Potency of a Novel Saw Palmetto Ethanol Extract, SPET-085, for Inhibition of 5α-Reductase II
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1 Adv Ther (2010) 27(7): 9. DOI /s ORIGINAL RESEARCH Potency of a Novel Saw Palmetto Ethanol Extract, SPET-085, for Inhibition of 5α-Reductase II Pilar Pais Received: May 7, 2010 / Published online: Springer Healthcare 2010 ABSTRACT Introduction: The nicotinamide adenine dinucleotide phosphate (NADPH)-dependent membrane protein 5α-reductase irreversibly catalyses the conversion of testosterone to the most potent androgen, 5α-dihydrotestosterone (DHT). In humans, two 5α-reductase isoenyzmes are expressed: type I and type II. Type II is found primarily in prostate tissue. Saw palmetto extract (SPE) has been widely used for the treatment of lower urinary tract symptoms secondary to benign prostatic hyperplasia (BPH). The mechanisms of the pharmacological effects of SPE include the inhibition of 5α-reductase, among other actions. Clinical studies of SPE have been equivocal, with some showing significant results and others not. These inconsistent results may be due, in part, to varying bioactivities of the SPE used in the studies. Methods: The aim of the present study was to determine the in vitro potency of a novel saw palmetto ethanol extract (SPET- 085), an inhibitor of the 5α-reductase isoenzyme type II, in a cell-free test system. On the basis of the enzymatic conversion of the substrate androstenedione to the 5α-reduced product 5α-androstanedione, the inhibitory potency was measured and compared to those of finasteride, an approved 5α-reductase inhibitor. Results: SPET-085 concentration-dependently inhibited 5α-reductase type II in vitro (IC 50 =2.88±0.45 μg/ml). The approved 5α-reductase inhibitor, finasteride, tested as positive control, led to 61% inhibition of 5α-reductase type II. Conclusion: SPET-085 effectively inhibits the enzyme that has been linked to BPH, and the amount of extract required for activity is very low compared to data reported for other extracts. It can be concluded from data in the literature that SPET-085 is as effective as a hexane extract of saw palmetto that exhibited the highest levels of bioactivity, and is more effective than other SPEs tested. This study confirmed that SPET-085 has prostate healthpromoting bioactivity that also corresponds favorably to that reported for the established prescription drug standard of therapy, finasteride. Pilar Pais ( ) Euromed, C/Rec de Dalt, 21-23, Mollet del Vallès, Barcelona, Spain. ppais@euromed.es Keywords: benign prostatic hyperplasia; prostate; saw palmetto ethanol extract; SPET- 085; 5α-reductase
2 2 Adv Ther (2010) 27(7): 9. INTRODUCTION Background on 5α-Reductase and Androgen Biosynthesis The nicotinamide adenine dinucleotide phosphate (NADPH)-dependent membrane protein 5α-reductase irreversibly catalyses the reduction of 4-en-3-oxosteroids, resulting in the corresponding 5α-3-oxosteroids. The conversion of testosterone to the most potent androgen, 5α-dihydrotestosterone (DHT), which displays the highest affinity towards the androgen receptor, is the most important reaction in this process. The irreversible reduction of testosterone to DHT represents the final step in androgen biosynthesis. In humans, two 5α-reductase isoenyzmes are expressed: type I and type II. These isoenzymes have a different pattern of distribution, which is still being elucidated. Type I is predominantly expressed in skin, scalp and follicles; type II is found primarily in prostate tissue. Recent reports indicate that type I is the predominant form in oil and sweat glands. In stroma and basal cells of the prostate, type II is expressed, but in epithelial cells of the prostate type I is also expressed. 1 To investigate whether the two known 5α-reductase isoenzymes were expressed in prostate tissue, Boudon et al. performed specific enzyme amplification after reverse transcription which showed the presence of 274 and 383 base pair fragments that were specific for 5α-reductase type I and type II, respectively, demonstrating the expression of mrna for both isoenzymes in enlarged prostate tissue. These results provide further evidence that 5α-reductase type II activity is primarily responsible for DHT production by human prostatic cells. 2 In a later study, Shirakawa et al. demonstrated that 5α-reductase type I has specific enzyme activity in the prostate, supporting the hypothesis that the type I isoenzyme may play a significant role in maintaining prostate enlargement, along with the type II isoenzyme. 1 Clinical Applications Benign Prostatic Hyperplasia (BPH) The prostate gland has only one known function: to secrete fluid that contains substances needed for reproduction. This requires an extremely high tissue concentration of androgens. 3 BPH is the most common benign proliferative disorder of unknown etiology found in men, affecting over 50% of males above the age of 70 years. It confers its morbidity through potentially bothersome lower urinary tract symptoms that can include urinary hesitancy, weak urine stream, nocturia, incontinence, and recurrent urinary tract infections. 4 Dysregulation of testosterone s conversion to DHT by 5α-reductase has been described as a key step in the development of BPH, and elevated DHT levels correlate with the pathogenesis and progression of androgendependent diseases such as prostate cancer and BPH. BPH seems to be related to the longterm exposure of the prostate to DHT and, possibly, to estrogens. The relation between prostate cancer and androgens is suggested to be U shaped, with both extremes of androgen concentrations being associated with increased risk of invasive cancer. 3 BPH has been successfully treated with drugs (5α-reductase inhibitors) that lower the level of DHT available to prostate tissue by blocking the action of the 5α-reductase that converts testosterone into DHT. Treatments for BPH also include drugs such as alphaadrenergic receptor blockers, minimally invasive therapies that use heat to damage or
3 Adv Ther (2010) 27(7): 9. 3 destroy prostate issue, and surgery, including transurethral resection of the prostate. Dietary supplements for promoting prostate health are gaining popularity in the USA. Evidence shows that the herbal agents saw palmetto extract (SPE), rye grass pollen extract, and pygeum relieve symptoms of BPH. 4,5 SPE and BPH SPE is the phytotherapeutic agent most frequently used for the treatment of lower urinary tract symptoms secondary to BPH. The mechanisms of the pharmacological effects of SPE include the inhibition of 5α-reductase, antiandrogenic effects, antiproliferative effects, and anti-inflammatory effects. 6 There are many types of SPEs available today, featuring a number of different extraction processes, and there is evidence to suggest that this may result in different levels of BPH-related bioactivity among the various extracts. In a recent in-vitro comparison of the potency of different brands of SPE products, all extracts tested, albeit variably, were able to inhibit both isoforms of 5α-reductase. However, the potency of the extracts appeared to be very different, as well as the potencies of two different batches of the same extract, a result probably due to qualitative and quantitative differences in the active ingredients. The investigators concluded that the extract product of each company must therefore be tested to evaluate clinical efficacy and bioactivity. 7 Clinical studies of SPE have been equivocal, with some showing significant results and others not. These inconsistent results may be due, in part, to varying bioactivities of the SPEs used in the studies. 4,8,9 In order to expand upon the findings reported in the literature, the goal of the present study was to confirm the ability of a novel saw palmetto ethanol extract (SPET) to bind to the enzyme that has been linked to BPH. Specifically, to determine the in-vitro potency of a SPET-085 (SPET-085 is a proprietary SPE manufactured by Euromed SA, Barcelona, Spain), an inhibitor of the 5α-reductase isoenzyme type II, in a cell-free test system. MATERIALS AND METHODS Homogenates containing 5α-reductase isoenzyme II were isolated from transfected human embryonic kidney cells (HEK293), stably expressing the 5α-reductase isoenzyme type II (HEK293-5α2=HEK II). 10,11 On the basis of the enzymatic conversion of the substrate androstenedione to the 5α-reduced product 5α-androstanedione, the inhibitory potency was measured and compared to those of finasteride, an approved 5α-reductase inhibitor. 2,12 Cell Culture HEK II cells were cultivated in Dulbecco s modified eagle medium (DMEM) (ph 7.4) with 10% fetal calf serum (FCS), penicillin/ streptomycin (100 U/mL and 100 μg/ml, respectively) and 0.5 mg/ml of geneticin-418- sulfate in a humidified 5% CO 2 atmosphere at 37 C. Preparation of 5α-Reductase Type I-Containing Cell Fractions For the cell-free in-vitro assays, HEK II cells were harvested, freed from the culture medium by centrifugation (500 g) and resuspended in a homogenate buffer consisting of 50 mm Tris- HCl (ph 7.4), 300 mm saccharose, 0.1 mm ethylenediamine tetra-acetic acid (EDTA), 10 mm dithiothreitol (DTT) and 100 μm phenylmethanesulfonyl fluoride (PMSF). By freezing at 196 C and thawing on ice, the cells were solubilized. After an incubation period of 30 minutes at 4 C with 1 mg/ml DNAse in 50 mm MgCl2 and vigorous shaking
4 4 Adv Ther (2010) 27(7): 9. inbetween, the obtained homogenate was centrifuged at 20,200 g in a refrigerated centrifuge for 50 minutes at 4 C. The pellet was resuspended in homogenate buffer and centrifuged again at 20,200 g for 30 minutes at 4 C. This procedure was repeated twice. The homogenate pellet was detached from the tube bottom with homogenate buffer, and resuspended by ultra-turrax mixing at the highest speed. Protein content was quantified according to the method of Bradford using the commercially available RotiQuant reagent. The fractionated cell suspension was aliquoted and stored at 80 C. Cell-Free In-Vitro Inhibition Assays SPET-085, provided as fluid extract, was diluted to working solutions of fivefold higher strength than the intended test dilutions: SPET-085 extract was dissolved in EtOH at a concentration of 0.25 g/ml. As the stock solution was not soluble in sodium citrate assay buffer, dilutions of the extract were prepared as follows: the stock solution was first diluted in phosphate-buffered saline (PBS) and NaOH added until the test item was dissolved (ph in the range, 10.7 to 12.2). The predilution (with a concentration of 0.5 mg/ml) was used to prepare the respective fivefold concentrated test item starting solutions. Before application, aliquots of test item starting solutions were diluted with sodium citrate buffer (ph 5.5) to the intended final test concentration in order to check the final solubility as well as the ph values again. The final solvent concentration was 0.03% EtOH. Incubations were performed at 37 C in a sodium citrate buffer incubation mixture with a final volume of 250 μl containing 0.24 mm NADPH, 250 nm androstenedione, 10 μg cell homogenate and inhibitor dilutions. Finasteride, used as internal control, was dissolved in EtOH, further diluted in PBS, and tested at a final concentration of 6 nm. Solvent-treated controls were handled the same way and contained 0.2% EtOH and 0.1% dimethylsulfoxide (DMSO) (concentration finding) or 0.02% EtOH and 0.01% DMSO (half maximal inhibitory concentration [IC 50 ] determination), respectively. The enzyme reactions were started by the addition of cellular homogenates. Incubations were stopped after 15 minutes by the addition of 50 μl 10 N NaOH and were shaken at 800 rpm. For the extraction of product and nonconverted substrate, 600 μl ethyl acetate containing the internal standard griseofulvin (ISTD, 0.03 μm) were added to each sample. After 10 minutes of shaking, samples were centrifuged (5 minutes at approximately 4800 g) and the ethyl acetate supernatant pipetted into fresh cups. The solvent was evaporated and the dried residues were reconstituted in 35 μl of methanol and subsequently subjected to liquid chromatography/mass spectrometry. The injection volume per sample was 12 μl. Liquid Chromatography/Mass Spectrometry (LC/MS) The high-pressure liquid chromatography (HPLC) system consisted of a MS Plus pump and an Autosampler Plus (Surveyor; Thermo Fisher Scientific, Rockford, IL, USA). MS was performed on a TSQ Quantum Discovery Max triplequadrupole mass spectrometer equipped with an APCI interface (Thermo Fisher Scientific) connected to a PC running the standard software Xcalibur (Xcalibur, Inc., Reston, VA, USA). Full scan mass spectra were acquired in the positive mode using syringe pump infusion to identify the protonated quasimolecular ions [M+H]+. Autotuning was
5 Adv Ther (2010) 27(7): 9. 5 carried out for maximizing ion abundance followed by the identification of characteristic fragment ions using a generic parameter set: APCI vaporizer temperature 400 C, ion transfer capillary temperature 350 C, discharge current setting 5.0, collision gas 0.8 mbar argon, sheath gas, ion sweep gas and aux gas pressure were 30, 2 and 8 (arbitrary units), respectively. Ions with the highest signal-to-noise ratio were used to quantify the item in the selected reaction monitoring mode and as qualifier, respectively. The pump flow rate was set to 300 μl/min and the compounds separated on a Gemini C6-Phenyl, 3 μm, mm (Phenomenex, Aschaffenburg, Germany) analytical column with a precolumn (Gemini C6-Phenyl, 3 μm, mm; Phenomenex) using the gradients presented in Table 1 to detect the test items. The organic component consisted of acetonitrile/0.1% (v/v) formic acid, and the aqueous component consisted of 10 mm ammonium formate/0.5% formic acid. MS and chromatographic parameters are displayed in Table 2. Data Analysis Results were displayed as peak area ratio (area of the analyte peak divided by the area of the internal standard peak). Conversion rates were calculated according to the following formula: conversion (%)=(area ratio androstenedione 100)/ (area ratio androstenedione+area ratio 5α-androstanedione). Inhibition rates, expressed as percent inhibition values relative to untreated controls, were calculated out of the mean conversion rates with and without inhibitor (n=2 each). The IC 50 values were calculated by linear interpolation of the concentrations (conc) of test compounds, and the corresponding percentage of inhibition (inh) that bracket 50%: IC 50 =(50% low inh %)/(high inh % low inh %) (high conc low conc)+low conc. Table 1. High-pressure liquid chromatography gradients for test and reference items. Mobile phase Androstenedione, 5α-androstanedione 0 minutes 0.2 minutes 1 minute 2.5 minutes 2.6 minutes 4.0 minutes A (%) B (%) A=acetonitrile/0.1% (v/v) formic acid. B=10 mm ammonium formate/0.5% formic acid. Table 2. Mass spectrometry and chromatographic parameters for test and reference items. Test item Androstenedione 5α-Androstanedione ISTD (griseofulvin) Molecular weight 0 minutes [M+H] (m/z) 0.2 minutes Monitoring ion (m/z) 1 minute ISTD=internal standard griseofulvin; m/z=mass to charge ratio. Scan time (seconds) 2.5 minutes Collision energy (V) 2.6 minutes Retention time (minutes) 4.0 minutes
6 6 Adv Ther (2010) 27(7): 9. The results obtained from the cell-free IC 50 determination experiment are shown in Figure 1. SPET-085 was a potent inhibitor of 5α-reductase type II in vitro with an IC 50 of 2.88±0.45 μg/ml. The approved 5α-reductase inhibitor, finasteride, was tested as positive control for the cell-free experiments at 6 nm, and led to 61% inhibition of 5α-reductase type II. The doseresponse curve for finasteride obtained with the cell homogenate used for the assays is displayed in Figure 2. DISCUSSION Quality Control Acceptability of the Assays A positive control inhibitor was included in the assay setup. The in-vitro assays were considered to be acceptable if they met the following criteria: 60% inhibition of 5α-reductase type II by finasteride at a concentration of 6 nm for the cell-free test system. RESULTS Assay Results SPET-085 was tested in vitro for the inhibitory potential towards 5α-reductase type II in a cellfree assay using cell homogenates isolated from stably transfected HEK293 cells. SPET-085 was tested at the following final concentrations: 10, 5, 2.5, 1.25, 1, and 0.5 μg/ml. As stated in the objectives for this study, the novel saw palmetto ethanol extract, SPET-085, was tested in vitro for the inhibitory potential towards 5α-reductase type II in a cell-free assay using cell homogenates isolated from stably transfected HEK293 cells. SPET-085 concentration-dependently inhibited 5α-reductase type II in vitro. For this extract, an IC 50 value of 2.88±0.45 μg/ml was determined. The approved 5α-reductase inhibitor, finasteride, was tested as positive control for the cell-free experiments at 6 nm, and led to 61% inhibition of 5α-reductase type II. The phytotherapeutic agent SPE is an effective dual inhibitor of 5α-reductase isoenzyme activity in the prostate. Unlike other inhibitors, SPE induces its effects without interfering with the cellular capacity to secrete prostate-specific antigen (PSA). In a recent study published by Abe et al., the bioactive compounds contained in hexane and diethyl ether extracts of saw palmetto were isolated and characterized. The components (oleic acid and lauric acid) were tested for their in-vitro potency towards 5α-reductase using female rat liver microsomes as a protein source and testosterone as substrate. Using this approach, IC 50 values in the range of μg/ml were determined. 6
7 Adv Ther (2010) 27(7): 9. 7 Habib et al. assessed 5α-reductase type II inhibition by SPE in a cell-based system. SPE at 10 μg/ml markedly inhibited the activity of 5α-reductase type II by 76%. 13 In another recent trial, different brands of SPEs were tested for their inhibitory potential towards 5α-reductase types I and II, using prostatic fibroblast and epithelial cells as enzyme source. All extracts tested inhibited 5α-reductase, although the potency of the extracts appeared to be very different, resulting in IC 50 values in the range of 3.8 to 908 mg/l. The most potent product in this study was a hexane extract of saw palmetto, for which IC 50 values of and mg/l (different batches) were determined. 7 Randomized clinical studies of SPE, alone or in combination with other plant extracts, have provided the strongest evidence for its competitive efficacy and tolerability in the treatment of BPH. SPE appears to be a useful option for improving lower urinary tract symptoms and flow measures. Hypoxis rooperi and Secale cereale also appear to improve BPH symptoms, although the evidence is less strong for these products. 14 In patients with BPH, moreover, saw palmetto relieves urinary symptoms as effectively as the pharmaceutical 5α-reductase inhibitor, finasteride. In addition to inhibiting 5α-reductase activity, saw palmetto possesses anti-inflammatory properties that may also have complementary effects on prostate health. 3 Gerber et al. assessed the efficacy of 160 mg of SPE given twice daily for 2 years to patients with BPH. At each 6-month evaluation, patients quality of life and maximum urinary flow had improved, and both prostate size and symptoms had decreased. The study participants reported that sexual function remained stable for the first year of treatment and significantly improved during the second year. 15 Another study examined men aged 45 or older with moderate to severe symptoms of BPH. After receiving placebo for 1 month, the men were randomly assigned to receive either SPE or placebo for an additional 6 months. The
8 8 Adv Ther (2010) 27(7): 9. saw palmetto group experienced a significant decrease in its prostate symptom scores. Moreover, its quality of life scores in the group receiving SPE increased to a greater degree than in those taking placebo. The researchers concluded that SPE significantly improved urinary symptoms compared to placebo. 15 A recent prospective study utilized three arms: SPE 320 mg per day (n=20), the selective alpha-blocker tamsulosin 0.4 mg per day (n=20), and SPE+tamsulosin (n=20) to assess the superiority or equivalence among these treatment regimens in BPH. Both SPE and tamsulosin were effective alone. No treatment demonstrated superiority over another, and combined therapy did not provide extra benefits. The investigators concluded that SPE is a well-tolerated agent that can be used in the treatment of urinary tract symptoms due to BPH. 16 Overall, however, clinical studies of SPE have been equivocal, with some showing significant results and others not. These inconsistent results may, in part, be due to the varying bioactivities of the SPEs used in the studies. 4,8,9 A European study showed that half of German urologists preferred SPE to pharmaceutical agents for the treatment of BPH. 17 A Cochrane review concluded that SPE produces mild to moderate improvement in urinary symptoms and flow measures that is comparable to that reported for finasteride. 18 However, a more recent high-quality, randomized controlled trial found no benefit with SPE in symptom relief or urinary flow measures after 1 year of therapy. 5 Future randomized controlled trials using standardized preparations of phytotherapeutic agents with longer study durations are needed to determine their long-term effectiveness in the treatment of BPH. CONCLUSION SPET-085 tested in this study concentrationdependently inhibited 5α-reductase type II in vitro. SPET-085 effectively inhibits the enzyme that has been linked to BPH, and the amount of extract required for activity is very low compared to data reported in similar tests with other extracts. It can be concluded from data in the literature that SPET-085 is as effective as a hexane extract of saw palmetto that exhibited the highest levels of bioactivity, and is more effective than other SPEs tested. This study confirmed that SPET-085 has prostate health-promoting bioactivity at a level that is superior to that of many other extracts. The bioactivity of SPET-085 corresponds favorably to that reported for the hexane extract that has been used in many of the positive saw palmetto BPH clinical trials, as well as to the established prescription drug standard of therapy, finasteride. ACKNOWLEDGMENTS This study was sponsored by Euromed, Barcelona, Spain. The author wishes to thank Pharmacelsus, Saarbrücken, Germany for their contributions to the design and conduct of this study, data analyses and data reporting; and Aesculapius Communications, Inc. for editorial assistance in the preparation of this manuscript. Support for this assistance was provided by Euromed. REFERENCES Shirakawa T, Okada H, Acharya B, et al. Messenger RNA levels and enzyme activities of 5 alphareductase types 1 and 2 in human benign prostatic hyperplasia (BPH) tissue. Prostate. 2004:58; Boudon C, Lobaccaro JM. 5 alpha-reductase activity in cultured epithelial and stromal cells
9 Adv Ther (2010) 27(7): from normal and hyperplastic human prostates effect of finasteride (Proscar), a 5 alpha-reductase inhibitor. Cell Mol Biol. 1995;41: Comhaire F Mahmoud A. Preventing diseases of the prostate in the elderly using hormones and nutriceuticals. Aging Male. 2004;7: and selective inhibitors. Proc Natl Acad Sci U S A. 2001;16: Anderson S, Russell DW. Structural and biochemical properties of cloned and expressed human and rat steroid 5α-reductases. Proc Natl Acad Sci U S A. 1990;87: Lee J, Andriole G, Avins A, et al. Redesigning a large-scale clinical trial in response to negative external trial results: the CAMUS study of phytotherapy for benign prostatic hyperplasia. Clin Trials. 2009;6: Edwards JL. Diagnosis and management of benign prostatic hyperplasia. Am Fam Physician. 2008;77: Delos S, Lehle C, Martin PM, et al. Inhibition of the activity of basic 5 alpha-reductase (type 1) detected in DU 145 cells and expressed in insect cells. Steroid Biochem Mol Biol. 1994;48: Habib FK, Ross M, Ho CK, et al. Serenoa repens (Permixon) inhibits the 5 alpha-reductase activity of human prostate cancer cell lines without interfering with PSA expression. Int J Cancer. 2005;114: Abe M, Ito Y, Suzuki A, et al. Isolation and pharmacologic characterization of fatty acids from saw palmetto extract. Anal Sci. 2009;25: Wilt TJ, Ishani A, Rutks I, MacDonald R. Phytotherapy for benign prostatic hyperplasia. Public Health Nutr. 2000;3: Scaglione F, Lucini V, Pannacci M, et al. Comparison of the potency of different brands of Serenoa repens extract on 5alpha-reductase types I and II in prostatic co-cultured epithelial and fibroblast cells. Pharmacology. 2008;82: Bent S, Kane C, Shinohara K, et al. Saw palmetto for benign prostatic hyperplasia. N Engl J Med. 2006;354: Gerber GS, Kuznetsov D. Randomized, double-blind, placebo-controlled trial of saw palmetto in men with lower urinary tract infections. Urology. 2001;58: Hizli F, Uygur MC. A prospective study of the efficacy of Serenoa repens, tamsulosin, and Serenoa repens plus tamsulosin treatment for patients with benign prostate hyperplasia. Int Urol Nephrol. 2007;39: Log T. Serenoa repens in benign prostatic hyperplasia. Tidsskr Nor Laegeforen. 2008;128: Article in Norwegian. 17. Lowe FC, Ku JC. Phytotherapy in treatment of benign prostatic hyperplasia: a critical review. Urology. 1996;48: Reichert W, Harmann RW, Jose J. Stable expression of the human 5alpha-reductase isoenzymes type I and type II in HEK293 cells to identify dual 18. Wilt T, Ishani A, MacDonald R. Serenoa repens for benign prostatic hyperplasia. Cochrane database Syst Rev. 2002;(3):CD
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