Inhibitory Effects of Garcinia cambogia Extract on CYP2B6 Enzyme Activity
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1 Inhibitory Effects of Garcinia cambogia Extract on CYP2B6 Enzyme Activity Authors Jun Sang Yu 1 *, Min Sun Choi 1 *, Jong Suk Park 1, Shaheed Ur Rehman 2, Katsunori Nakamura 3, Hye Hyun Yoo 1 Affiliations 1 Institute of Pharmaceutical Science and Technology and College of Pharmacy, Hanyang University, Ansan, Republic of Korea 2 Department of Pharmacy, COMSATS Institute of Information Technology, Abbottabad, Pakistan 3 Department of Pharmacy, Ryukyu University Hospital, Okinawa, Japan Key words Garcinia cambogia, Clusiaceae, CYP, drug metabolism, drug interaction received September 29, 2016 revised February 9, 2017 accepted February 22, 2017 Bibliography DOI Published online Georg Thieme Verlag KG Stuttgart New York ISSN Correspondence Prof. Dr. Hye Hyun Yoo Institute of Pharmaceutical Science and Technology and College of Pharmacy, Hanyang University 55 Hanyangdaehak-ro, Sangnok-gu, Ansan, Gyeonggi-do 15588, Republic of Korea Phone: ,Fax: yoohh@hanyang.ac.kr Supporting information available online at ABSTRACT This study assessed the inhibitory effects of Garcinia cambogia extract on the cytochrome P450 enzymes in vitro. G. cambogia extract was incubated with cytochrome P450 isozyme-specific substrates in human liver microsomes and recombinant CYP2B6 isozyme, and the formation of the marker metabolites was measured to investigate the inhibitory potential on cytochrome P450 enzyme activities. The results showed that G. cambogia extract has significant inhibitory effects on CYP2B6 activity in a concentration-dependent manner. Furthermore, the inhibition was potentiated following preincubation with NADPH, indicating that G. cambogia extract is a time-dependent inhibitor of CYP2B6. Meanwhile, hydroxycitric acid, the major bioactive ingredient of G. cambogia extract, did not exhibit significant inhibition effects on cytochrome P450 enzyme activities. G. cambogia extract could modulate the pharmacokinetics of CYP2B6 substrate drugs and lead to interactions with those drugs. Therefore, caution may be required with respect to concomitant intake of dietary supplements containing G. cambogia extract with CYP2B6 substrates. ABBREVIATIONS CYP cytochrome P450 HCA hydroxycitric acid MRM multiple reaction monitoring * Jun Sang Yu and Min Sun Choi contributed equally to this work. Introduction Garcinia cambogia L. (Garcinia gummi-gutta L.) is a tropical species of Garcinia belonging to the plant family Clusiaceae. G. cambogia is grown mainly in Southeast Asia and West and Central Africa. G. cambogia fruits have been commonly used in cooking as a food preservative or flavoring agent. It has also been traditionally used for the treatment of constipation, edema, rheumatism, and irregular menstruation in Asian countries [1]. Recently, G. cambogia has gained considerable attention and popularity as a medicinal food for weight loss since G. cambogia extract was introduced as
2 Table 1 Effects of G. cambogia extract on CYP-specific metabolite formation in human liver microsomes (n = 3). P450 isozyme (Specific metabolite) CYP1A2 (Acetaminophen) CYP2A6 (7-OH-Coumarin) CYP2B6 (OH-Bupropion) CYP2C8 (6-OH-paclitaxel) CYP2C9 (4-OH-Diclofenac) CYP2C19 (4-OH-Mephenytoin) CYP2D6 (Dextrophan) (1-OH-Midazolam) (6-β-OH-Testosterone) Data are expressed as the mean ± SD Metabolite formation (% of control) G. cambogia extract (µg/ml) ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 28.7 an exciting breakthrough in natural weight loss [2]. Accordingly, there are many dietary supplement products containing G. cambogia extract on the market. Many studies have investigated the antiobesity effects of G. cambogia extract in experimental animals or humans. HCA is known as a principal bioactive component responsible for the weight-loss effects of G. cambogia [3]. The fruits of G. cambogia contain approximately 10 to 30% HCA as a mineral salt or lactone [4]. It has been reported that HCA reduces weight gain by inhibiting adenosine triphosphate (ATP)-citrate lyase, the enzyme responsible for catalyzing the extra mitochondrial cleavage of citrate to oxaloacetate and acetyl-coenzyme A, a building block of fatty acid synthesis [5]. However, there are many conflicting views on the efficacy and safety of G. cambogia. As for the adverse effects of G. cambogia, it has been reported that G. cambogia has a toxic effect to testis at a high dose [6] and that it has hepatotoxicity [7 10]. One of the most important issues that should be considered in the use of dietary supplements is their interactions with drugs. Such interactions may occur via the modulation by dietary supplements of the pharmacokinetic processes of coadministered drugs. One typical mechanism of modulation is inhibition or induction of CYP, a principal drug-metabolizing enzyme. Therefore, an evaluation of the modulation of CYP activity is necessary to predict any possible interactions of dietary supplements with drugs. In particular, herbal dietary supplements consist of a complex mixture of bioactive ingredients. Therefore, a complete chemical profiling of those products is generally unavailable. Such a complex nature of natural products complicates the evaluation of drug-herb interactions [11]. As mentioned above, G. cambogia extract has become popular as a dietary supplement for the purpose of weight loss in obese individuals. Thus, it is generally taken for long periods. Most obese individuals have risk factors for various chronic diseases, such as diabetes, hypertension, and hyperlipidemia [12], and they may be taking prescription drugs for those diseases. Therefore, the likelihood of concomitant use of prescription drugs and G. cambogia extract is high. However, to our knowledge, no report has investigated the potential effects of G. cambogia extract on CYPmediated drug metabolism. Therefore, in this study, the potential for a drug interaction with G. cambogia extract was investigated based on its inhibition of the activities of the CYP enzyme. Results A CYP inhibition assay was conducted using seven well-known CYP selective inhibitors. The formation of each CYP-specific metabolite was reduced by > 95% by treatment with its corresponding inhibitor, pointing to the validity of the assay system. Subsequently, the inhibitory effects of the G. cambogia extract on eight CYP isozymes were evaluated at concentrations of 1, 3, 10, 30, 100, 300, and 1000 µg/ml. The results are shown in Table 1. TheG. cambogia extract did not show significant inhibitory effects against most of the CYP isozymes tested. At a concentration of 1000 µg/ ml, the activities of the CYP enzyme seemed to be somewhat inhibited, but this was thought to be the result of nonspecific inhi-
3 bition caused by the addition of the high concentration of extract. Among the eight CYP isozymes tested, the inhibition of CYP2B6 was significant and dose dependent. The IC 50 value for CYP2B6 was µg/ml. As the G. cambogia extract inhibited CYP2B6 activity, its inhibitory effects were further evaluated using cdna-expressed CYP2B6 supersomes. The formation of a CYP2B6-specific metabolite (OH-bupropion) at different concentrations of the G. cambogia extract is depicted in Fig. 1. The metabolite formation decreased in a concentration-dependent manner, indicating that the G. cambogia extract inhibited the activity of CYP2B6. Based on inhibition curves, the calculated IC 50 value was µg/ml. In addition, G. cambogia extract was preincubated with CYP2B6 supersomes for 30 min prior to the addition of the substrate, and the inhibition of CYP was measured to investigate whether the extract exerted its activity in a time-dependent manner (i.e., acted as a mechanism-based inactivator). Metabolite formation following preincubation was plotted, together with the results from the experiments without preincubation ( Fig. 1). As shown in Fig. 1, the inhibitory effects of G. cambogia extract were slightly potentiated following preincubation; the calculated IC 50 value was µg/ml. The fold shift in the IC 50 ratio was 1.7. According to a previous report, compounds with a fold shift in the IC 50 ratio of 1.5 can be considered positive in terms of time-dependent inhibition [13]. Thus, G. cambogia extract may act as a time-dependent inhibitor on CYP2B6 and exhibit an irreversible inhibitory effect on CYP2B6-dependent drug metabolism. As HCA is the principal bioactive constituent of G. cambogia extract, its potential role in the inhibition of CYP was evaluated. HCA was tested at concentrations ranging from 0.1 to 100 µm. HCA did not significantly inhibit the activities of CYP enzymes up to a concentration level of 30 µm. At the highest concentration tested (100 µm), HCA showed some inhibition activity against several CYP isozymes, including CYP1A2, CYP2B6, CYP2C8, CYP2C19, and CYP2D6. The inhibition potential was around 50% for all the isozymes mentioned above ( Table 2). Discussion The present results showed that G. cambogia extract had an inhibitory effect on the activity of CYP2B6 isozyme. Although the inhibitory potential of G. cambogia extract was moderate, it functioned as a time-dependent inhibitor, which suggested that the clinical effects of the extract could be greater than those observed in the in vitro assay. According to the labels of some commercial G. cambogia extract products, the recommended daily dose of G. cambogia extract for weight loss is mg, although this can vary, depending on the product or HCA content. No pharmacokinetic data on G. cambogia extracts are available at present. However, if it is assumed that the extract behaves as a single compound, the plasma concentration could reach up to 1 mg/ml or more after taking the extract at the recommended daily dose ( mg). Therefore, considering its IC 50 value (130.9 µg/ ml for CYP2B6 after preincubation), a drug interaction with CYP2B6 is likely in clinical use. Fig. 1 The effect of G. cambogia extract on metabolic activities of CYP2B6 with and without preincubation. G. cambogia extract was incubated in human CYP2B6 supersomes with bupropion in the presence of an NADPH-generating system for 30 min. In addition, the incubation was carried out following 30 min preincubation. The formation of the CYP2B6 specific metabolite was plotted as the percentage of control. In the present study, HCA, the main ingredient of G. cambogia extract, showed some inhibitory effects on the activities of CYP enzymes at the highest concentration tested (100 µm). However, inhibitory activity against several isozymes other than CYP2B6 was observed, demonstrating that the inhibition was not specific to CYP2B6. This finding suggests that components other than HCA may be more responsible for the inhibitory activity of G. cambogia extract against CYP2B6. CYP2B6, a member of the cytochrome P450 family of pharmacogenes, makes up approximately 2 10% of the total hepatic CYP content. CYP2B6 is also expressed in the brain. It may play an important role in the metabolism of drugs by acting on the central nervous system, resulting in neurological side effects of drug treatments [14]. CYP2B6 is responsible for the metabolism of 4% of the top 200 drugs and is known to be highly inducible by xenobiotics [14]. Substrates of CYP2B6 include artemisinin (an antimalarial drug), bupropion and methoxetamine (antidepressants), cyclophosphamide, ifosphamide, and tamoxifen (antitumor drugs), efavirenz and nevirapine (nonnucleoside reverse transcriptase inhibitors of HIV), ketamine and propofol (anesthesia agents), meperidine and methadone (analgesics), mephenytoin and valproic acid (anticonvulsants), prasugrel (antiplatelet agent), and selegiline (Parkinsonʼs disease drug) [15 18]. Considering recent trends in the interest of weight loss and ease of access to dietary supplements for that purpose, it is likely that some of the aforementioned drugs are taken concomitantly with G. cambogia extract. Among the substrates of CYP2B6 noted above, particular attention should be paid to possible interactions of obesity-related drugs, such as antidepressants, common drugs (e.g., analgesics), and drugs used to treat chronic diseases, such as anticonvulsants and antiplatelets, with G. cambogia extract.
4 Table 2 Effects of HCA on CYP-specific metabolite formation in human liver microsomes (n = 3). P450 isozyme (Specific metabolite) CYP1A2 (Acetaminophen) CYP2A6 (7-OH-Coumarin) CYP2B6 (OH-Bupropion) CYP2C8 (6-OH-paclitaxel) CYP2C9 (4-OH-Diclofenac) CYP2C19 (4-OH-Mephenytoin) CYP2D6 (Dextrophan) (1-OH-Midazolam) (6-β-OH-Testosterone) Data are expressed as the mean ± SD In conclusion, G. cambogia extract is a popular dietary supplement used for weight loss worldwide. As the use of G. cambogia as a food supplement continues to grow, there is a high likelihood of concomitant use with prescription drugs. Information regarding its potential in the inhibition of CYP enzymes is not available at present. In this study, we demonstrated that G. cambogia extract inhibited the activity of CYP2B6 isozyme. Further studies are warranted using an in vivo model to confirm CYP inhibition by G. cambogia extract. In the meantime, caution should be exercised when consuming G. cambogia extract with CYP2B6 substrate drugs. Materials and Methods Chemicals Metabolite formation (% of control) HCA (µm) ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.5 G. cambogia extract (Lot no. FBM ) was purchased from the International Biological Material Research Center, Korea Research Institute of Bioscience & Biotechnology, Daejeon, Korea. The extract was prepared by extracting the fruits of G. cambogia with methanol at 45 C for 24 h. A voucher specimen (HY ) was deposited at the Herbarium of the College of Pharmacy, Hnyang University, Ansan, Korea. The extract was standardized to contain 7.8 ± 1.0% of HCA by LC MS/MS analysis. ( )-Calcium hydroxycitrate tribasic (> 97%) was purchased from Sigma-Aldrich Co. Pooled human liver microsomes and cdna-expressed human CYP2B6 supersomes were purchased from BD Gentest. Glucose 6-phosphate (> 98%), β-nadp+ (> 95%), glucose 6-phosphate dehydrogenase, phenacetin (> 8%), acetaminophen (> 99%), coumarin (> 99%), 7-OH-coumarin (> 98%), bupropion (> 98%), (±)-hydroxybupropion (> 98%), paclitaxel (> 95%), 6 - OH-paclitaxel (> 98%), diclofenac (> 98.5%), 4 -OH-diclofenac (> 98%), mephenytoin (> 98%), 4 -OH-mephenytoin (> 98%), dextromethorphan (> 98%), dextrorphan (> 99%), midazolam (> 98%), 1 -OH-midazolam (> 98%), testosterone (> 99%), 6 -OHtestosterone (> 98%), furafylline (> 98%), methoxsalen (> 98%), quercetin (> 95%), sulfaphenazole (> 98%), ticlopidine (> 99%), quinidine (> 98%), ketoconazole (> 99%), and terfenadine (> 99%) were purchased from Sigma-Aldrich Co. 4-Hydroxy mephenytoin (> 98%) and 6-hydroxy paclitaxel (> 99%) were purchased from BD Gentest. All other chemicals used were of analytical grades and used as received. Distilled water was prepared using a Milli-Q purification system (Millipore). All standard solutions and mobile phases were passed through a 0.22-µm membrane filter before use. Cytochrome inhibition assay The incubation mixtures consisted of 0.5 mg/ml of human liver microsomes; various concentrations of G. cambogia extract in DMSO (1, 3, 10, 30, 100, 300, and 1000 µg/ml) or various concentrations of ( )-calcium hydroxycitrate tribasic in 10 mm ammonium formate solution (0.1, 0.3, 1, 3, 10, 30, and 100 µm); a substrate mixture (40 µm phenacetin for CYP1A2; 2.5 µm coumarin for CYP2A6; 80 µm bupropion for CYP2B6; 10 µm paclitaxel for CYP2C8; 10 µm diclofenac for CYP2C9; 80 µm [±]-mephenytoin for CYP2C19; 5 µm dextromethorphan for CYP2D6; and 2.5 µm midazolam and 30 µm testosterone for ); and an NADPHgenerating system (NGS; 0.1 M glucose-6-phosphate, 10 mg/ml
5 β-nadp+, and 1 U/mL glucose-6-phosphate dehydrogenase) in a total volume of 200 µl of potassium phosphate buffer (0.1 M, ph 7.4). The reaction mixture without NGS was preincubated at 37 C for 5 min and then further incubated with NGS for 30 min in a water bath. Well-known selective CYP inhibitors were tested as positive controls (ketoconazole for, ticlopidine for CYP2B6, and quercetin for CYP2D6). After incubation, the reaction was stopped by adding 400 µl of internal standard (terfenadine, 0.16 µm) in ice-cold 0.1% acetic acid. The experiments were performed in triplicate. Cytochrome 2B6 inhibition assay As the data showed that G. cambogia extract had an inhibitory effect on CYP2B6, a further inhibition test with CYP2B6 was conducted. All procedures were the same, but CYP2B6 supersomes and a single substrate (bupropion) were used instead of human liver microsomes and the substrate mixture. In addition, a CYP2B6 inhibition assay was performed following 30 min preincubation without the substrate to determine whether G. cambogia extract is a time-dependent inhibitor. The experiments were performed in triplicate. Sample preparation The reaction solutions were passed through the activated Sep-Pak C18 cartridges (96-well type OASIS HLB extraction cartridge; Waters). Then, the cartridges were washed twice with 1 ml 0.1% acetic acid and eluted with 1 ml methanol. The eluate was dried under nitrogen gas. The residue was resolved in 0.1% formic acid/acetonitrile (85 : 15, 100 µl), and a 5-µL aliquot was injected into the HPLC column for LC MS/MS analysis. LC MS/MS analysis An Agilent 1260 binary pump HPLC system, with the Agilent 6460 Triple Quadrupole mass spectrometer (Agilent Technologies), equipped with an electrospray ionization source, was used as an LC MS/MS system. Chromatographic separation was achieved on a Fortis C8 column ( mm, 5.0 µm; Fortis Technologies Ltd.). The HPLC mobile phases consisted of (A) 0.1% formic acid and (B) 0.1% formic acid in 90% acetonitrile. A gradient elution was used with an initial concentration of 15% of solvent B and a flow rate of 0.25 ml/min. The solvent B composition changed as follows: min, 85% (gradually increased); min, 85% (maintained); min 15%; min, 15% (re-equilibrium). The total run time was 8.0 min, and the injection volume was 5 µl. Mass detection was performed in the positive ion mode with MRM. The MRM mode used for the precursor production pairs (Q1/Q3) is shown in Table 3. Statistics Data are presented as the mean ± S. D. (n = 3). The IC 50 value was calculated based on the metabolite formation curves using SigmaPlot The four parameters logistic regression was used for curve fitting. Table 3 Precursor product ion pairs of CYP-specific metabolites for MRM detection. P450 isozyme Supporting information The representative LC MS/MS chromatograms for the CYP isozyme-specific metabolites are available as Supporting Information. Acknowledgements This research was supported by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education, Science and Technology (NRF- 2014R1A1A1A ). Prof. Hye Hyun Yoo is an Invitation Research Fellow of the Japan Society for the Promotion of Science in Conflict of Interest The authors declare no conflict of interest. References Metabolites monitored Precursor ion Product ion CYP 1A2 Acetaminophen CYP 2A6 7-OH-Coumarin CYP 2B6 OH-Bupropion CYP 2C8 6-OH-Paclitaxel CYP 2C9 4-OH-Diclofenac CYP 2C19 4-OH-Mephenytoin CYP 2D6 Dextrorphan CYP 3A4 1-OH-Midazolam CYP 3A4 6-β-OH-Testosterone Internal standard Terfenadine [1] Tharachand SI, Avadhani M. Medicinal properties of Malabar tamarind [Garcinia cambogia (Gaertn.) Desr.]. Int J Pharm Sci Rev Res 2013; 19: [2] Semwal RB, Semwal DK, Vermaak I, Viljoen A. A comprehensive scientific overview of Garcinia cambogia. Fitoterapia2015;102: [3] Hayamizu K, Ishii Y, Kaneko I, Shen M, Okuhara Y, Shigematsu N, Tomi H, Furuse M, Yoshino G, Shimasaki H. Effects of Garcinia cambogia (Hydroxycitric Acid) on visceral fat accumulation: a double-blind, randomized, placebo-controlled trial. Curr Ther Res Clin Exp 2003; 64: [4] Márquez F, Babio N, Bullo M, Salas-Salvado J. Evaluation of the safety and efficacy of hydroxycitric acid or Garcinia cambogia extracts in humans. Crit Rev Food Sci Nutr 2012; 52: [5] Rasha HM, Salha A, Thanai A, Zahar A. The biological importance of Garcinia cambogia: A review. J Nutr Food Sci 2015; S5: 1 5 [6] Saito M, Ueno M, Ogino S, Kubo K, Nagata J, Takeuchi M. High dose of Garcinia cambogia is effective in suppressing fat accumulation in devel-
6 oping male Zucker obese rats, but highly toxic to the testis. Food Chem Toxicol 2005; 43: [7] Kim YJ, Choi MS, Park YB, Kim SR, Lee MK, Jung UJ. Garcinia cambogia attenuates diet-induced adiposity but exacerbates hepatic collagen accumulation and inflammation. World J Gastroenterol 2013; 19: [8] Shim M, Saab S. Severe hepatotoxicity due to hydroxycut: a case report. Dig Dis Sci 2009; 54: [9] Jones FJ, Andrews AH. Acute liver injury associated with the herbal supplement hydroxycut in a soldier deployed to Iraq. Am J Gastroenterol 2007; 102: [10] Stevens T, Qadri A, Zein NN. Two patients with acute liver injury associated with use of the herbal weight-loss supplement hydroxycut. Ann Intern Med 2005; 142: [11] Rehman SU, Choi MS, Choe K, Yoo HH. Interactions between herbs and antidiabetics: an overview of the mechanisms, evidence, importance, and management. Arch Pharm Res 2015; 38: [12] Molarius A, Seidell JC. Selection of anthropometric indicators for classification of abdominal fatness a critical review. Int J Obes 1998; 22: [13] Manda VK, Avula B, Dale OR, Chittiboyina AG, Khan IA, Walker LA, Khan SI. Studies on pharmacokinetic drug interaction potential of vinpocetine. Medicines 2015; 2: [14] Thorn CF, Lamba JK, Lamba V, Klein TE, Altman RB. PharmGKB summary: very important pharmacogene information for CYP2B6. Pharmacogenet Genomics 2010; 20: [15] Turpeinen M, Raunio H, Pelkonen O. The functional role of CYP2B6 in human drug metabolism: substrates and inhibitors in vitro, in vivo and in silico. Curr Drug Metab 2006; 7: [16] Meyer MR, Bach M, Welter J, Bovens M, Turcant A, Maurer HH. Ketaminederived designer drug methoxetamine: metabolism including isoenzyme kinetics and toxicological detectability using GC MS and LC- (HR-)MSn. Anal Bioanal Chem 2013; 405: [17] Tan L, Yu JT, Sun YP, Ou JR, Song JH, Yu Y. The influence of cytochrome oxidase CYP2A6, CYP2B6, and CYP2C9 polymorphisms on the plasma concentrations of valproic acid in epileptic patients. Clin Neurol Neurosurg 2010; 112: [18] Jeon HS, Kim MJ, Choi HY, Kim YH, Kim EH, Kim AR, Park HJ, Bae KS, Lim HS. Pharmacokinetics and pharmacodynamics of ticagrelor and prasugrel in healthy male Korean volunteers. Clin Ther 2015; 37:
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