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192435859.Pdf European Journal of Pharmacology 691 (2012) 275–282 Contents lists available at SciVerse ScienceDirect European Journal of Pharmacology journal homepage: www.elsevier.com/locate/ejphar Endocrine pharmacology Egonol gentiobioside and egonol gentiotrioside from Styrax perkinsiae promote the biosynthesis of estrogen by aromatase Danfeng Lu, Lijuan Yang, Qilin Li, Xiaoping Gao, Fei Wang n, Guolin Zhang nn Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, PR China article info abstract Article history: Estrogen deficiency is associated with a variety of diseases, including osteoporosis, atherosclerosis, and Received 11 May 2012 Alzheimer’s disease. Aromatase cytochrome P450 is the only enzyme in vertebrates known to catalyze Received in revised form the biosynthesis of estrogens from androgens. Inhibitors of aromatase have been developed for the 2 July 2012 treatment of estrogen-dependent breast cancer. However, small molecular agonists of aromatase, Accepted 2 July 2012 which would be useful to locally promote estrogen biosynthesis for the prevention of estrogen Available online 13 July 2012 deficiency-induced diseases, are rarely reported. In this study, we established a nonradioactive assay Keywords: for measuring aromatase activity by using human ovarian granulosa KGN cells and identified two Egonol estrogen biosynthesis-promoting compounds, egonol gentiobioside and egonol gentiotrioside from Estrogen Styrax perkinsiae. The compounds also promoted estrogen biosynthesis in 3T3-L1 preadipocyte cells. Aromatase Further study showed that neither compound affected the transcriptional and translational expression Styrax perkinsiae KGN cell line of aromatase in KGN cells, but that both significantly promoted the in vitro enzyme activity of recombinant expressed aromatase. Egonol gentiotrioside was also found to increase the serum estrogen level in ovariectomized rats. These results suggest that these two compounds may promote estrogen biosynthesis through the allosterical regulation of aromatase activity. Egonol gentiobioside and egonol gentiotrioside are, therefore, valuable targets for structural modification and warrant further investiga- tion for their potential as novel pharmaceutical tools for the prevention of estrogen deficiency-induced diseases. & 2012 Elsevier B.V. All rights reserved. 1. Introduction et al., 1995). In adipose cells and osteoblasts, aromatase expression is driven by promoter I.4, which is regulated by class I cytokines (Zhao Estrogens are steroid hormones that regulate growth, differentia- et al., 1995; Shozu and Simpson, 1998). Thus, the regulation of tion, and function in a broad range of target tissues in the body. The estrogen biosynthesis in each tissue site of expression is unique, actions of estrogen are mediated by the estrogen receptors, which are and switches in promoter usage have been found to be associated expressed in a variety of cells and function through genomic or with the incidence of breast cancer (Simpson et al., 1997). nongenomic actions on target genes (Heldring et al., 2007). Estrogen Aromatase inhibitors, such as anastrozole, letrozole, and exe- biosynthesis is catalyzed by aromatase (CYP19A1), which is respon- mestane, have been developed for the treatment of hormone- sible for binding of the C19 androgenic steroid substrate and dependent breast cancer in postmenopausal women since they catalyzing the necessary reactions to form the phenolic A ring show superiority over conventional anti-estrogen receptor drugs characteristic of estrogens (Simpson et al., 2002). In humans, the such as tamoxifen (Johnston and Dowsett, 2003). In comparison expression of aromatase at the various sites is regulated by tissue- with the extensive number of studies dedicated to discovering specific promoters through the use of alternative splicing mechan- new aromatase inhibitors, the search for small molecular aroma- isms (Simpson, 2004). In the ovary and testes, aromatase expression tase agonists that promote estrogen biosynthesis has been small. is mediated by promoter II, which binds the transcription factors Although some herbicides, fungicides, and insecticides have been cAMP-response element binding protein (CREB) and steroidogenic found to promote aromatase expression in a cAMP-dependent or - factor-1. Aromatase expression inthegonadsisthusregulatedby independent manner (Sanderson et al., 2000; You et al., 2001; gonadotropins through the stimulation of cAMP generation (Michael Morinaga et al., 2004), more work is needed to find potent aromatase agonists that produce less side effects. Epidemiological studies have suggested the involvement of estrogen insufficiency in n osteoporosis, neurodegenerative diseases, and cardiovascular dis- Corresponding author. Tel./fax: þ86 28 85256758. nn Corresponding author. Tel./fax: þ86 28 85229901. eases (Deroo and Korach, 2006). Estrogen therapy is an established E-mail addresses: [email protected] (F. Wang), [email protected] (G. Zhang). regimen for the prevention of these diseases, but recent evidence 0014-2999/$ - see front matter & 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.ejphar.2012.07.005 276 D. Lu et al. / European Journal of Pharmacology 691 (2012) 275–282 indicates that its long-term use is accompanied by side effects such 2.4. Cell-based estrogen biosynthesis assay as increased risks of breast, ovarian, and endometrial cancer (Davison and Davis, 2003). Thus, alternative methods that improve KGN cells or 3T3-L1 cells were seeded in 24-well plates the therapeutic efficacy and safety by locally promoting estrogen overnight. The following day, the cells were replaced with biosynthesis should be developed for the prevention and treatment serum-free DMEM/F-12 medium and pretreated with the test of these diseases caused by estrogen deficiency. chemicals for 24 h. Testosterone (10 nM) was then added to each In this study, we established a nonradioactive assay for well, and the cells were incubated for a further 24 h. The culture measuring aromatase activity by using human ovarian granulosa medium and cell lysate were collected and stored at À20 1C. The KGN cells. Two natural products, egonol gentiobioside and egonol 17b-estradiol in the culture medium was quantified using a 17b- gentiotrioside from Styrax perkinsiae, were identified to signifi- estradiol magnetic particle-based ELISA according to the manu- cantly promote estrogen biosynthesis, and their effects on aro- facturer’s instructions. The OD was measured at 550 nm with the matase activity in vitro and in vivo were examined. Verioskan Flash Multimode Reader (Thermo Scientific, Waltham, MA, USA). The results, normalized to the total cellular protein content, were expressed as percentages of the control. Protein determination was carried out with the bicinchoninic acid (BCA) 2. Materials and methods protein assay kit (Bestbio, Shanghai, China). 2.1. Materials 2.5. Recombinant expressed aromatase activity assay Testosterone, formestane, forskolin, dibenzylfluorescein, and An in vitro recombinant expressed aromatase activity assay nilestriol were purchased from Sigma (Shanghai, China), dissolved was conducted as described previously with minor modifications in DMSO to a concentration of 100 mM, and stored at À20 1C. (Stresser et al., 2000; Maiti et al., 2007). In brief, the test The NADPH regenerating system was purchased from Promega compounds (5 l) were preincubated with an NADPH regenerat- (Madison, WI, USA). The recombinant expressed human aroma- m ing system (45 l of 2.6 mM NADPþ , 7.6 mM glucose-6-phos- tase plus reductase was purchased from BD Biosciences (San Jose, m phate, 0.8 U/ml glucose-6-phosphate dehydrogenase, and 1 mg/ml CA, USA). The magnetic particle-based 17b-estradiol enzyme- albumin, in 50 mM potassium phosphate, pH 7.4) for 10 min at linked immunosorbent assay (ELISA) kit was purchased from 37 1Cbefore50 l of the enzyme and substrate mixture (40 pM Bio-Ekon Biotechnology (Beijing, China). Seeds of S. perkinsiae m recombinant aromatase and 0.4 M dibenzylfluorescein in 50 mM were collected from Yongde County within the Yunnan Province m potassium phosphate, pH 7.4) were added. The reaction mixture of China, in August 2003. The seeds were identified by Prof. Xin-fen was then incubated for 2 h at 37 1C to allow the aromatase to Gao of the Chengdu Institute of Biology, Chinese Academy of generate the product and quenched with 37.5 l of 2 N NaOH. The Sciences, based on the Flora Reipublicae Popularis Sinicae, in which m mixture was then shaken for 5 min and incubated for 2 h at 37 1Cto the Engeler system was used for the definition of the plant names. enhance the noise/background ratio. The fluorescence intensity was A voucher specimen (A-157) was deposited in the Herbarium of measured at 485 nm (excitation) and 530 nm (emission). Three the Chengdu Institute of Biology, Chinese Academy of Sciences. independent experiments were performed in duplicate. 2.2. Plant extraction and isolation 2.6. Quantitative real-time RT-PCR The air-dried seeds of S. perkinsiae (1 kg) were extracted with Total cellular RNA was isolated using TRIzol reagent according 75% ethanol (3 Â 8 l) for 1.5 h under reflux. The ethanol solution to the manufacturer’s instructions (Invitrogen). Total RNA (2 mg) was concentrated under reduced pressure. The resulting extract was reverse-transcribed using SuperScript III Reverse Transcrip- (250 g) was suspended in warm H2O (2 l), and then the solution tase (Invitrogen) with oligo(dT)18 primers. Equal amounts (1 ml) was extracted with petroleum
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