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Current Topics in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Review Article

The Role of Aromatase Enzyme in Hormone Related Diseases and Plant- Based Aromatase Inhibitors as Therapeutic Regimens

Author(s): Kevser Taban Akça, Murside Ayşe Demirel and Ipek Süntar*

Volume 22, Issue 3, 2022

Published on: 11 January, 2022

Page: [229 - 246] Pages: 18

DOI: 10.2174/1568026621666211129141631

Price: $65

Abstract

Medicinal plants have a long history of use as food and remedy in traditional and modern societies. They have been used as herbal drugs and sources of novel bioactive compounds. They provide a wide array of chemical compounds, many of which can not be synthesized via current synthesis methods. Natural products may provide aromatase inhibitory activity through various pathways and may act clinically effective for treating pathologies associated with excessive aromatase secretion, including breast, ovarian, and endometrial cancers, endometriosis, uterine fibroid, benign prostatic hyperplasia (BPH), prostate cancer, infertility, and gynecomastia. Recent studies have shown that natural products with aromatase inhibitory activity can also be good options against secondary recurrence of breast cancer by exhibiting chemopreventive effects. Therefore, screening for new plant-based aromatase inhibitors may provide novel leads for drug discovery and development, particularly with increased clinical efficacy and decreased side effects.

Keywords: Aromatase, Natural products, Medicinal plants, Secondary metabolites, Estrogen, Testosterone.

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[1]
Herson, P.S.; Koerner, I.P.; Hurn, P.D. Sex, sex steroids, and brain injury. Semin. Reprod. Med., 2009, 27(3), 229-239.
[http://dx.doi.org/10.1055/s-0029-1216276] [PMID: 19401954]
[2]
Patel, S. Disruption of aromatase homeostasis as the cause of a multiplicity of ailments: A comprehensive review. J. Steroid Biochem. Mol. Biol., 2017, 168, 19-25.
[http://dx.doi.org/10.1016/j.jsbmb.2017.01.009] [PMID: 28109841]
[3]
Balunas, M.J.; Su, B.; Brueggemeier, R.W.; Kinghorn, A.D. Natural products as aromatase inhibitors. Anticancer Agents Med Chem, 2008, 8(6), 646-682.
[PMID: 18690828]
[4]
Gansser, D.; Spiteller, G. Aromatase inhibitors from Urtica dioica roots. Planta Med., 1995, 61(2), 138-140.
[http://dx.doi.org/10.1055/s-2006-958033] [PMID: 17238068]
[5]
Ducrey, B.; Marston, A.; Göhring, S.; Hartmann, R.W.; Hostettmann, K. Inhibition of 5 alpha-reductase and aromatase by the ellagitannins oenothein A and oenothein B from Epilobium species. Planta Med., 1997, 63(2), 111-114.
[http://dx.doi.org/10.1055/s-2006-957624] [PMID: 9140222]
[6]
Grube, B.J.; Eng, E.T.; Kao, Y.C.; Kwon, A.; Chen, S. White button mushroom phytochemicals inhibit aromatase activity and breast cancer cell proliferation. J. Nutr., 2001, 131(12), 3288-3293.
[http://dx.doi.org/10.1093/jn/131.12.3288] [PMID: 11739882]
[7]
Lee, D.; Bhat, K.P.; Fong, H.H.; Farnsworth, N.R.; Pezzuto, J.M.; Kinghorn, A.D. Aromatase inhibitors from Broussonetia papyrifera. J. Nat. Prod., 2001, 64(10), 1286-1293.
[http://dx.doi.org/10.1021/np010288l] [PMID: 11678652]
[8]
Lee, T.K.; Kim, D.I.; Han, J.Y.; Kim, C.H. Inhibitory effects of Scutellaria barbata D. Don. and Euonymus alatus Sieb. on aromatase activity of human leiomyomal cells. Immunopharmacol. Immunotoxicol., 2004, 26(3), 315-327.
[http://dx.doi.org/10.1081/IPH-200026840] [PMID: 15518167]
[9]
Balunas, M.J.; Su, B.; Riswan, S.; Fong, H.H.S.; Brueggemeier, R.W.; Pezzuto, J.M.; Kinghorn, A.D. Isolation and characterization of aromatase inhibitors from Brassaiopsis glomerulata (Araliaceae). Phytochem. Lett., 2009, 2(1), 29-33.
[http://dx.doi.org/10.1016/j.phytol.2008.10.009] [PMID: 20161072]
[10]
Chen, Y.; Chen, C.; Shi, S.; Han, J.; Wang, J.; Hu, J.; Liu, Y.; Cai, Z.; Yu, C. Endometriotic implants regress in rat models treated with puerarin by decreasing estradiol level. Reprod. Sci., 2011, 18(9), 886-891.
[http://dx.doi.org/10.1177/1933719111398500] [PMID: 21673282]
[11]
Kim, J.; Jayaprakasha, G.K.; Patil, B.S. Obacunone exhibits anti-proliferative and anti-aromatase activity in vitro by inhibiting the p38 MAPK signaling pathway in MCF-7 human breast adenocarcinoma cells. Biochimie, 2014, 105, 36-44.
[http://dx.doi.org/10.1016/j.biochi.2014.06.002] [PMID: 24927687]
[12]
Pailee, P.; Prachyawarakorn, V.; Ruchirawat, S.; Mahidol, C. Bioactive cardinane sesquiterpenes from the stems of Alangium salviifolium. Chem. Asian J., 2015, 10(4), 910-914.
[http://dx.doi.org/10.1002/asia.201403253] [PMID: 25645740]
[13]
Dawood, H.M.; Ibrahim, R.S.; Shawky, E.; Hammoda, H.M.; Metwally, A.M. Integrated in silico-in vitro strategy for screening of some traditional Egyptian plants for human aromatase inhibitors. J. Ethnopharmacol., 2018, 224, 359-372.
[http://dx.doi.org/10.1016/j.jep.2018.06.009] [PMID: 29909120]
[14]
Miao, L.; Jiao, C.; Shao, R.; Qi, Y.; Fan, G.; Li, X.; Wang, Y.; Zhu, Y.; Zhang, J.; Gao, X. Bakuchiol suppresses oestrogen/testosterone-induced Benign Prostatic Hyperplasia development through up-regulation of epithelial estrogen receptor β and down-regulation of stromal aromatase. Toxicol. Appl. Pharmacol., 2019, 381, 114637.
[http://dx.doi.org/10.1016/j.taap.2019.114637] [PMID: 31238046]
[15]
Ali, A.; Jan, N.U.; Ali, S.; Ahmad, B.; Ali, A.; Samrana, S.; Jahan, A.; Ali, H.; Khan, I.A.; Rahim, H.; Ali, I.; Kifayatullah, M.; Amin, F. Steroidal alkaloids efficient aromatase inhibitors with potential for the treatment of postmenopausal breast cancer. Chem. Biol. Drug Des., 2020, 95(2), 233-239.
[http://dx.doi.org/10.1111/cbdd.13635] [PMID: 31584741]
[16]
Demura, M.; Martin, R.M.; Shozu, M.; Sebastian, S.; Takayama, K.; Hsu, W-T.; Schultz, R.A.; Neely, K.; Bryant, M.; Mendonca, B.B.; Hanaki, K.; Kanzaki, S.; Rhoads, D.B.; Misra, M.; Bulun, S.E. Regional rearrangements in chromosome 15q21 cause formation of cryptic promoters for the CYP19 (aromatase) gene. Hum. Mol. Genet., 2007, 16(21), 2529-2541.
[http://dx.doi.org/10.1093/hmg/ddm145] [PMID: 17584767]
[17]
Bulun, S.E.; Price, T.M.; Aitken, J.; Mahendroo, M.S.; Simpson, E.R. A link between breast cancer and local estrogen biosynthesis suggested by quantification of breast adipose tissue aromatase cytochrome P450 transcripts using competitive polymerase chain reaction after reverse transcription. J. Clin. Endocrinol. Metab., 1993, 77(6), 1622-1628.
[http://dx.doi.org/10.1210/jcem.77.6.8117355] [PMID: 8117355]
[18]
Piriu, G.; Torac, E.; Gaman, L.E.; Iosif, L.; Tivig, I.C.; Delia, C.; Gilca, M.; Stoian, I.; Atanasiu, V. Clozapine and risperidone influence on cortisol and estradiol levels in male patients with schizophrenia. J. Med. Life, 2015, 8(4), 548-551.
[PMID: 26664488]
[19]
Mori, T.; Ito, F.; Koshiba, A.; Kataoka, H.; Tanaka, Y.; Okimura, H.; Khan, K.N.; Kitawaki, J. Aromatase as a target for treating endometriosis. J. Obstet. Gynaecol. Res., 2018, 44(9), 1673-1681.
[http://dx.doi.org/10.1111/jog.13743] [PMID: 30043503]
[20]
Oktem, O.; Urman, B. Understanding follicle growth in vivo. Hum. Reprod., 2010, 25(12), 2944-2954.
[http://dx.doi.org/10.1093/humrep/deq275] [PMID: 20937745]
[21]
Rimon-Dahari, N.; Yerushalmi-Heinemann, L.; Alyagor, L.; Dekel, N. Ovarian folliculogenesis. Results Probl Cell Differ., 2016, 58, 167-190.
[http://dx.doi.org/10.1007/978-3-319-31973-5_7] [PMID: 27300179]
[22]
Monniaux, D.; Cadoret, V.; Clément, F.; Dalbies-Tran, R.; Elis, S.; Fabre, S.; Maillard, V.; Monget, P.; Uzbekova, S. Folliculogenesis. In: Encyclopedia of Endocrine Diseases, 2nd Ed.; Huhtaniemi, I.; Martini, L., Eds.; Academic Press: Oxford, 2019, pp. 377-398.
[23]
Gervásio, C.G.; Bernuci, M.P.; Silva-de-Sá, M.F.; Rosa-E-Silva, A.C. The role of androgen hormones in early follicular development. ISRN Obstet. Gynecol., 2014, 2014, 818010.
[http://dx.doi.org/10.1155/2014/818010] [PMID: 25006485]
[24]
Hannon, P.R.; Curry, T.E. Folliculogenesis. In: Encyclopedia of Reproduction, 2nd ed; Skinner, M.K., Ed.; Academic Press: Oxford, Encyclopedia of Reproduction., 2018, pp. 72-79.
[http://dx.doi.org/10.1016/B978-0-12-801238-3.64628-7]
[25]
Altmäe, S.; Haller, K.; Peters, M.; Saare, M.; Hovatta, O.; Stavreus-Evers, A.; Velthut, A.; Karro, H.; Metspalu, A.; Salumets, A. Aromatase gene (CYP19A1) variants, female infertility and ovarian stimulation outcome: a preliminary report. Reprod. Biomed. Online, 2009, 18(5), 651-657.
[http://dx.doi.org/10.1016/S1472-6483(10)60009-0] [PMID: 19549443]
[26]
Carrer, H.F.; Cambiasso, M.J.; Brito, V.; Gorosito, S. Neurotrophic factors and estradiol interact to control axogenic growth in hypothalamic neurons. Ann. N. Y. Acad. Sci., 2003, 1007, 306-316.
[http://dx.doi.org/10.1196/annals.1286.029] [PMID: 14993063]
[27]
Lanfranco, F.; Zirilli, L.; Baldi, M.; Pignatti, E.; Corneli, G.; Ghigo, E.; Aimaretti, G.; Carani, C.; Rochira, V. A novel mutation in the human aromatase gene: insights on the relationship among serum estradiol, longitudinal growth and bone mineral density in an adult man under estrogen replacement treatment. Bone, 2008, 43(3), 628-635.
[http://dx.doi.org/10.1016/j.bone.2008.05.011] [PMID: 18590994]
[28]
Giampietro, L.; Gallorini, M.; Gambacorta, N.; Ammazzalorso, A.; De Filippis, B.; Della Valle, A.; Fantacuzzi, M.; Maccallini, C.; Mollica, A.; Cataldi, A.; Nicolotti, O.; Amoroso, R. Synthesis, structure-activity relationships and molecular docking studies of phenyldiazenyl sulfonamides as aromatase inhibitors. Eur. J. Med. Chem., 2021, 224, 113737.
[http://dx.doi.org/10.1016/j.ejmech.2021.113737] [PMID: 34365129]
[29]
Hong, Y.; Chen, S. Aromatase inhibitors: structural features and biochemical characterization. Ann. N. Y. Acad. Sci., 2006, 1089, 237-251.
[http://dx.doi.org/10.1196/annals.1386.022] [PMID: 17261771]
[30]
Pazaiti, A.; Fentiman, I.S. Basal phenotype breast cancer: implications for treatment and prognosis. Womens Health (Lond. Engl.), 2011, 7(2), 181-202.
[http://dx.doi.org/10.2217/WHE.11.5] [PMID: 21410345]
[31]
Khan, S.I.; Zhao, J.; Khan, I.A.; Walker, L.A.; Dasmahapatra, A.K. Potential utility of natural products as regulators of breast cancer-associated aromatase promoters. Reprod. Biol. Endocrinol., 2011, 9, 91-91.
[http://dx.doi.org/10.1186/1477-7827-9-91] [PMID: 21693041]
[32]
Darbre, P.D. Underarm antiperspirants/deodorants and breast cancer. Breast Cancer Res., 2009, 11 Suppl 3(Suppl 3), S5.
[http://dx.doi.org/10.1186/bcr2424] [PMID: 20030880]
[33]
Burstein, H.J.; Griggs, J.J.; Prestrud, A.A.; Temin, S. American society of clinical oncology clinical practice guideline update on adjuvant endocrine therapy for women with hormone receptor-positive breast cancer. J. Oncol. Pract., 2010, 6(5), 243-246.
[http://dx.doi.org/10.1200/JOP.000082] [PMID: 21197188]
[34]
Schmid, B.C.; Oehler, M.K. New perspectives in ovarian cancer treatment. Maturitas, 2014, 77(2), 128-136.
[http://dx.doi.org/10.1016/j.maturitas.2013.11.009] [PMID: 24380827]
[35]
Simpkins, F.; Hevia-Paez, P.; Sun, J.; Ullmer, W.; Gilbert, C.A.; da Silva, T.; Pedram, A.; Levin, E.R.; Reis, I.M.; Rabinovich, B.; Azzam, D.; Xu, X.X.; Ince, T.A.; Yang, J.Y.; Verhaak, R.G.W.; Lu, Y.; Mills, G.B.; Slingerland, J.M. Src Inhibition with saracatinib reverses fulvestrant resistance in ER-positive ovarian cancer models in vitro and in vivo. Clin. Cancer Res., 2012, 18(21), 5911-5923.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-1257] [PMID: 22896656]
[36]
Bulun, S.E.; Lin, Z.; Imir, G.; Amin, S.; Demura, M.; Yilmaz, B.; Martin, R.; Utsunomiya, H.; Thung, S.; Gurates, B.; Tamura, M.; Langoi, D.; Deb, S. Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol. Rev., 2005, 57(3), 359-383.
[http://dx.doi.org/10.1124/pr.57.3.6] [PMID: 16109840]
[37]
Giudice, L.C. Clinical practice. Endometriosis. N. Engl. J. Med., 2010, 362(25), 2389-2398.
[http://dx.doi.org/10.1056/NEJMcp1000274] [PMID: 20573927]
[38]
Takaoka, O.; Mori, T.; Ito, F.; Okimura, H.; Kataoka, H.; Tanaka, Y.; Koshiba, A.; Kusuki, I.; Shigehiro, S.; Amami, T.; Kitawaki, J. Daidzein-rich isoflavone aglycones inhibit cell growth and inflammation in endometriosis. J. Steroid Biochem. Mol. Biol., 2018, 181, 125-132.
[http://dx.doi.org/10.1016/j.jsbmb.2018.04.004] [PMID: 29679753]
[39]
Beavis, A.L.; Smith, A.J.B.; Fader, A.N. Lifestyle changes and the risk of developing endometrial and ovarian cancers: opportunities for prevention and management. Int. J. Womens Health, 2016, 8, 151-167.
[PMID: 27284267]
[40]
Attar, E.; Bulun, S.E. Aromatase and other steroidogenic genes in endometriosis: translational aspects. Hum. Reprod. Update, 2006, 12(1), 49-56.
[http://dx.doi.org/10.1093/humupd/dmi034] [PMID: 16123052]
[41]
Zhang, Y.; Cao, H.; Yu, Z.; Peng, H-Y.; Zhang, C-J. Curcumin inhibits endometriosis endometrial cells by reducing estradiol production. Iran. J. Reprod. Med., 2013, 11(5), 415-422.
[PMID: 24639774]
[42]
Song, H.; Lu, D.; Navaratnam, K.; Shi, G. Aromatase inhibitors for uterine fibroids. Cochrane Database Syst. Rev., 2013, (10), CD009505.
[PMID: 24151065]
[43]
Wallach, E.E.; Vlahos, N.F. Uterine myomas: an overview of development, clinical features, and management. Obstet. Gynecol., 2004, 104(2), 393-406.
[http://dx.doi.org/10.1097/01.AOG.0000136079.62513.39] [PMID: 15292018]
[44]
Gurates, B.; Parmaksiz, C.; Kilic, G.; Celik, H.; Kumru, S.; Simsek, M. Treatment of symptomatic uterine leiomyoma with letrozole. Reprod. Biomed. Online, 2008, 17(4), 569-574.
[http://dx.doi.org/10.1016/S1472-6483(10)60246-5] [PMID: 18854113]
[45]
Shah, C.; Nayak, M.; Kulkarni, K. Use of PR2000, a Herbal Formulation in the Medical Management of Benign Prostatic Hyperplasia. 2002, 13, 53-66.
[46]
Vitalone, A.; Bordi, F.; Baldazzi, C.; Mazzanti, G.; Saso, L.; Tita, B. Anti-proliferative effect on a prostatic epithelial cell line (PZ-HPV-7) by Epilobium angustifolium L. Farmaco, 2001, 56(5-7), 483-489.
[http://dx.doi.org/10.1016/S0014-827X(01)01067-9] [PMID: 11482783]
[47]
Azimi, H.; Khakshur, A.A.; Aghdasi, I.; Fallah-Tafti, M.; Abdollahi, M. A review of animal and human studies for management of benign prostatic hyperplasia with natural products: perspective of new pharmacological agents. Inflamm. Allergy Drug Targets, 2012, 11(3), 207-221.
[http://dx.doi.org/10.2174/187152812800392715] [PMID: 22512478]
[48]
Séralini, G.; Moslemi, S. Aromatase inhibitors: past, present and future. Mol. Cell. Endocrinol., 2001, 178(1-2), 117-131.
[http://dx.doi.org/10.1016/S0303-7207(01)00433-6] [PMID: 11403901]
[49]
Ellem, S.J.; Risbridger, G.P. Treating prostate cancer: a rationale for targeting local oestrogens. Nat. Rev. Cancer, 2007, 7(8), 621-627.
[http://dx.doi.org/10.1038/nrc2174] [PMID: 17611544]
[50]
Bosland, M.C. The role of steroid hormones in prostate carcinogenesis. J. Natl. Cancer Inst. Monogr., 2000, (27), 39-66.
[http://dx.doi.org/10.1093/oxfordjournals.jncimonographs.a024244] [PMID: 10963619]
[51]
Alhadrami, H.A.; Sayed, A.M.; Melebari, S.A.; Khogeer, A.A.; Abdulaal, W.H.; Al-Fageeh, M.B.; Algahtani, M.; Rateb, M.E. Targeting allosteric sites of human aromatase: a comprehensive in-silico and in-vitro workflow to find potential plant-based anti-breast cancer therapeutics. J. Enzyme Inhib. Med. Chem., 2021, 36(1), 1334-1345.
[http://dx.doi.org/10.1080/14756366.2021.1937145] [PMID: 34139914]
[52]
Ross, R.K.; Bernstein, L.; Lobo, R.A.; Shimizu, H.; Stanczyk, F.Z.; Pike, M.C.; Henderson, B.E. 5-alpha-reductase activity and risk of prostate cancer among Japanese and US white and black males. Lancet, 1992, 339(8798), 887-889.
[http://dx.doi.org/10.1016/0140-6736(92)90927-U] [PMID: 1348296]
[53]
Nelles, J.L.; Hu, W-Y.; Prins, G.S. Estrogen action and prostate cancer. Expert Rev. Endocrinol. Metab., 2011, 6(3), 437-451.
[http://dx.doi.org/10.1586/eem.11.20] [PMID: 21765856]
[54]
Kruit, W.H.J.; Stoter, G.; Klijn, J.G.M. Effect of combination therapy with aminoglutethimide and hydrocortisone on prostate-specific antigen response in metastatic prostate cancer refractory to standard endocrine therapy. Anticancer Drugs, 2004, 15(9), 843-847.
[http://dx.doi.org/10.1097/00001813-200410000-00004] [PMID: 15457124]
[55]
Liang, Z.; Cao, J.; Tian, L.; Shen, Y.; Yang, X.; Lin, Q.; Zhang, R.; Liu, H.; Du, X.; Shi, J.; Zhang, J. Aromatase-induced endogenous estrogen promotes tumour metastasis through estrogen receptor-α/matrix metalloproteinase 12 axis activation in castration-resistant prostate cancer. Cancer Lett., 2019, 467, 72-84.
[http://dx.doi.org/10.1016/j.canlet.2019.09.001] [PMID: 31499120]
[56]
Schlegel, P.N. Aromatase inhibitors for male infertility. Fertil. Steril., 2012, 98(6), 1359-1362.
[http://dx.doi.org/10.1016/j.fertnstert.2012.10.023] [PMID: 23103016]
[57]
Inkster, S.; Yue, W.; Brodie, A. Human testicular aromatase: immunocytochemical and biochemical studies. J. Clin. Endocrinol. Metab., 1995, 80(6), 1941-1947.
[PMID: 7539819]
[58]
Pavlovich, C.P.; King, P.; Goldstein, M.; Schlegel, P.N. Evidence of a treatable endocrinopathy in infertile men. J. Urol., 2001, 165(3), 837-841.
[http://dx.doi.org/10.1016/S0022-5347(05)66540-8] [PMID: 11176482]
[59]
Braunstein, G.D. Gynecomastia. N. Engl. J. Med., 1993, 328(7), 490-495.
[http://dx.doi.org/10.1056/NEJM199302183280708] [PMID: 8421478]
[60]
Braunstein, G.D. Aromatase and gynecomastia. Endocr. Relat. Cancer, 1999, 6(2), 315-324.
[http://dx.doi.org/10.1677/erc.0.0060315] [PMID: 10731125]
[61]
Jeong, H-J.; Chang, L.C.; Kim, H-K.; Kim, I-H.; Kinghorn, A.D.; Pezzuto, J.M. Aromatase inhibitors from Isodon excisus var. coreanus. Arch. Pharm. Res., 2000, 23(3), 243-245.
[http://dx.doi.org/10.1007/BF02976453] [PMID: 10896056]
[62]
Yu, C.; Li, Y.; Chen, H.; Yang, S.; Xie, G. Decreased expression of aromatase in the Ishikawa and RL95-2 cells by the isoflavone, puerarin, is associated with inhibition of c-jun expression and AP-1 activity. Food Chem. Toxicol., 2008, 46(12), 3671-3676.
[http://dx.doi.org/10.1016/j.fct.2008.09.045] [PMID: 18848966]
[63]
Kao, Y.C.; Zhou, C.; Sherman, M.; Laughton, C.A.; Chen, S. Molecular basis of the inhibition of human aromatase (estrogen synthetase) by flavone and isoflavone phytoestrogens: A site-directed mutagenesis study. Environ. Health Perspect., 1998, 106(2), 85-92.
[http://dx.doi.org/10.1289/ehp.9810685] [PMID: 9435150]
[64]
Sanderson, J.T.; Hordijk, J.; Denison, M.S.; Springsteel, M.F.; Nantz, M.H.; van den Berg, M. Induction and inhibition of aromatase (CYP19) activity by natural and synthetic flavonoid compounds in H295R human adrenocortical carcinoma cells. Toxicol. Sci., 2004, 82(1), 70-79.
[http://dx.doi.org/10.1093/toxsci/kfh257] [PMID: 15319488]
[65]
van Meeuwen, J.A.; Korthagen, N.; de Jong, P.C.; Piersma, A.H.; van den Berg, M. (Anti)estrogenic effects of phytochemicals on human primary mammary fibroblasts, MCF-7 cells and their co-culture. Toxicol. Appl. Pharmacol., 2007, 221(3), 372-383.
[http://dx.doi.org/10.1016/j.taap.2007.03.016] [PMID: 17482226]
[66]
van Meeuwen, J.A.; Nijmeijer, S.; Mutarapat, T.; Ruchirawat, S.; de Jong, P.C.; Piersma, A.H.; van den Berg, M. Aromatase inhibition by synthetic lactones and flavonoids in human placental microsomes and breast fibroblasts--a comparative study. Toxicol. Appl. Pharmacol., 2008, 228(3), 269-276.
[http://dx.doi.org/10.1016/j.taap.2007.12.007] [PMID: 18201740]
[67]
Maia, H., Jr; Haddad, C.; Pinheiro, N.; Casoy, J. Advantages of the association of resveratrol with oral contraceptives for management of endometriosis-related pain. Int. J. Womens Health, 2012, 4, 543-549.
[http://dx.doi.org/10.2147/IJWH.S36825] [PMID: 23091400]
[68]
Kellis, J.T., Jr; Vickery, L.E. Inhibition of human estrogen synthetase (aromatase) by flavones. Science, 1984, 225(4666), 1032-1034.
[http://dx.doi.org/10.1126/science.6474163] [PMID: 6474163]
[69]
Ibrahim, A.R.; Abul-Hajj, Y.J. Aromatase inhibition by flavonoids. J. Steroid Biochem. Mol. Biol., 1990, 37(2), 257-260.
[http://dx.doi.org/10.1016/0960-0760(90)90335-I] [PMID: 2268557]
[70]
Campbell, D.R.; Kurzer, M.S. Flavonoid inhibition of aromatase enzyme activity in human preadipocytes. J. Steroid Biochem. Mol. Biol., 1993, 46(3), 381-388.
[http://dx.doi.org/10.1016/0960-0760(93)90228-O] [PMID: 9831487]
[71]
Wang, Y.; Lee, K.W.; Chan, F.L.; Chen, S.; Leung, L.K. The red wine polyphenol resveratrol displays bilevel inhibition on aromatase in breast cancer cells. Toxicol. Sci., 2006, 92(1), 71-77.
[http://dx.doi.org/10.1093/toxsci/kfj190] [PMID: 16611627]
[72]
Wang, Y.; Leung, L.K. Pharmacological concentration of resveratrol suppresses aromatase in JEG-3 cells. Toxicol. Lett., 2007, 173(3), 175-180.
[http://dx.doi.org/10.1016/j.toxlet.2007.07.009] [PMID: 17766065]
[73]
Wang, Y.; Ye, L.; Leung, L.K. A positive feedback pathway of estrogen biosynthesis in breast cancer cells is contained by resveratrol. Toxicology, 2008, 248(2-3), 130-135.
[http://dx.doi.org/10.1016/j.tox.2008.03.017] [PMID: 18462857]
[74]
Adams, L.S.; Chen, S. Phytochemicals for breast cancer prevention by targeting aromatase. Front. Biosci., 2009, 14, 3846-3863.
[http://dx.doi.org/10.2741/3493] [PMID: 19273315]
[75]
Zhao, H.; Chen, Z. Screening of aromatase inhibitors in traditional Chinese medicines by electrophoretically mediated microanalysis in a partially filled capillary. J. Sep. Sci., 2013, 36(16), 2691-2697.
[http://dx.doi.org/10.1002/jssc.201300474] [PMID: 23757179]
[76]
Wang, Y.; Chan, F.L.; Chen, S.; Leung, L.K. The plant polyphenol butein inhibits testosterone-induced proliferation in breast cancer cells expressing aromatase. Life Sci., 2005, 77(1), 39-51.
[http://dx.doi.org/10.1016/j.lfs.2004.12.014] [PMID: 15848217]
[77]
Ye, L.; Gho, W.M.; Chan, F.L.; Chen, S.; Leung, L.K. Dietary administration of the licorice flavonoid isoliquiritigenin deters the growth of MCF-7 cells overexpressing aromatase. Int. J. Cancer, 2009, 124(5), 1028-1036.
[http://dx.doi.org/10.1002/ijc.24046] [PMID: 19065667]
[78]
Chen, S.; Cho, M.; Karlsberg, K.; Zhou, D.; Yuan, Y-C. Biochemical and biological characterization of a novel anti-aromatase coumarin derivative. J. Biol. Chem., 2004, 279(46), 48071-48078.
[http://dx.doi.org/10.1074/jbc.M406847200] [PMID: 15358790]
[79]
Le Bail, J-C.; Champavier, Y.; Chulia, A-J.; Habrioux, G. Effects of phytoestrogens on aromatase, 3β and 17β-hydroxysteroid dehydrogenase activities and human breast cancer cells. Life Sci., 2000, 66(14), 1281-1291.
[http://dx.doi.org/10.1016/S0024-3205(00)00435-5] [PMID: 10755463]
[80]
Jeong, H.J.; Shin, Y.G.; Kim, I.H.; Pezzuto, J.M. Inhibition of aromatase activity by flavonoids. Arch. Pharm. Res., 1999, 22(3), 309-312.
[http://dx.doi.org/10.1007/BF02976369] [PMID: 10403137]
[81]
Pelissero, C.; Lenczowski, M.J.; Chinzi, D.; Davail-Cuisset, B.; Sumpter, J.P.; Fostier, A. Effects of flavonoids on aromatase activity, an in vitro study. J. Steroid Biochem. Mol. Biol., 1996, 57(3-4), 215-223.
[http://dx.doi.org/10.1016/0960-0760(95)00261-8] [PMID: 8645631]
[82]
Adlercreutz, H.; Bannwart, C.; Wähälä, K.; Mäkelä, T.; Brunow, G.; Hase, T.; Arosemena, P.J.; Kellis, J.T., Jr; Vickery, L.E. Inhibition of human aromatase by mammalian lignans and isoflavonoid phytoestrogens. J. Steroid Biochem. Mol. Biol., 1993, 44(2), 147-153.
[http://dx.doi.org/10.1016/0960-0760(93)90022-O] [PMID: 8382517]
[83]
Wang, C.; Mäkelä, T.; Hase, T.; Adlercreutz, H.; Kurzer, M.S. Lignans and flavonoids inhibit aromatase enzyme in human preadipocytes. J. Steroid Biochem. Mol. Biol., 1994, 50(3-4), 205-212.
[http://dx.doi.org/10.1016/0960-0760(94)90030-2] [PMID: 8049151]
[84]
Satoh, K.; Sakamoto, Y.; Ogata, A.; Nagai, F.; Mikuriya, H.; Numazawa, M.; Yamada, K.; Aoki, N. Inhibition of aromatase activity by green tea extract catechins and their endocrinological effects of oral administration in rats. Food Chem. Toxicol., 2002, 40(7), 925-933.
[http://dx.doi.org/10.1016/S0278-6915(02)00066-2] [PMID: 12065214]
[85]
Way, T-D.; Lee, H-H.; Kao, M-C.; Lin, J-K. Black tea polyphenol theaflavins inhibit aromatase activity and attenuate tamoxifen resistance in HER2/neu-transfected human breast cancer cells through tyrosine kinase suppression. Eur. J. Cancer, 2004, 40(14), 2165-2174.
[http://dx.doi.org/10.1016/j.ejca.2004.06.018] [PMID: 15341993]
[86]
Ozcan-Sezer, S.; Ince, E.; Akdemir, A.; Ceylan, Ö.Ö.; Suzen, S.; Gurer-Orhan, H. Aromatase inhibition by 2-methyl indole hydrazone derivatives evaluated via molecular docking and in vitro activity studies. Xenobiotica, 2019, 49(5), 549-556.
[http://dx.doi.org/10.1080/00498254.2018.1482029] [PMID: 29804490]
[87]
Barbieri, R.L.; Gochberg, J.; Ryan, K.J. Nicotine, cotinine, and anabasine inhibit aromatase in human trophoblast in vitro. J. Clin. Invest., 1986, 77(6), 1727-1733.
[http://dx.doi.org/10.1172/JCI112494] [PMID: 3711333]
[88]
Kadohama, N.; Shintani, K.; Osawa, Y. Tobacco alkaloid derivatives as inhibitors of breast cancer aromatase. Cancer Lett., 1993, 75(3), 175-182.
[http://dx.doi.org/10.1016/0304-3835(93)90060-M] [PMID: 8313352]
[89]
Du, B.W.; Zhang, X.J.; Shi, N.; Peng, T.; Gao, J.B.; Azimova, B.; Zhang, R.; Pu, D.B.; Wang, C.; Abduvaliev, A.; Rakhmanov, A.; Zhang, G.L.; Xiao, W.L.; Wang, F. Luteolin-7-methylether from Leonurus japonicus inhibits estrogen biosynthesis in human ovarian granulosa cells by suppression of aromatase (CYP19). Eur. J. Pharmacol., 2020, 879, 173154.
[http://dx.doi.org/10.1016/j.ejphar.2020.173154] [PMID: 32360836]

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