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Phytoestrogens As Inhibitors of Fungal 17Я-Hydroxysteroid Dehydrogenase

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Phytoestrogens As Inhibitors of Fungal 17Я-Hydroxysteroid Dehydrogenase Steroids 70 (2005) 694–703 Phytoestrogens as inhibitors of fungal 17␤-hydroxysteroid dehydrogenase Katja Kristan a, Katja Krajnc b, Janez Konc b, Stanislav Gobec b, Jure Stojan a, Tea Lanisnikˇ Riznerˇ a,∗ a Institute of Biochemistry, Medical Faculty, University of Ljubljana, Vrazov trg 2, 1000 Ljubljana, Slovenia b Faculty of Pharmacy, University of Ljubljana, Aˇskerˇceva 7, 1000 Ljubljana, Slovenia Received 3 November 2004; received in revised form 25 February 2005; accepted 28 February 2005 Available online 4 June 2005 Abstract Different phytoestrogens were tested as inhibitors of 17␤-hydroxysteroid dehydrogenase from the fungus Cochliobolus lunatus (17␤- HSDcl), a member of the short-chain dehydrogenase/reductase superfamily. Phytoestrogens inhibited the oxidation of 100 ␮M17␤- hydroxyestra-4-en-3-one and the reduction of 100 ␮M estra-4-en-3,17-dione, the best substrate pair known. The best inhibitors of oxidation, with IC50 below 1 ␮M, were flavones hydroxylated at positions 3, 5 and 7: 3-hydroxyflavone, 3,7-dihydroxyflavone, 5,7-dihydroxyflavone (chrysin) and 5-hydroxyflavone, together with 5-methoxyflavone. The best inhibitors of reduction were less potent; 3-hydroxyflavone, 5- methoxyflavone, coumestrol, 3,5,7,4 -tetrahydroxyflavone (kaempferol) and 5-hydroxyflavone all had IC50 values between 1 and 5 ␮M. Docking the representative inhibitors chrysin and kaempferol into the active site of 17␤-HSDcl revealed the possible binding mode, in which they are sandwiched between the nicotinamide moiety and Tyr212. The structural features of phytoestrogens, inhibitors of both oxidation and reduction catalyzed by the fungal 17␤-HSD, are similar to the reported structural features of phytoestrogen inhibitors of human 17␤-HSD types 1 and 2. © 2005 Elsevier Inc. All rights reserved. Keywords: Phytoestrogens; Flavonoids; Hydroxysteroid dehydrogenase; Short-chain dehydrogenase/reductase superfamily; Fungi; Cochliobolus lunatus 1. Introduction ductases (4HNR) from Magnaporthe grisea, Ophiostoma floccosum and other fungi involved in melanin biosynthesis 17␤-Hydroxysteroid dehydrogenase from the filamentous [2]. Sequence similarity was found also to bacterial 7␣-HSD fungus Cochliobolus lunatus (17␤-HSDcl) is an NADPH- and even to human 17␤-HSD types 4 and 8 [2]. dependent enzyme that catalyses the oxidoreduction prefer- We are studying 17␤-HSDcl as a model enzyme of the entially of estrogens and androgens, with estra-4-en-3,17- SDR superfamily. This superfamily includes about 3000 en- dione and 17␤-hydroxyestra-4-en-3-one as the best pair of zymes involved in steroid hormone metabolism, fatty acid substrates [1]. The enzyme belongs to the short-chain de- oxidation and biotransformation of xenobiotics [3]. HSDs hydrogenase/reductase superfamily (SDR) [2]. It possesses a from the SDR superfamily are implicated in the develop- high percentage of sequence identity to fungal ketoreductases ment of polycystic kidney disease [4], regulation of blood – the versicolorin reductases from Aspergillus parasiticus and pressure [5], Alzheimer’s disease [6], obesity [7] and steroid- Emericella nidulans (Ver-1 and Ver-A) involved in myco- dependent forms of cancer [8]. Of the hormone-dependent toxin biosynthesis – and to the 1,3,8-trihydroxynaphthalene forms of cancer, huge geographical differences in incidence reductases (3HNR) and 1,3,6,8-tetrahydroxynaphthalene re- were reported for breast, endometrial and prostate cancer [9]. The incidence of these diseases is much higher in Northern ∗ Corresponding author. Tel.: +386 1543 7657; fax: +386 1543 7641. Europe and USA than in Asia [9,10]. These differences were E-mail address: [email protected] (T.L. Rizner).ˇ correlated with environmental and dietary factors, especially 0039-128X/$ – see front matter © 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.steroids.2005.02.023 K. Kristan et al. / Steroids 70 (2005) 694–703 695 with phytoestrogens that are abundant in soy products, a ma- [31]. The enzyme was homogeneous by SDS-PAGE with jor component of the Asian diet [9,10]. Coomassie blue staining. Phytoestrogens are plant-derived, non-steroidal com- pounds with estrogenic activity that can be divided into 2.3. Enzyme assay three structural groups: flavonoids, coumestans and lignans. Flavonoids comprise flavones, flavanones and isoflavones Phytoestrogens were tested for their inhibitory action [11]. Phytoestrogens possess antiviral, anti-inflammatory, an- against recombinant 17␤-HSDcl. 17␤-HSDcl catalyzes the timutagenic and anticarcinogenic activities [12] and have dif- oxidation of 17␤-hydroxyestra-4-en-3-one to estra-4-en- ferent mechanisms of action. They can interfere with the com- 3,17-dione in the presence of NADP+ and the reduction of plex human endocrine system in several ways: estra-4-en-3,17-dione to 17␤-hydroxyestra-4-en-3-one in the presence of coenzyme NADPH. The reaction was followed (1) they can act as agonists or antagonists of estrogen recep- spectrophotometrically by measuring NADPH concentration tors (ER␣ and ER␤), pregnane X receptor and constitu- (absorbance at 340 nm) in the absence and presence of dif- tive androstane receptor [13], ferent phytoestrogens. Assays were carried out in 0.6 ml sys- (2) they have stimulatory effects on hepatic sex hormone tems in 100 mM phosphate buffer, pH 8.0, containing 1% binding globulin (SHBG), DMSO as co-solvent, as described earlier [32]. Both the sub- (3) they inhibit tyrosine kinase, and thus, prevent growth strate and the coenzyme were 100 ␮M, the concentrations factor-mediated stimulation of proliferation, of inhibitors were from 0.1 to 100 ␮M and the enzyme was (4) they modulate activity of the key enzymes in the biosyn- 0.5 ␮M. Initial velocities were calculated and percentage in- thesis and metabolism of steroid hormones [14] and in hibition was given by 100 − [(v (with inhibitor)/v (without this manner act at the pre-receptor level. 0 0 inhibitor)) × 100]. IC50 values were determined graphically Among steroid metabolizing enzymes, the inhibitory ef- from a plot of log10 (inhibitor concentration) versus percent- fect of phytoestrogens has been studied against aromatase, age inhibition using GraphPad Prism Version4.00 (GraphPad sulfatase, sulfotransferases, 5␣-reductase, 3␤-HSD 5/4 Software Inc.). isomerase, 11␤-HSD type 1 and 17␤-HSDs [12,15–20].Phy- toestrogens were shown to inhibit human 17␤-HSD types 1, 2.4. Docking of kaempferol and chrysin into the active 2, 3 and 5 [21–28]. There are, however, no reports on phytoe- site of 17β–HSDcl and 17β-HSD type 1 strogen inhibition of other human 17␤-HSD isoforms (types 4, 7, 8, 10 or 11) [29,30]. Docking was performed using Autodock3 computer In this work, we examined the action of phytoestrogens program [33]. Homology built model of 17␤-HSDcl was at the pre-receptor level by testing their inhibitory poten- used with Kollman charges and solvent parameters added tial towards the fungal 17␤-HSD. We tested the inhibitory by Autodock. The ligands kaempferol and chrysin were action of flavones, flavanones, isoflavones, coumestans and modeled with Molden [34] and further refined by Gaussian coumarins, two plant-derived organic acids, one mycotoxin 03 in vacuum. Planar structures were obtained which were and three synthetic estrogens/antiestrogens. Of these, coume- then submitted for docking as rigid bodies. Additionally, strol and different hydroxylated flavones exerted the highest CHARMM [35] force field parameters, reproducing ab initio inhibitory action. geometry were worked out. Prior to docking of the two inhibitors, the coenzyme molecule had to be added. We used, as a template, the position of NADPH from the structure 2. Experimental of the complex between THNR, coenzyme and tricyclazole (1YBV). After insertion of the coenzyme, it was relaxed in a 2.1. Phytoestrogens, substrates and cofactors constrained protein by using molecular mechanics optimiza- tion routines (50 steps of steepest descent, SD, followed Phytoestrogens originally purchased from ICN Biochem- by 50 steps of Gauss–Newton, ABNR). Subsequently, the icals GmbH, Steraloids Inc. and Sigma Aldrich Chemie complex structure was refined by 30 steps of Gauss–Newton GmbH were the kind gift of Dr. Jerzy Adamski (GSF, optimization using QMMM algorithm, without any con- Neuherberg, Germany). Substrates estra-4-en-3,17-dione and strains (QM atoms: Tyr, coenzyme). After docking of 17␤-hydroxyestra-4-en-3-one and coenzymes NADP+ and inhibitors, CHARMM molecular simulation program was NADPH were from Sigma Aldrich Chemie, GmbH. employed once again: molecular mechanics relaxation of coenzyme and inhibitor, followed by QMMM optimiza- 2.2. Preparation of recombinant 17β-HSDcl tion without any constrains (QM atoms: Tyr, coenzyme, inhibitor). We repeated this procedure for both the oxidized 17␤-HSDcl was expressed as a GST-fusion protein in Es- and the reduced coenzyme forms. The charges and solvent cherichia coli BL21 cells and purified as previously described parameters for the two coenzyme forms were generated by [2]. Protein concentration of the enzyme preparation was Autodock while the charges for the inhibitors were taken determined by the Bradford method with BSA as standard from Gaussian minimization. In all quantum mechanical 696 K. Kristan et al. / Steroids 70 (2005) 694–703 calculations with Gaussian and CHARMM, we used 6–31 g 100 ␮M coenzyme NADP+ (Table 1). The most effective in- basis set. hibitors, with IC50 around 1 ␮M were: 3-hydroxyflavone, 3,7- Also, docking of kaempferol into the crystal structure of dihydroxyflavone, 5-methoxyflavone, 5,7-dihydroxyflavone ␤ human 17 -HSD type 1 (PDB code 1EQU) was performed (chrysin) and 5-hydroxyflavone. Inhibitors with IC50 be- as described above. The atomic coordinates of docked in- tween 1 and 10 ␮M were: flavone, quercetin, kaempferol, hibitors into the 17␤-HSDcl model and the crystal structure apigenin, coumestrol and biochanin A. Others, luteolin, 7- of 17␤-HSD type 1 can be downloaded from the website hydroxyflavone, flavanone, naringenin and mycoestrogen ∼ http://www2.mf.uni-lj.si/ stojan/stojan.html. zearalenone had IC50 values above 10 ␮M(Table 1). Flavones hydroxylated at positions 3, 5 and 7 or methoxy- lated at position 5 were the best inhibitors in the oxidative di- 3.
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