Зборник Матице српске за природне науке / Matica Srpska J. Nat. Sci. Novi Sad, № 133, 163—171, 2017

UDC 615.322:582.28 https://doi.org/10.2298/ZMSPN1733163K

Aleksandar Z. KNEŽEVIĆ1 * , Ivan N. MILOVANOVIĆ1 , Jelena B. VUKOJEVIĆ1

1 University of Belgrade, Faculty of Biology, Takovska 43, 11000 Belgrade, Republic of

ANTIOXIDATIVE ACTIVITY OF warnieri BASIDIOCARPS

ABSTRACT: Considering that mushrooms synthesize different kinds of compounds with antioxidative activity and that search for natural antioxidants is a topical study area, testing of unstudied is fully justified. The aim of the study was to evaluate antioxidative capacity of Lenzites warnieri basidiocarps using different solvents. Antioxidative potential of 96% ethanolic, 70% ethanolic and methanolic extracts was evaluated by 2,2’-azino-bis (3-ethylbenzothiazoline-6-sulphonic acid) (ABTS) bleaching assay and 2,2-diphenyl-1-picryl- hydrazyl (DPPH) scavenging assay. Additionally, total content of phenols and flavonoids in extracts was determined as galic acid equivalent (GAE) and quercetin equivalent (QE), respectively. Presented as EC50, 70% ethanolic extracts showed the highest antioxidative capacity by DPPH assay (3.08 ± 0.49 mg/mL) and 96% ethanolic extract by ABTS assay (3.08 ± 0.24 mg/mL). Methanolic extract exhibited the lowest antioxidative activity in both assays (6.02 ± 0.99 mg/mL and 4.92 ± 0.38 mg/mL, respectively). Results showed that anti- oxidative capacity of extracts depended on solvents and assay used, indicating that ethanolic extracts were with higher capacity in free radicals neutralization. The highest content of total phenols was detected in 70% ethanolic extract (37.45 ± 0.36 µg GAE/mg of dried extract) while the lowest amount was noted in methanolic extract (22.73 ± 0.05 µg GAE/mg of dried extract). Total flavonoid contents were negligible and ranged between 1.91 ± 0.10 and 2.24 ± 0.13 µg QE/mg of dried extract. The obtained results indicate that Lenzites warnieri possess significant antioxidative capacity which is mainly correlated to phenols present in the extracts. KEYWORDS: Lenzites warnieri, antioxidative activity, basidiocarps, extracts

INTRODUCTION

Mushrooms have been used for thousands of years as food but also in traditional medicine as a reach source of biologically active compounds (Was- ser, 2010; Roupas et al. 2012). However, this great pharmacological potential is still underutilized since, approximately, only 5% of the species are well studied and comprehensive studies are needed for both unstudied and already examined species (Wasser, 2002).

* Corresponding author. E-mail: [email protected] 163 Species of the genus Lenzites has been used in traditional Chinese medi- cine for treatment of several diseases and disorders such as haunch and femoral pain, acropathy, apoplexy and cold (Ren et al. 2006). Medicinal effects have been also demonstrated in conventional medicine and until nowadays, there have been several studies on the various properties of Lenzites spp. basidiocarps and extracts as scavengers of free radicals, antimicrobials, anti-oxidant, anti-viral and immunosuppressant (Liu et al. 2014; Milovanović et al. 2015; Hussin et al. 2016). The contemporary life style brings human and animal populations to face with abundant presence of free radicals, endogenously or in the environment, which further leads to appearance of oxidative stress which is a basis of aging and the initiation of various diseases and disorders (Limón- Pacheco and Gonsebatt, 2009). The capacity of organisms to defend against free radicals can be improved by various synthetic or natural antioxidants. From this aspect, macromycetes can be of a great interest due to the synthesis of different antioxidative compounds such as phenols, tocopherols, carotenoids, ascorbic acid, etc. (Stajić et al. 2013). Lenzites warnieri Mont. & Durieu () is a white rot plant pathogen which can be found on living wood of several deciduous trees such as , cottonwood, and , prefering wet habitats such as riparian woodland or fens and warm temperatures (Ryvarden and Gilbertson, 1993). Species primarily inhabit Central and Southern Europe but also parts of Asia and Northern Africa (Tortić, 1972; Winterhoff, 1986). Formation of resupinate fruiting bodies occurs in autumn while sporulation is expected in following spring (Ryvarden and Gilbertson, 1993). Since described activities might have been responsible for medicinal effects of Lenzites spp. in traditional practice, the goal of the study was to evaluate possible antioxidative potential of basidiocarp extracts of unstudied Lenzites warnieri.

MATERIALS AND METHODS

Organism and extraction

The basidiocarps were collected in Gornje Podunavlje Special Nature Reserve, Serbia, and identified as Lenzites warnieri according to the macroscopic features and the micro morphology of the reproductive structures (Ryvarden and Gilbertson, 1993; Vukojević and Hadžić, 2013). Fruiting bodies (3.0 g) were air-dried, grinded to powder in laboratory blender (Waring Commercial 8010S, USA). Extraction was carried out with 96% ethanol, 70% ethanol and methanol (90.0 mL) on a magnetic stirrer (150 rpm, 30 °C) for 72 hours. The resultant extracts were then centrifuged (20 °C, 3,000 rpm, 10 min), and supernatants filtrated through Whatmann No. 4 filter paper. The filtrates were concentrated under reduced pressure in a rotary evaporator (Büchi R-114, Germany) at 40 °C to dryness and redissolved in 96% ethanol

164 to an initial concentration of 16.0 mg/mL. The extraction yield was determined as the ratio of dry fungal biomass before extraction and dry extract weight after the evaporation process.

Determination of antioxidative activity

Antioxidative activities of basidiocarp extracts were determined spectro- photometrically (CECIL CE2501) by DPPH and ABTS tests.

DPPH assay The free radical scavenging activity of extracts was based on the reduction of a methanol solution of 1,1-diphenyl-2-picrylhydrazyl radicals (DPPH●) (Blois, 1958). The reaction mixtures composed of 1,800.0 µL of 4% methanol solution of DPPH● and 200 µL of extract at defined concentration (series of double dilutions with ethanol from 16.0 mg/mL to 0.125 mg/mL) were mixed and shaken vigorously. After 30 min of incubation in the dark, absorbance was measured at 517 nm against methanol as a blank. The negative control contained all the reaction reagents except the extract. Scavenging effect was calculated using the equation:

DPPH scavenging effect (%) = ((Ac-As)/Ac) × 100 where Ac – absorbance of the negative control; As – absorbance of the reaction mixture (with samples at different concentrations). EC50 values (mg extract/mL) represent the concentration of test samples or L-ascorbic acid (standard antioxidant) providing 50% inhibition of DPPH radicals were calculated by interpolation of DPPH● absorbance curve at 517 nm from linear regression analysis.

ABTS assay This test was based on measuring the level of ABTS+● stock solution color change in presence of antioxidants according to the procedure of Miller et al. (1993). The initial solution of ABTS cation radicals was prepared by dissolution of 9.0 µg ABTS in 2.5 mL dH2O and addition of 44.0 µL 140 mM potassium persulphate (K2S2O8) solution, 12 to 16 hours before use, while the stock solu- tion was prepared immediately prior to measurement by dilution of the initial solution with dH2O and adjustment of solution absorbance on 0.700 ± 0.020 at 734 nm. The reaction mixture (1,500.0 µL of the ABTS stock solution and 15.0 µL of extract of concentration of 1.0 mg/mL) was incubated at room tempera- ture for 4 min and absorbance change was measured at 734 nm. Distilled water was used as a blank. Extract concentration required for ABTS cation radicals reduction, equivalent to reduction of 1.0 mg/mL ascorbic acid (AAEC) was determined using equation of calibration curve for ascorbic acid. EC50 value (mg extract/mL) presents effective extract concentration that scavenges 50% of ABTS cation radicals and it is obtained by linear regression analysis.

165 Determination of phenol and flavonoid contents

The total contents of soluble phenolic compounds in the extracts of fruiting bodies were estimated using Folin-Ciocalteu reagent and gallic acid as stand- ards according to the method described by Singleton and Rossi (1965). The reaction mixture (1,000.0 µL of 10% Folin-Ciocalteu reagent and 200.0 µL of sample in concentration of 1.0 mg/mL) was incubated for 6 min in dark and thereafter 800.0 µL of 7.5% Na2CO3 was added. The mixture was then vortexed and incubated on a rotary shaker (100 rpm) in dark at room temperature for 2 hours. The absorbance was measured spectrophotometrically at 740 nm against a blank (mixture without extract). The total concentration of phenols was pre- sented as µg of gallic acid equivalent (GAE) per mg of dried extract using equation of calibration curve for GAE. Total flavonoid contents in extracts were determined using quercetin as standard according to the method of Park et al. (1997). The reaction mixture (1,000.0 µL of extract in concentration of 1.0 mg/mL, 4,100.0 µL of 80% ethanol, 100.0 µL of 10% Al (NO3)3 × 9H2O and 100.0 µL of 1.0 M water solution of potassium acetate) was incubated in dark on a rotary shaker (100 rpm) and room temperature for 40 min and thereafter absorbance was measured at 415 nm against blank (mixture which contained ethanol instead extract). Total flavonoid content was expressed as µg of quercetin equivalent (QE) per mg of dried extract using equation of calibration curve for QE.

Statistical analysis

All measurements were carried out in triplicate and the results are expressed as mean ± standard error. One-way analysis of variance (ANOVA) and Tukey`s HSD post-hoc test were performed to test any significant differences among means. Statistical significance was declared at P < 0.01. All statistical analyses were done using software STATISTICA, version 6.0 (StatSoft, Inc., Tulsa, USA).

RESULTS AND DISCUSSION

Extraction yields of Lenzites warnieri basidiocarps differed statistically depending on solvent used for the extraction (P < 0.01). The highest extraction yield was noticed when 96% ethanol was used as solvent (4.53 ± 0.05%) while the lowest yield was obtained in methanol (3.57 ± 0.06%) (Table 1).

Table 1. Extractions Yields (%) of Lenzites warnieri basidiocarps

Solvent Extraction Yield (%) 96% Ethanol 4.53 ± 0.05 70% Ethanol 4.23 ± 0.04 Methanol 3.57 ± 0.06

166 Previous studies showed that biomass extractability strongly depends on species, strain and solvent used for the extraction (Knežević et al. 2015). Thus, it can be said that the obtained extraction yields using alcohols as solvents are expected for Lenzites spp. basidiocarps or fungi belonging to family Polypo- raceae, which usually ranges from 2.0% to 10.0% (Liu et al. 2014; Knežević et al. 2015; Ogidi et al. 2015). Compared to results of Oyetayo (2009) who obtained extraction yield of 2.3% for Lenzites sp. basidiocarps using ethanol as solvent, material used in our study exhibited double higher extractability. However, Liu et al. (2013) showed almost the same extractability of L. betu­ lina basidiocarps in 96% ethanol as it was demonstrated for L. warnieri in our study which was approximately 4.5%. Additionally, for fruiting bodies of L. warnieri ethanol in both applied concentrations was better solvent than methanol. The most likely explanation for this is the polarity of major compounds extractable in alcohols, i.e. less polar compounds were present in higher quantities and dissolved in ethanol with higher yields (Anwar and Przybylski, 2012). Antioxidative activity of L. warnieri extracts was determined using two parallel assays for the evaluation of free-radical scavenging activity, i.e., DPPH and ABTS tests (Table 2). Tested extracts showed significant antioxidative potentials which varied depending on solvent used for the extraction but also applied assay. Scavenging activities of extracts, presented by EC50 values, ranged from 3.08 ± 0.49 mg/mL to 6.57 ± 0.27 mg/mL. The highest antioxida- tive capacities were noticed for both 96% ethanolic extract in ABTS assay (3.08 ± 0.24 mg/mL) and 70% ethanolic extract in DPPH assay (3.08 ± 0.49 mg/mL). The lowest activity was detected for 96% ethanolic extract in DPPH assay (6.57 ± 0.27 mg/mL). L-ascorbic acid was far better free-radical scavenger compared to extracts, i.e. EC50 value was 0.035 ± 0.001 mg/mL (Table 2).

Table 2. Antioxidative activities of Lenzites warnieri basidiocarp extracts and commercial antioxidant

Extracts and synthetic antioxidant EC50 (mg/mL) DPPH assay ABTS assay 96% Ethanolic 6.57 ± 0.27 3.08 ± 0.24 70% Ethanolic 3.08 ± 0.49 4.47 ± 0.34 Methanolic 6.02 ± 0.99 4.92 ± 0.38 L-ascorbic acid 0.035 ± 0.001 0.247 ± 0.012

The tested extracts were good antioxidative agents, but compared to L-ascor- bic acid, they showed lower scavenging activity. Results also indicated that neutralization of free radicals depended on two factors and solvent used for the extraction coupled with assay applied for the evaluation of antioxidative activity. Regarding this, our results showed that scavenging effect of 70% ethanolic extract on DPPH radicals significantly differed (P<0.01) from 96% ethanolic and methanolic extract which did not show any statistically significant difference in radicals neutralization. On the other side, there was no difference in ABTS cation radicals’ neutralization between 70% ethanolic and methanolic

167 extracts. Previous studies have also showed the antioxidative potential of Lenzites species (Lee et al. 1996; Oyetayo 2009; Liu et al. 2013; Milovanović et al. 2015). Compared to results of Oyetayo (2009), who demonstrated DPPH radical scav- enging of L. betulina ethanolic extract for approximately 40% at concentration of 1.0 mg/mL, our results for L. warnieri were quite similar (32.4 ± 0.2 % at 1.0 mg/mL of ethanolic extract – data not shown). Some detailed studies showed that separate fractions obtained from L. betulina basidiocarps exhibited much higher antioxidative capacity than crude extract (Liu et al. 2013). This study also showed that, compared to mycelial extracts of L. betulina, fruiting bodies of L. warnieri possess higher capacity in DPPH radical scavenging (Milovanović et al. 2015). Total phenol contents in extracts were significant compared to total fla- vonoid contents which were very low (Table 3). The highest amount of phenols was obtained after extraction with 70% ethanol (37.45 ± 0.36 µg GAE/mg of dried extract) while the lowest amount was detected in methanol extract (22.73 ± 0.05 µg GAE/mg of dried extract). Total amounts of flavonoids were negli- gible and ranged between 1.91 ± 0.10 and 2.24 ± 0.13 µg QE/mg of dried extract (Table 3).

Table 3. Phenol and flavonoid contents in extracts of Lenzites warnieri basidiocarps

Extracts Total phenol content Total flavonoid content (µg GAE/mg of dried extract) (µg QE/mg of dried extract) 96% Ethanolic 35.33 ± 0.53 2.24 ± 0.13 70% Ethanolic 37.45 ± 0.36 2.11 ± 0.06 Methanolic 22.73 ± 0.05 1.91 ± 0.10

The degree of correlation between the DPPH and ABTS free radicals scavenging activity of the extracts and phenol contents was very low with R2 of 0.238 and 0.344, respectively. Accordingly, there was no correlation between DPPH radicals scavenging activity and flavonoids (R2 = 0.0). However, the level of ABTS cation radicals neutralization and flavonoids content was highly correlated (R2 = 0.837). According to the large number of previous studies, phenols and tocophe- rols have the main roles in the antioxidative activity of mushrooms (Stajić et al. 2013). These compounds are abundant and important constituents of basidio- carps and our results showed significant total phenol content compared to flavonoids. The mechanism of antioxidative action of phenols is based on the presence of hydroxyl groups acting as reducing agents, metal chelators, hydro- gen donors and singlet oxygen quenchers (Rice-Evans et al. 1996). Results for L. warnieri phenolic contents were comparable with those of Oyetayo et al. (2013) who detected similar content of phenols in L. betulina ethanolic extract (35.3 and 30.0 µg GAE/mg of extract, respectively). Even though the detection of total phenol content is the first step in characterization of extracts, search for specific compounds in basidiocarps is a promising approach in evaluation of antioxidative potential of macro fungi. Some compounds isolated from

168 L. betulina basidiocarps, such as betulinan A and B, can significantly inhibit lipid peroxidation (Smolibowska et al. 2016). Furthermore, according to Lee et al. (1996) betulinan A isolated from L. betulina basidiocarps was about four times more active as a radical scavenger than vitamin E in inhibition of lipid peroxidation. Despite low correlation between total phenol contents and radi- cals scavenging activity, which implies that some other compounds were re- sponsible for neutralization of DPPH and ABTS free radicals, characterization of phenolic compounds which can be isolated from L. warnieri basidiocarps will be of a great importance. Additionally, even though total flavonoid content in extracts was characterized as negligible, they were significantly responsible for ABTS cation radicals’ neutralization.

CONCLUSION

Results showed for the first time that L. warnieri basidiocarps possess significant antioxidative capacity correlated to phenol content in the extracts. Further studies should focus on isolation, purification and determination or description of specific bioactive compounds with free-radical scavenging activity.

ACKNOWLEDGEMENTS

The authors are grateful to Prof. Dr Gordana Subakov-Simić, from Univer- sity of Belgrade, Faculty of Biology for supplying fungal materials. This study was carried out under Project No. 173032, which is financially supported by the Ministry of Education, Science and Technological Development of Republic of Serbia.

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АНТИОКСИДАТИВНА АКТИВНОСТ ПЛОДОНОСНИХ ТЕЛА Lenzites warnieri Александар З. КНЕЖЕВИЋ1*, Иван Н. МИЛОВАНОВИЋ1, Јелена Б. ВУКОЈЕВИЋ1

1Универзитет у Београду, Биолошки факултет, Таковска 43, Београд 11000, Република Србија

РЕЗИМЕ: С обзиром на чињеницу да гљиве синтетишу различите врсте је- дињења с различитим антиоксидативним потенцијалом и да је потрага за новим природним антиоксидансима тренд у данашњим истраживањима, може се рећи да је потпуно оправдано тестирање нових врста. Циљ истраживања био је да се испита антиоксидативни капацитет екстраката плодоносних тела Lenzites warnieri користе­ ћи различите екстрактанте. Антиоксидативни капацитет 96% етанолног, 70% етанол­ ног и метанолног екстракта је одређиван ABTS (2,2’-азини-бис(3-етилбензотиа­зо­ лин-6-сулфонска киселина)) и DPPH (2,2-дифенил-2-пикрил-хидразил) тестом. Такође је одређена укупна концентрација фенола и флавоноида у екстрактима као еквивалената галне киселине (GAE) односно кверцетина (QE). На основу EC50 вред- ности, 70% етанолни екстракт је показао највиши антиоксидативни капацитет DPPH тестом (3.08 ± 0.49 mg/mL) а 96% етанолни екстракт ABTS тестом (3.08 ± 0.24 mg/mL). Метанолни екстракт имао је најслабију антиоксидативну активност коришћењем оба теста (6.02 ± 0.99 mg/mL односно 4.92 ± 0.38 mg/mL). Резултати су показали да антиоксидативни капацитет екстракта зависи од екстрактанта и примењеног теста, па су тако етанолни екстракти имали већи капацитет у неутрализацији слободних ра­дикала. Највећа концентрација укупних фенола је детектована у 70% етанолном екс­тракту (37.45 ± 0.36 µg GAE/mg сувог екстракта) док је најнижа забележена у ме­танолном екстракту (22.73 ± 0.05 µg GAE/mg сувог екстракта). Укупна количина флавоноида је била занемарљиво мала и кретала се у опсегу од 1.91 ± 0.10 до 2.24 ± 0.13 µg QE/mg сувог екстракта. Добијени резултати показују да Lenzites warnieri има значајан антиоксидативни капацитет који је највећим делом у корелацији са садржајем фенола у екстракту. КЉУЧНЕ РЕЧИ: Lenzites warnieri, антиоксидативна активност, плодоносна тела, екстракти

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