ANTIOXIDANT ACTIVITY AND BIOACTIVE CONSTITUENTS OF THE AERIAL PARTS OF HARPAGOPHYTUM PROCUMBENS PLANTS
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1 ANTIOXIDANT ACTIVITY AND BIOACTIVE CONSTITUENTS OF THE AERIAL PARTS OF HARPAGOPHYTUM PROCUMBENS PLANTS M.I. Georgiev 1, K.I. Alipieva 2 and P. Denev 3 1 Institute of Microbiology, Bulgarian Academy of Sciences, Department of Microbial Biosynthesis and Biotechnologies, Laboratory in Plovdiv, Plovdiv, Bulgaria 2 Institute of Organic Chemistry with Centre of Phytochemistry, Bulgarian Academy of Sciences, Sofia, Bulgaria 3 Institute of Organic Chemistry with Centre of Phytochemistry, Bulgarian Academy of Sciences, Laboratory of Bioactive Substances, Plovdiv, Bulgaria Correspondence to: Milen Georgiev Milen.Georgiev@mailbox.tu-dresden.de, milengeorgiev@gbg.bg ABSTRACT Harpagophytum procumbens is an herbaceous plant with high medicinal value that grows in the Kalahari Desert region of Africa. Devil s claw plant tubers have been used since time immemorial by the native population of Southern Africa for treating a huge number of human ailments, including fever, diabetes, diarrhea and blood diseases. More recently, extracts of the secondary roots of the species have been found to be effective in the treatment of degenerative rheumatoid arthritis, osteoarthritis, tendonitis, kidney inflammation and heart disease. Therefore, Harpagophytum procumbens has been increasingly considered an alternative to non-steroidal anti-inflammatory drugs. The antioxidant activities of pure metabolites, as well as of total methanol extracts of the Devil s claw plants were evaluated in 2,2 -diphenyl-1-picrylhydrazyl (DPPH ), oxygen radical absorbance capacity (ORAC FL ) and hydroxyl radical averting capacity (HORAC FL ) assays. The crude methanolic extract may be attractive for various commercial purposes since it displayed antioxidant activity and it can be conveniently and economically prepared. Keywords: antioxidant, devil s claw, harpagide, harpagoside DPPH, HORAC FL, ORAC FL Introduction 438 Reactive oxygen species (ROS) are unavoidable by-products of aerobic metabolism and (hence) are continuously formed in eukaryotic cells (14). Depending on their concentration, ROS can be beneficial or harmful to cells and tissues. At physiological low levels, ROS function as redox messengers in intracellular signaling and regulation (1), whereas their increased generation may cause substantial oxidative stress and oxidative damage to DNA, proteins and lipids (5). This could further results in the development of many pathological conditions in the human body, such as cancer, ischemic vascular disease and arteriosclerosis (7). The levels of ROS are generally maintained under certain levels in the cells by a battery of molecules (of enzymatic or nonenzymatic nature) with antioxidant properties. Hence, nonenzymatic low molecular mass antioxidants provide very important protection for cells, and antioxidants with suitable properties for various purposes are being intensively sought and will continue in future (3). The interest in finding prominent naturally-occurring antioxidants rises in the recent years to replace synthetic ones (such as butylated hydroxyanisole and butylated hydroxytoluene), since the latter possess some toxic and mutagenic effects (10). Harpagophytum procumbens DC (Pedaliaceae family), commonly known as Devil s claw, is a perennial herbaceous plant, native to Kalahari Desert regions of Southern Africa (namely Namibia, RSA, Botswana and Zimbabwe). The indigenous peoples of Southern Africa have used Devil s claw in their tribal medicine for treatment a number of medical conditions (for over 30 diseases) and even as both a laxative and abortifacient (18). The exact composition of the
2 Harpagophytum s medicinally active agents and the effects of each of them have not been fully uncovered yet. However it is clear that the main active agents are harpagoside and concomitant harpagide (both belong to iridoid glycosides group; Fig. 1). These active agents are mainly found in the secondary roots (store tubers), which are exclusively used as raw material for producing Devil s claw-based products (9). Fig. 1. Chemical structures of iridoids glycosides harpagoside and harpagide. During the 1960s H. procumbens has been introduced to Europe and traded under the pharmaceutical name of Harpagophyti radix. Devil s claw products are generally registered as an herbal medicine in France and Germany or as a food supplement in the United Kingdom, the Netherlands, and the Far East (18). In the USA Harpagophytum extracts undergoing phase II clinical trials for treatment of hip and knee osteoarthritis (19). Today, Harpagophytum tubers are used mainly in West European countries the treatment of degenerative rheumatoid arthritis, osteoarthritis, tendonitis, kidney inflammation and heart diseases (6, 13). In addition, in recent years Devil s claw has been increasingly considered as an alternative to nonsteroidal anti-inflammatory drugs (NSAIDs), such as aspirin, ibuprofen as well as prescription NSAID drugs rofecoxib and celecoxib (18). The annual market of dried Devil s claw tubers is estimated to ~ tonnes, as Namibia is the main exporting country (12, 18). Kathe et al. (9) reported that 57 pharmaceutical products from the Devil s claw species have cumulative sale volumes in Germany alone worth approximately 30 million euros, representing nearly 75% of the prescriptions for rheumatism (18). It is expected that the global demands for Devil s claw therapeutic molecules will increase during the next years. A large number of methods have been developed and utilized to evaluate the total antioxidant capacity of target plants (17). In the investigation presented here, we evaluated 439 the antioxidant potential of the aerial parts of Devil s claw plants and their main constituents by a number of methods, as DPPH, ORAC FL and HORAC FL assays. Results from these assays are expected to provide additional information for eventual further utilization of Devil s claw above ground parts as antioxidants. Materials and Methods Plant material and sample preparation Devil s claw plants, grown in vitro, were kindly supplied by Dr. G. Kerns (Saxon Institute for Applied Biotechnology, Leipzig, Germany). The freeze-dried leaves (500 mg) were extracted with methanol (solid:liquid ratio 1:30) in an ultrasonic bath (3 x 15 min). The obtained extracts were then pooled, filtered (through 0.2-µm filters) and evaporated to dryness (89.6 mg). Rosmarinic acid used as a positive standard was purchased from Sigma-Aldrich (Milwaukee, WI, USA). High performance liquid chromatography detection (HPLC) The HPLC system consisted of a 1525 binary HPLC system controlled by Breeze software version 3.30 SPA, a 2487 dual λ absorbance detector (all from Waters Corp., Milford, MA, USA) and a Discovery HS reverse phase (C 18 ), 250 mm x 4.6 mm i.d., 5 µm particle size column (Supelco). The metabolites were separated using a mobile phase consisting of 10:90 (A:B) at a flow rate of 1.0 ml/min for 5 min, followed by a linear gradient to 50:50 (A:B) at a flow rate of 1.1 ml/min over 10 min, where A is methanol and B is water. After each separation the column was washed by 100% methanol at a flow rate of 0.8 ml/min, then equilibrated to the starting composition (10:90, A:B) at a flow rate of 1.0 ml/min for 5 min. The column temperature was 25 C and the detection wavelength was 278 nm for all analysis. Pure harpagoside (Extrasynthese, Genay, France) was used for the preparation of the calibration curve (0 200 µg/l). 2,2 -diphenyl-1-picrylhydrazyl (DPPH) radical scavenging assay The ability of the samples tested to scavenge DPPH radicals was determined following the procedure described by Kovatcheva-Apostolova et al. (11) with slight modifications. Briefly, 2 ml of DPPH solution (0.1 mm) was mixed with 0.5 ml of a solution containing different concentrations of the dry extract and pure compounds to be tested. The reduction of DPPH radicals (in percent) was determined after 5 min by
3 reading the absorbance at 516 nm (Shimadzu 1240 UV/vis as follows: 15.7 mg of CoF 2.4H 2 O and 20 mg of picolinic spectrophotometer) using the following formula: acid were dissolved in 20 ml of distilled water. 170 μl FL (60 nm, final concentration) and 10 µl of the sample were incubated at 37 C for 20 min directly in the [1] FLUOstar Inhibition of DPPH (%) = [A 0 (A 1 A 2 )/A 0 ] x 100, plate where A 0, A 1 and A 2 are the absorbance of DPPH, tested sample with DPPH added and the self absorption of the tested sample, respectively. IC 50 values, indicating the final concentrations of samples required for 50 % reduction of the absorbance of DPPH radicals, were also calculated. Oxygen radical absorbance capacity (ORAC) assay ORAC assay measures the antioxidant scavenging activity of samples or test substances (15); more precisely their ability to scavenge peroxyl radicals generated by 2,2 -azobis (2- amidino-propane) dihydrochloride (AAPH) at 37 C. The loss of fluorescence of fluorescein (FL) is used as an indicator of the abundance of the radicals and the protective effect of an antioxidant is measured by comparing the area under the fluorescence decay curve (AUC) obtained from assays with it to the areas obtained from assays with control mixtures in which no antioxidant is present. For this purpose, samples and solutions of AAPH, fluorescein and Trolox were prepared in a phosphate buffer (75 mm, ph 7.4), then 170 μl of the FL solution (final concentration 5.36 x 10-8 M) and 10 μl of the sample to be assayed were mixed and incubated at 37 C for 10 min. Finally, 20 μl of the AAPH solution (final concentration mm) was added, the mixture was incubated for 30 s before the initial fluorescence was measured. After that, fluorescence readings were taken at the end of every cycle, after shaking. For the blanks, 10 μl of phosphate buffer was used instead of test samples. Antioxidant activity was expressed in Trolox equivalents, estimated from a standard curve obtained using μm Trolox solutions. One ORAC FL unit was assigned to the net protection area provided by a 1 μm solution of Trolox. The final ORAC FL values were calculated using a regression equation describing the relationship between the Trolox concentration and the net area under the curve. The results are expressed as µm Trolox equivalents (TE). Hydroxyl radical averting capacity (HORAC) assay HORAC measures the metal-chelating activity of antioxidants under the conditions of Fenton-like reactions, employing a Co (II) complex and hence the protecting ability against formation of hydroxyl radical (16) M H 2 O 2 were prepared in distilled water, while 4.6 mm Co (II) were prepared 440 reader. After incubation, 10 μl H 2 O 2 (27.5 mm, final concentration) and 10 μl of Co (II) (230 µm, final concentration) solutions were added. The initial fluorescence was measured, after which the readings were taken every minute after shaking. For the blank sample, a phosphate buffer solution was used. 100, 200, 400, 500 and 600 μm gallic acid solutions (in phosphate buffer 75 mm, ph 7.4) were used for building the standard curve. The final HORAC values were calculated using a regression equation between gallic acid concentration and the net area under the curve. One HORAC unit was assigned to the net protection area provided by 1 µm gallic acid and the activity of the sample is expressed as μm gallic acid equivalents (GAE) per gram of dry extract. Both ORAC and HORAC analyses were carried out using a FLUOstar OPTIMA plate reader (BMG LABTECH, Offenburg, Germany); excitation wavelength of 485 nm and emission wavelength of 520 nm were used. The results presented in this paper have been summarized from three independent experiments. All determinations were performed in at least three replicates. Results and Discussion Chemical profile of the Harpagophytum procumbens aerial parts To evaluate the antioxidant activity of Harpagophytum constituents we extracted the bio-active metabolites with methanol (at room temperature), which yielded a crude extract with ~18% of the dry weight of the sample. HPLC was further used for quantification of the main constituent of Devil s claw aerial parts. The method used allowed good separation and quantification of the major constituent within 25 min (Fig. 2). Harpagoside, harpagide and some phenylethanoids were accumulated in the Devil s claw plants. Using a commercially available harpagoside we prepared a calibration curve (r ) and the content of harpagoside in the aerial parts was calculated as 7.40 ± 0.30 mg/g on dry weight basis. These amounts (0.74 %) are consistent with previous report of Levieille and Wilson (12), who reported for ~1% total iridoids accumulation in the Devil s claw leaves. However, it has yet to be shown that leaf extracts have the same pharmacological efficacy as tuber
4 extracts (12). 80 Fig. 2. Representative HPLC chromatogram of Harpagophytum procumbens aerial parts. Inhibition of DPPH (%) Evaluation of antioxidant activities The antioxidant properties of extracts and active constituents of Devil s claw plants were evaluated in vitro by DPPH, ORAC FL and HORAC FL assays, using rosmarinic acid as a reference antioxidant. Briefly, the mechanism of scavenging DPPH by radical scavengers can be described as: DPPH (purple) + (A) DPPH-H (yellow) + (A ), where AH is an antioxidant; A is a non-radical product (8). The DPPH is a stable radical, which could be easily used for detection of antioxidant properties of different compounds. The advantages of this method are expressed mainly in its rapidity and selectivity. By this reasons DPPH was widespread used in the recent years for assessment of different antioxidants (3, 8, 11). The DPPH radical scavenging activity (presented as percentages of inhibition) of the Harpagophytum procumbens crude methanolic extract, and pure harpagoside and harpagide is show in Fig. 3. A dose dependent inhibition of DPPH was observed for all tested samples. The highest DPPH radical scavenging activities were displayed by crude methanolic extract (70.6 % inhibition at highest concentration; IC 50 = µg/ml), while harpagide and harpagoside showed weak activity. Both harpagoside and harpagide were ineffective at concentration lower than 50 µg/ml. Similar results for harpagoside were observed before (4). At the maximal concentration (200 µg/ml) harpagide exhibited slightly higher activity than harpagoside (~2.6-fold). This could be attributed to the higher number of hydroxyl group in harpagide molecule, as only antioxidants that are sufficiently potent hydrogen donors are capable of reacting with DPPH radicals (stoichiometrically). Concentration ( g/ml) Fig. 3. Dose dependent effects of Harpagophytum procumbens methanolic extract (green color), and pure harpagoside (red) and harpagide (blue) on DPPH inhibition. IC 50 values are designated with dash line. Error bars represent standard deviations (n = 3). With respect to the ORAC FL assay crude methanolic extract expressed significant antioxidant activity, being times higher compared to pure harpagoside and harpagide (Table 1). The ORAC FL assay measures hydrophilic antioxidant activity against peroxyl radicals. Although ORAC FL cannot be considered as total antioxidant activity assay, it directly estimates the chain-breaking antioxidant activity (15). Direct comparison with previously published data showed that the observed ORAC FL values of Devil s claw crude methanolic extracts are higher than those reported for extracts of bilberry, elderberry (15) and Amazonian palm berry (17), which clearly highlights their high antioxidant potential. It should be also mentioned that rosmarinic acid, used as positive standard, exhibited highest ORAC FL value (21.1 µm TE/µM rosmarinic acid) reported so far. TABLE 1 Scavenging of stable radicals by extracts and pure compounds of Harpagophytum procumbens aerial parts a Crude methanolic extract ORAC FL /g HORAC FL /g ± ± 9.22 Harpagoside ± ± 1.19 Harpagide ± ± 6.3 Rosmarinic acid 21.1 ± 0.82 b 3.25 ± 0.21 c a Means ± SD (n = 3) b µm Trolox equivalents/µm rosmarinic acid c µm Gallic acid equivalents/µm rosmarinic acid 441
5 Hydroxyl (HO) radical (R) averting (A) capacity (C) assay has been introduced several years ago by Ou et al. (16). In opposite of DPPH and ORAC FL assays, it measures the hydroxyl radical prevention activity through determination of the metal-chelating capacity of tested samples. The highest HORAC FL value exhibited Devil s claw crude methanolic extract, followed by harpagide and harpagoside (Table 1). In opposite of previous assay (ORAC FL ), harpagide expressed higher activity than harpagoside (~2-times higher), probably suggesting that the cinnamic acid moiety of the harpagoside molecule does not play crucial role in HORAC FL assay. Although ORAC FL and HORAC FL measure two different aspects of antioxidant properties (radical chain breaking and radical prevention, respectively) we observed strong correlation between both assays (r 2 ~0.94) used to evaluate the antioxidant activities of Devil s claw methanolic extract, isolated compounds and pure rosmarinic acid (Fig. 4). Similar correlation coefficient, between both assays mentioned above, has been calculated by Čiž et al. (2), who studied the antioxidant activity of 22 selected vegetables. Therefore several methods have to be studied in parallel to evaluate the full potential of candidate antioxidant on the target radicals (2). HORAC ( M GAE/g) Y = X r2 = ORAC ( M TE/g) Fig. 4. Correlation among oxygen radical absorbance capacity (ORAC FL ) and hydroxyl radical averting capacity (HORAC FL ) assays for measurement of antioxidant activity of Harpagophytum procumbens extracts and pure substances. Conclusions To conclude, Devil s claw aerial parts contain iridoid glycosides (mainly harpagoside) and several other compounds with significant antioxidant activity. Therefore, it can be highlighted that in addition to providing of therapeutically active compounds, Devil s claw plants (especially their aerial parts) could serve as attractive and sustainable source of powerful antioxidants for the food, cosmetics and pharmaceutical industries. Acknowledgement This research has been supported by a grant (contract number DO /2008) from the National Science Fund of Bulgaria. The authors express their thanks to Dr. G. Kerns (SIAB, Leipzig, Germany) for kindly supplying the Harpagophytum procumbens plants. We thank also the student Vediha Homova for her excellent technical assistance. REFERENCES 1. Circu M.L., Aw T.Y. (2010) Free Radic. Biol. Med. 48, Čiž M., Čižova H., Denev P., Kratchanova M., Slavov A., Lojek A. (2010) Food Control 21, Georgiev M., Alipieva K., Pashova S., Denev P., Angelova M., Kerns G., Bley Th. (2010) Food Chem. 121, Grant L., McBean D.E., Fyfe L., Warnock A.M. (2009) Phytother. Res. 23, Halliwell B., Whiteman M. (2004) Br. J. Pharmacol. 142, Heinrich M., Barnes J., Gibbons S., Williamson E. (2004) Fundamentals of Pharmacognosy and Phytotherapy. Churchill Livingston Press, Edinburgh. 7. Herrera E., Jimenez R., Aruoma O.I., Hercberg S., Sanchez-Garcia I., Fraga C. (2009) Nutr. Rev. 67, S140-S Hu M., Skibsted L.H. (2002) Food Chem. 76, Kathe W., Barsch F., Honnef S. (2003) Prepared for the FAO of the UN, Non-Wood Forest Products Programme, pp Kovacheva E., Georgiev M., Pashova S. Angelova M., Ilieva M. (2006) Z. Naturforsch. 61c, Kovatcheva-Apostolova E.G., Georgiev M.I., Ilieva M.P., Skibsted L.H., Rodtjer A., Andersen M.P. (2008) Eur. Food Res. Technol. 227, Levieille G., Wilson G. (2002) Plant Cell Rep. 21, Ludwig-Müller J., Georgiev M., Bley Th. (2008) 442
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