Abstract
In this study, Daedalea quercina (L.) Pers., Hydnum repandum L., Inonotus radiatus (Sowerby) P. Karst., Omphalotus olearius (DC.) Singer, and Schizophyllum commune Fr. hexane and methanol extracts were subjected to the spectrophotometric assays for antioxidant and enzyme inhibitory activities, which are linked with human diseases that are very prevalent in recent years. Additionally, phenolic compounds of the mushrooms were quantified by HPLC–DAD. The best antioxidant activity was found in H. repandum methanol extract (IC50: 12.04 ± 0.24 µg/mL) in the β-carotene-linoleic assay; I. radiatus methanol extract in DPPH• (81.22 ± 0.50%), ABTS•+ (IC50: 73.47 ± 0.18 µg/mL), and CUPRAC (A0.50: 88.21 ± 0.02 µg/mL) assays; S. commune hexane extract (53.36 ± 0.89%) in the metal chelating assay. O. olearius hexane extract was found as the best inhibitor against AChE (71.58 ± 0.28%) and BChE (67.30 ± 0.15%). When I. radiatus methanol (95.88 ± 0.74%) and H. repandum hexane (95.75 ± 0.16%) extracts showed close α-amylase inhibitory activity to acarbose (96.68 ± 0.08%), D. quercina methanol extract (70.79 ± 0.34%) had higher α-glucosidase inhibitory activity than acarbose (67.01 ± 2.28%). Among 16 phenolic compounds analyzed, gallic acid (0.02 ± 0.01–0.23 ± 0.01 µg/g) was detected in all studied mushrooms. This study provides that investigated mushrooms can be used for further research, which can lead to the development of new natural remedies to alleviate complications related to oxidative stress, diabetes, and neurological diseases.
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The data that support the findings of this study are available from the corresponding author, upon reasonable request.
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Abbreviations
- ABTS:
-
2,2′-Azino bis (3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt
- AChE:
-
Acetylcholinesterase
- AD:
-
Alzheimer’s disease
- BChE:
-
Butyrylcholinesterase
- BHA:
-
Butylated hydroxyl anisole
- CUPRAC:
-
Cupric reducing antioxidant capacity
- DM:
-
Diabetes mellitus
- DPPH:
-
1,1-Diphenyl-2-picrylhydrazyl
- EDTA:
-
Ethylenediaminetetraacetic acid
- HPLC–DAD:
-
High-performance liquid chromatography–diode array detection
- IC50 :
-
Half-maximal inhibitory concentration
- PDA:
-
Photodiode array detector
References
Ahmad W, Ijaz B, Shabbiri K, Ahmed F, Rehman S (2017) Oxidative toxicity in diabetes and Alzheimer’s disease: mechanisms behind ROS/RNS generation. J Biomed Sci 24:76. https://doi.org/10.1186/s12929-017-0379-z
Akata I, Zengin G, Picot CMN, Mahomoodally MF (2019) Enzyme inhibitory and antioxidant properties of six mushroom species from the Agaricaceae family. S Afr J Bot 120:95–99. https://doi.org/10.1016/j.sajb.2018.01.008
Bal C, Akgul H, Sevindik M, Akata I, Yumrutas O (2017) Determination of the anti-oxidative activities of six mushrooms. Fresenius Environ Bull 26:6246–6252
Barchan A, Bakkali M, Arakrak A, Pagan R, Laglaoui A (2014) The effects of solvents polarity on the phenolic contents and antioxidant activity of three Mentha species extracts. Int J Curr Microbiol Appl Sci 3:399–412
Çayan F, Tel-Çayan G, Deveci E, Öztürk M, Duru ME (2019) Chemical profile, in vitro enzyme inhibitory, and antioxidant properties of Stereum species (Agaricomycetes) from Turkey. Int J Med Mushrooms 21(11):1075–1087. https://doi.org/10.1615/IntJMedMushrooms.2019032893
Çayan F, Deveci E, Tel-Çayan G, Duru ME (2020) Identification and quantification of phenolic acid compounds of twenty-six mushrooms by HPLC–DAD. J Food Meas Charact 14:1690–1698. https://doi.org/10.1007/s11694-020-00417-0
Deveci E, Tel-Çayan G, Usluer Ö, Duru ME (2019) Chemical composition, antioxidant, anticholinesterase and anti-tyrosinase activities of essential oils of two Sideritis species from Turkey. Iranian J Pharm Res 18(2):903–913. https://doi.org/10.22037/IJPR.2019.1100657
Deveci E, Tel-Cayan G, Duru ME (2020) In vitro antidiabetic activity of seven medicinal plants naturally growing in Turkey. Eur J Biol 79:23–28. https://doi.org/10.26650/EurJBiol.2020.0011
Deveci E, Çayan F, Tel-Çayan G, Duru ME (2021) Inhibitory activities of medicinal mushrooms on α-amylase and α-glucosidase-enzymes related to type 2 diabetes. S Afr J Bot 137:19–23. https://doi.org/10.1016/j.sajb.2020.09.039
Dundar A, Okumus V, Ozdemir S, Celik KS, Boga M, Ozcagli E, Ozhan G, Yildiz A (2015) Antioxidant, antimicrobial, cytotoxic and anticholinesterase activities of seven mushroom species with their phenolic acid composition. J Horticulture 2(4):1000161. https://doi.org/10.4172/2376-0354.1000161
Dundar A, Okumus V, Ozdemir S, Celik KS, Boğa M, Ozcagli E (2016) Determination of cytotoxic, anticholinesterase, antioxidant and antimicrobial activities of some wild mushroom species. Cogent Food Agric 2:1178060. https://doi.org/10.1080/23311932.2016.1178060
Ellman GL, Courtney KD, Andres V, Featherston RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Emsen B, Kocabas A, Kaya A, Cinar S, Aasim M, Sadi G (2017) In vitro cytotoxicity, antibacterial and antioxidant properties of various extracts from Schizophyllum commune. FR Fresenius Environ Bull 26:1144–1153
Ferreira-Vieira TH, Guimaraes IM, Silva FR, Ribeiro FM (2016) Alzheimer’s disease: targeting the cholinergic system. Curr Neuropharmacol 14:101–115. https://doi.org/10.2174/1570159X13666150716165726
Garrab M, Edziri H, ElMokni R, Mastouri M, Mabrouk H, Douki W (2019) Phenolic composition, antioxidant and anticholinesterase properties of the three mushrooms Agaricus silvaticus Schaeff., Hydnum rufescens Pers. and Meripilus giganteus (Pers.) Karst. in Tunisia. S Afr J Bot 124:359–363. https://doi.org/10.1016/j.sajb.2019.05.033
Gülçin I, Scozzafava A, Supuran CT, Koksal Z, Turkan F, Çetinkaya S, Bingöl Z, Huyut Z, Alwasel SH (2016) Rosmarinic acid inhibits some metabolic enzymes including glutathione S-transferase, lactoperoxidase, acetylcholinesterase, butyrylcholinesterase and carbonic anhydrase isoenzymes. J Enzyme Inhib Med Chem 31(6):1698–1702. https://doi.org/10.3109/14756366.2015.1135914
Hou WC, Lin RD, Cheng KT, Hung YT, Cho CH, Chen CH, Hwang SY, Lee MH (2003) Free radical scavenging activity of Taiwanese native plants. Phytomedicine 10:170–175. https://doi.org/10.1078/094471103321659898
Hu H, Zhang Z, Lei Z, Yang Y, Sugiura N (2009) Comparative study of antioxidant activity and antiproliferative effect of hot water and ethanol extracts from the mushroom Inonotus obliquus. J Biosci Bioeng 107(1):42–48. https://doi.org/10.1016/j.jbiosc.2008.09.004
Kakon AJ, Choudhury MBK, Saha S (2012) Mushroom is an ideal food supplement. J Dhaka Nat Med Coll Hos 18(01):58–62. https://doi.org/10.3329/jdnmch.v18i1.12243
Kalyoncu F, Oskay M, Kayalar H (2010) Antioxidant activity of the mycelium of 21 wild mushroom species. Mycology 1(3):195–199. https://doi.org/10.1080/21501203.2010.511292
Kazeem MI, Adamson JO, Ogunwande IA (2013) Modes of Inhibition of α-amylase and α-glucosidase by aqueous extract of Morinda lucida Benth leaf. Biomed Res Int 2013:527570. https://doi.org/10.1155/2013/527570
Kumar A, Dandapat S, Kumar M, Sinha MP (2018) Anti-inflammatory and amylase inhibitory properties of Indian edible macrofungi Dacryopinax spathularia (schwein) and Schizophyllum commune (fries). Bioscan 13(2):715–718
Maraschin JF, Murussi N, Witter V, Silveiro SP (2010) Diabetes mellitus classification. Arq Bras Cardiol 95:40–46. https://doi.org/10.1590/S0066-782X2010001200025
Morales D, Piris AJ, Ruiz-Rodriguez A, Prodanov M, Soler-Rivas C (2018) Extraction of bioactive compounds against cardiovascular diseases from Lentinula edodes using a sequential extraction method. Biotechnol Prog 34(3):746–755. https://doi.org/10.1002/btpr.2616
Morales D, Rutckeviski R, Villalva M, Abreu H, Soler-Rivas C, Santoyo S, Iacomini M, Smiderle FR (2020) Isolation and comparison of α- and β-d-glucans from shiitake mushrooms (Lentinula edodes) with different biological activities. Carbohyd Polym 229:115521. https://doi.org/10.1016/j.carbpol.2019.115521
Nawaz H, Shad MAS, Rehman N, Andaleeb H, Ullah N (2020) Effect of solvent polarity on extraction yield and antioxidant properties of phytochemicals from bean (Phaseolus vulgaris) seeds. Braz J Pharm Sci 56:e17129. https://doi.org/10.1590/s2175-97902019000417129
Papoutsis K, Zhang J, Bowyer MC, Brunton N, Gibney ER, Lyng J (2021) Fruit, vegetables, and mushrooms for the preparation of extracts with α-amylase and α-glucosidase inhibition properties: a review. Food Chem 338:128119. https://doi.org/10.1016/j.foodchem.2020.128119
Piazzi L, Cavalli A, Colizzi F, Belluti F, Bartolini M, Mancini F, Recanatini M, Andrisano V, Rampa A (2008) Multi-target directed coumarin derivatives: AChE and BChE1 inhibitors as potential anti-Alzheimer compounds. Bioorg Med Chem Lett 8:423–426. https://doi.org/10.1016/j.bmcl.2007.09.100
Podkowa A, Kryczyk-Poprawa A, Opoka W, Muszyńska B (2021) Culinary–medicinal mushrooms: a review of organic compounds and bioelements with antioxidant activity. Eur Food Res Technol 247:513–533. https://doi.org/10.1007/s00217-020-03646-1
Puttaraju NG, Venkateshaiah SU, Dharmesh SM, Urs SMN, Somasundaram R (2006) Antioxidant activity of indigenous edible mushrooms. J Agric Food Chem 54:9764–9772. https://doi.org/10.1021/jf0615707
Sanchez C (2017) Reactive oxygen species and antioxidant properties from mushrooms. Synth Syst Biotechnol 2:13e22. https://doi.org/10.1016/j.synbio.2016.12.001
Stojanova M, Pantić M, Karadelev M, Čuleva B, Nikšić M (2021) Antioxidant potential of extracts of three mushroom species collected from the Republic of North Macedonia. J Food Process Preserv 45:e15155. https://doi.org/10.1111/jfpp.15155
Stojkovic D, Smiljkovic M, Ciric A, Glamoclija J, Griensven VL, Ferreira ICFR, Sokovic M (2019) An insight into antidiabetic properties of six medicinal and edible mushrooms: inhibition of α-amylase and α-glucosidase linked to type-2 diabetes. S Afr J Bot 120:100–103. https://doi.org/10.1016/j.sajb.2018.01.007
Su CH, Lai MN, Ng LT (2013) Inhibitory effects of medicinal mushrooms on α-amylase and α-glucosidase–enzymes related to hyperglycemia. Food Funct 4:644. https://doi.org/10.1039/c3fo30376d
Tel G, Ozturk M, Duru ME, Turkoglu A (2015) Antioxidant and anticholinesterase activities of five wild mushroom species with total bioactive contents. Pharm Biol 53(6):824–830. https://doi.org/10.3109/13880209.2014.943245
Thompson PA, Wright DE, Counsell CE, Zajicek J (2012) Statistical analysis, trial design and duration in Alzheimer’s disease clinical trials: a review. Int Psychogeriatr 24:689–697. https://doi.org/10.1017/S1041610211001116
Tundis R, Loizzo MR, Menichini F (2010) Natural products as α-amylase and α-glucosidase inhibitors and their hypoglycaemic potential in the treatment of diabetes: an update. Mini-Rev Med Chem 10:315–331. https://doi.org/10.2174/138955710791331007
Uttara B, Singh AV, Zamboni P, Mahajan RT (2009) Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 7:65–74. https://doi.org/10.2174/157015909787602823
Vallverdu-Queralt A, Regueiro J, Martínez-Huélamo M, Alvarenga JFR, Leal LN, Lamuela-Raventos RM (2014) A comprehensive study on the phenolic profile of widely used culinary herbs and spices: rosemary, thyme, oregano, cinnamon, cumin and bay. Food Chem 154:299–307. https://doi.org/10.1016/j.foodchem.2013.12.106
Vaz JA, Barros L, Martins A, Sá Morais J, Vasconcelos MH, Ferreira ICFR (2011) Phenolic profile of seventeen Portuguese wild mushrooms. LWT Food Sci Technol 44:343–346. https://doi.org/10.1016/j.lwt.2010.06.029
Vetter J (2019) Biological values of cultivated mushrooms-a review. Acta Aliment 48(2):229–240. https://doi.org/10.1556/066.2019.48.2.11
WHO (1999) Definition, diagnosis and classification of diabetes mellitus and its complications. Report of a WHO Consultation: Part 1 diagnosis and classification of diabetes mellitus. https://apps.who.int/iris/bitstream/handle/10665/66040/WHO_NCD_NCS_99.2.pdf?sequence=1&isAllowed=y
Wong JH, Ng TB, Chan HHL, Liu Q, Man GCW, Zhang CZ, Guan S, Ng CCW, Fang EW, Wang H, Liu F, Ye X, Rolka K, Naude R, Zhao S, Sha O, Li C, Xia L (2020) Mushroom extracts and compounds with suppressive action on breast cancer: evidence from studies using cultured cancer cells, tumor-bearing animals, and clinical trials. Appl Microbiol Biotechnol 104:4675–4703. https://doi.org/10.1007/s00253-020-10476-4
Xu DP, Li Y, Meng X, Zhou T, Zhou Y, Zheng J, Zhang JJ, Li HB (2017) Natural antioxidants in foods and medicinal plants: extraction, assessment and resources. Int J Mol Sci 18(1):96. https://doi.org/10.3390/ijms18010096
Acknowledgements
Authors would like to thank Cansu Korkmaz (Department of Biology, Muğla Sıtkı Koçman University) for the collection of the mushroom samples.
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FÇ: data curation, methodology, formal analysis, and software. GT-Ç: conceptualization, software, formal analysis, methodology, data curation, supervision, and writing—review and editing. ED: methodology, software, investigation, and writing—original draft preparation. MED: conceptualization, resources, supervision, and project administration.
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Çayan, F., Tel-Çayan, G., Deveci, E. et al. HPLC–DAD characterization of phenolic profile and in vitro antioxidant, anticholinesterase, and antidiabetic activities of five mushroom species from Turkey. 3 Biotech 11, 273 (2021). https://doi.org/10.1007/s13205-021-02819-3
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DOI: https://doi.org/10.1007/s13205-021-02819-3