, Liang SS, Han YB, Teng XM and Yang JZ: Follicular hyperandrogenism downregulates aromatase in luteinized granulosa cells in polycystic ovary syndrome women. Reproduction. 150:289–296. 2015. View Article : Google Scholar : PubMed/NCBI | |
Dewailly D, Robin G, Peigne M, Decanter C, Pigny P and Catteau-Jonard S: Interactions between androgens, FSH, anti-Müllerian hormone and estradiol during folliculogenesis in the human normal and polycystic ovary. Hum Reprod Update. 22:709–724. 2016. View Article : Google Scholar : PubMed/NCBI | |
Che Q, Liu M, Zhang D, Lu Y, Xu J, Lu X, Cao X, Liu Y, Dong X and Liu S: Long noncoding RNA HUPCOS promotes follicular fluid androgen excess in PCOS patients via aromatase inhibition. J Clin Endocrinol Metab. 105:dgaa0602020. View Article : Google Scholar : PubMed/NCBI | |
Gu Y, Xu W, Zhuang B and Fu W: Role of A-kinase anchoring protein 95 in the regulation of cytochrome P450 family 19 subfamily A member 1 (CYP19A1) in human ovarian granulosa cells. Reprod Fertil Dev. 30:1128–1136. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ma X, Hayes E, Prizant H, Srivastava RK, Hammes SR and Sen A: Leptin-induced CART (cocaine- and amphetamine-regulated transcript) is a novel intraovarian mediator of obesity-related infertility in females. Endocrinology. 157:1248–1257. 2016. View Article : Google Scholar : PubMed/NCBI | |
Turkistani A and Marsh S: Pharmacogenomics of third-generation aromatase inhibitors. Expert Opin Pharmacother. 13:1299–1307. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kharb R, Haider K, Neha K and Yar MS: Aromatase inhibitors: Role in postmenopausal breast cancer. Arch Pharm (Weinheim). 353:e20000812020. View Article : Google Scholar | |
Usluogullari B, Duvan C and Usluogullari C: Use of aromatase inhibitors in practice of gynecology. J Ovarian Res. 8:42015. View Article : Google Scholar : PubMed/NCBI | |
Ammazzalorso A, Gallorini M, Fantacuzzi M, Gambacorta N, De Filippis B, Giampietro L, Maccallini C, Nicolotti O, Cataldi A and Amoroso R: Design, synthesis and biological evaluation of imidazole and triazole-based carbamates as novel aromatase inhibitors. Eur J Med Chem. 211:1131152021. View Article : Google Scholar | |
Haltia UM, Pihlajoki M, Andersson N, Mäkinen L, Tapper J, Cervera A, Horlings HM, Turpeinen U, Anttonen M, Bützow R, et al: Functional profiling of FSH and estradiol in ovarian granulosa cell tumors. J Endocr Soc. 4:bvaa0342020. View Article : Google Scholar : PubMed/NCBI | |
Ghosh D, Lo J and Egbuta C: Recent progress in the discovery of next generation inhibitors of aromatase from the structure-function perspective. J Med Chem. 59:5131–5148. 2016. View Article : Google Scholar : | |
Steinkampf MP, Mendelson CR and Simpson ER: Effects of epidermal growth factor and insulin-like growth factor I on the levels of mRNA encoding aromatase cytochrome P-450 of human ovarian granulosa cells. Mol Cell Endocrinol. 59:93–99. 1988. View Article : Google Scholar : PubMed/NCBI |