Evaluation of Some Biological Applications of Pleurotus citrinopileatus and Boletus edulis Fruiting Bodies

Author(s): Ahmed M. Younis, Marwa M. Abdel-Aziz, Mohamed Yosri*.

Journal Name: Current Pharmaceutical Biotechnology

Volume 20 , Issue 15 , 2019

Become EABM
Become Reviewer


Background: Mushrooms are deemed as a special delicacy in many countries. They are considered an important cuisine due to their bioactive ingredients and possible health benefits.

Methods: Herein, we measured selected biological properties of methanol extracts of Pleurotus citrinopileatus and Boletus edulis fruiting bodies including; in vitro antimicrobial activity, anti-α- glucosidase activity, antioxidant activity, anti-lipase activity and cytotoxic activity against different cancer cells and normal cells.

Results: B. edulis methanol extracts showed high antimicrobial and anti-α-glucosidase activity. In contrast, P. citrinopileatus methanol extracts showed superior antioxidant activity indicated by (1,1- diphenyl-2-picrylhydrazyl) DPPH radical scavenging with half maximal inhibitory concentration of IC50 37.4 µg/ml, anti-lipase activities with IC50 65.2 µg/ml and high cytotoxicity activity against HepG2 and HeLa cell lines with IC50 22.8 and 36.7 µg/ml, respectively. Flow cytometric analysis of the cell cycle was used to show apoptotic effects of methanol extracts against HepG2 and HeLa cells.

Conclusion: P. citrinopileatus and B. edulis methanolic extracts appear to contain biologically active compounds that might be used to treat some common human diseases.

Keywords: Pleurotus citrinopileatus, Boletus edulis, antimicrobial activity, antioxidant activity, antitumor activity, anti-α- glucosidase activity, anti-lipase activity, apoptosis.

Bandow, J.E.; Brötz, H.; Leichert, L.I.O.; Labischinski, H.; Hecker, M. Proteomic approach to understanding antibiotic action. Antimicrob. Agents Chemother., 2003, 47(3), 948-955.
[http://dx.doi.org/10.1128/AAC.47.3.948-955.2003] [PMID: 12604526]
Mbaveng, A.T.; Sandjo, L.P.; Tankeo, S.B.; Ndifor, A.R.; Pantaleon, A.; Nagdjui, B.T.; Kuete, V. Antibacterial activity of nineteen selected natural products against multi-drug resistant Gram-negative phenotypes. Springerplus, 2015, 4, 823.
[http://dx.doi.org/10.1186/s40064-015-1645-8] [PMID: 26753111]
Pereira, D.F.; Cazarolli, L.H.; Lavado, C.; Mengatto, V.; Figueiredo, M.S.; Guedes, A.; Pizzolatti, M.G.; Silva, F.R. Effects of flavonoids on α-glucosidase activity: Potential targets for glucose homeostasis. Nutrition, 2011, 27(11-12), 1161-1167.
[http://dx.doi.org/10.1016/j.nut.2011.01.008] [PMID: 21684120]
Mohan, S.; Nandhakumar, L. Role of various flavonoids: Hypotheses on novel approach to treat diabetes. J. Med. Hypo. Ideas, 2014, 8, 1-6.
Benhabyles, N.; Arab, K.; Bouchenak, O.; Baz, A. Phytochemical screening, hypoglycemic and antihyperglycemic effect of flavonoids from the leaves of Algerian Olea europaea L. in normal and alloxan-induced diabetic rats. Int. J. Pharmacol., 2015, 11(5), 477-483.
Oh, Y.S. Plant-derived compounds targeting pancreatic beta cells for the treatment of diabetes. Evid. Based Complement. Alternat. Med., 2015. 2015629863
[http://dx.doi.org/10.1155/2015/629863] [PMID: 26587047]
Kim, K.Y.; Nam, K.A.; Kurihara, H.; Kim, S.M. Potent α-glucosidase inhibitors purified from the red alga Grateloupia elliptica. Phytochemistry, 2008, 69(16), 2820-2825.
[http://dx.doi.org/10.1016/j.phytochem.2008.09.007] [PMID: 18951591]
Drew, B.S.; Dixon, A.F.; Dixon, J.B. Obesity management: Update on orlistat. Vasc. Health Risk Manag., 2007, 3(6), 817-821.
[PMID: 18200802]
Brug, J.; Crawford, D. The obesity pandemic. Is it bad or worse? Eur. J. Public Health, 2009, 19(6), 570-571.
[http://dx.doi.org/10.1093/eurpub/ckp160] [PMID: 19934226]
Jäger, S.; Trojan, H.; Kopp, T.; Laszczyk, M.N.; Scheffler, A. Pentacyclic triterpene distribution in various plants - rich sources for a new group of multi-potent plant extracts. Molecules, 2009, 14(6), 2016-2031.
[http://dx.doi.org/10.3390/molecules14062016] [PMID: 19513002]
Neovius, M.; Johansson, K.; Rössner, S. Head-to-head studies evaluating efficacy of pharmaco-therapy for obesity: A systematic review and meta-analysis. Obes. Rev., 2008, 9(5), 420-427.
[http://dx.doi.org/10.1111/j.1467-789X.2008.00463.x] [PMID: 18208467]
Viner, R.M.; Hsia, Y.; Tomsic, T.; Wong, I.C. Efficacy and safety of anti-obesity drugs in children and adolescents: Systematic review and meta-analysis. Obes. Rev., 2010, 11(8), 593-602.
[http://dx.doi.org/10.1111/j.1467-789X.2009.00651.x] [PMID: 19922432]
Mikulic-Petkovsek, M.; Samoticha, J.; Eler, K.; Stampar, F.; Veberic, R. Traditional elderflower beverages: A rich source of phenolic compounds with high antioxidant activity. J. Agric. Food Chem., 2015, 63(5), 1477-1487.
[http://dx.doi.org/10.1021/jf506005b] [PMID: 25646848]
Singh, R. Kumari. Comparative determination of phytochemicals and antioxidant activity from leaf and fruit of Sapindus mukorrossi Gaertn. A valuable medicinal tree. Ind. Crops Prod., 2015, 73, 1-8.
Bursal, E.; Köksal, E. Evaluation of reducing power and radical scavenging activities of water and ethanol extracts from sumac (Rhus coriaria L.). Food Res. Int., 2011, 44, 2217-2221.
Ismail, M.; Bagalkotkar, G.; Iqbal, S.; Adamu, H.A. Anticancer properties and phenolic contents of sequentially prepared extracts from different parts of selected medicinal plants indigenous to Malaysia. Molecules, 2012, 17(5), 5745-5756.
[http://dx.doi.org/10.3390/molecules17055745] [PMID: 22628046]
Surekha, C.; Kaladhar, D.S.; Raju, S.J. Evaluation of antioxidant and antimicrobial potentiality of some edible mushrooms. Int. J. Adv. Biotech. Res., 2011, 2(1), 130-134.https://www.researchgate.net/publication/213534731_EVALUATION_OF_ANTIOXIDANT_AND_ANTIMICROBIAL_POTENTIALITY_OF_SOME_EDIBLE_MUSHROOMS
Jonathan, G.; Loveth, K.; Elijah, O. Antagonistic effect of extracts of some nigerian higher fungi against selected pathogenic microorganisms American-Eurasian. J. Agric and Environ., 2007, 4, 364-368.http://www.idosi.org/aejaes/jaes2(4)/7.pdf
Aziz, T.; Mehmet, E.D.; Nazime, A.M. Antioxidant and antimicrobial activity of Russula delica Fr: An. Edi. Wild Mus. Eur. J. Anal. Chem., 2007, 2, 64-67.
Younis, A.M.; Wu, F.S.; El Shikh, H.H. Antimicrobial activity of extracts of the oyster culinary medicinal mushroom Pleurotus ostreatus (Higher Basidiomycetes) and identification of a new antimicrobial compound. Int. J. Med. Mushrooms, 2015, 17(6), 579-590.
[http://dx.doi.org/10.1615/IntJMedMushrooms.v17.i6.80] [PMID: 26349515]
Meng, T.X.; Ishikawa, H.; Shimizu, K.; Ohga, S.; Kondo, R. A glucosylceramide with antimicrobial activity from the edible mushroom Pleurotus citrinopileatus. J. Wood Sci., 2012, 58, 81-86.
Zhang, J.; Wang, G.; Li, H.; Zhuang, C.; Mizuno, T.; Ito, H.; Suzuki, C.; Okamoto, H.; Li, J. Antitumor polysaccharides from a Chinese mushroom, “yuhuangmo,” the fruiting body of Pleurotus citrinopileatus. Biosci. Biotechnol. Biochem., 1994, 58(7), 1195-1201.
[http://dx.doi.org/10.1271/bbb.58.1195] [PMID: 7765244]
Kosanić, M.; Ranković, B.; Dašić, M. Mushrooms as possible antioxidant and antimicrobial agents. Iran. J. Pharm. Res., 2012, 11(4), 1095-1102.
[PMID: 24250542]
Shu-Yao, T.; Hui-Li, T.; Jeng-Leun, M. Antioxidant properties of Agaricus blazei, Agrocybe cylindracea, and Boletus edulis. Lebensm. Wiss. Technol., 2007, 40, 1392-1402.
Sarikurkcu, C.; Tepe, B.; Yamac, M. Evaluation of the antioxidant activity of four edible mushrooms from the Central Anatolia, Eskisehir - Turkey: Lactarius deterrimus, Suillus collitinus, Boletus edulis, Xerocomus chrysenteron. Bioresour. Technol., 2008, 99(14), 6651-6655.
[http://dx.doi.org/10.1016/j.biortech.2007.11.062] [PMID: 18178083]
Lee, H.H.; Lee, S.; Lee, K.; Shin, Y.S.; Kang, H.; Cho, H. Anti-cancer effect of Cordyceps militaris in human colorectal carcinoma RKO cells via cell cycle arrest and mitochondrial apoptosis. Daru, 2015, 23(1), 35.
[http://dx.doi.org/10.1186/s40199-015-0117-6] [PMID: 26141646]
Sharma, J.R. Aphyllophorales of Himalaya; Botanical Survey of India, Salt Lake: Kolkata, 2012. DOI.org/10.11646/phytotaxa.246.2.5
Younis, A. Anticancer potential of Hericium ernaceus extracts against particular human cancer cell lines. Microbial BioSystems J. Microb. Biosys., 2017, 2(1), 9-20.http://fungiofegypt.com/Journal/index.html
Barros, L.; Falcão, S.; Baptista, P.; Freire, C.; Vilas-Boas, M.; Ferreira, I.C.F.R. Antioxidant activity of Agaricus sp. mushrooms by chemical, biochemical and electrochemical assays. Food Chem., 2008, 111, 61-66.
Younis, A.; Stewart, J.; Wu, F.S.; El Shikh, H.; Hassan, F.; Elaasser, M. Effectiveness of different solvents extracts from edible mushrooms in inhibiting the growth of tumor cells. Cancer Biol., 2014, 4(4), 1-15.
Ramesh, Ch.; Pattar, M.G. Antimicrobial properties, antioxidant activity and bioactive compounds from six wild edible mushrooms of western ghats of Karnataka, India. Pharmacognosy Res., 2010, 2(2), 107-112.
[http://dx.doi.org/10.4103/0974-8490.62953] [PMID: 21808550]
Souza, L.K. Fernandes, Ode.F.; Kobayashi, C.C.; Passos, X.S.; Costa, C.R.; Lemos, J.A.; Souza-Júnior, A.H.; Silva, Mdo.R. Antifungal susceptibilities of clinical and environmental isolates of Cryptococcus neoformans in Goiânia city, Goiás, Brazil. Rev. Inst. Med. Trop. São Paulo, 2005, 47(5), 253-256.
[http://dx.doi.org/10.1590/S0036-46652005000500003] [PMID: 16302107]
Shi, M.; Zhang, Z.; Yang, Y. Antioxidant and immunoregulatory activity of Ganoderma lucidum polysaccharide (GLP) Carbohydr. Polym, 2013, 5, 95(1), 200-206.
Kim, Y.S.; Lee, Y.M.; Kim, H.; Kim, J.; Jang, D.S.; Kim, J.H.; Kim, J.S. Anti-obesity effect of Morus bombycis root extract: Anti-lipase activity and lipolytic effect. J. Ethnopharmacol., 2010, 130(3), 621-624.DOI.org/10.1016/j.jep.2010.05.053
[http://dx.doi.org/10.1016/j.jep.2010.05.053] [PMID: 20669373]
Shai, L.J.; Magano, S.R.; Lebelo, S.L.; Mogale, A.M. Inhibitory effects of five medicinal plants on rat alpha-glucosidase: Comparison with their effects on yeast alpha-glucosidase. J. Med. Plants Res., 2011, 5, 2863-2867.https://www.researchgate.net/publication/250002943_Inhibitory_effects_of_five_medicinal_plants_on_rat_alphaglucosidase_Comparison_with_their_effects_on_yeast_alpha-glucosidase
Li, W.C.; Ralphs, K.L.; Tosh, D. Isolation and culture of adult mouse hepatocytes. Methods Mol. Biol., 2010, 633, 185-196.
[http://dx.doi.org/10.1007/978-1-59745-019-5_13] [PMID: 20204628]
Shabna, M.; Maha, M.S.; Shahira, M.E.; Laila, R.I.J. In vitro and in vivo anticancer activity of the fruit peels of Solanum melongena L. against hepatocellular carcinoma. Carcinogene Mutagene, 2013, 4, 3.
[http://dx.doi.org/10.4172/2157- 2518.1000149]
Riccardi, C.; Nicoletti, I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat. Protoc., 2006, 1(3), 1458-1461.
[http://dx.doi.org/10.1038/nprot.2006.238] [PMID: 17406435]
Sandrina, A.; Heleno, R.C.; Amilcar, L.A.; Maria-João, R.P.; Lillian, B.; Isabel, C.F. Nutritional value, bioactive compounds and antioxidant properties of three edible mushrooms from Poland. Food Biosci., 2015, 11 , 48-55.
Giannenas, I.; Pappas, I.S.; Mavridis, S.; Kontopidis, G.; Skoufos, J.; Kyriazakis, I. Performance and antioxidant status of broiler chickens supplemented with dried mushrooms (Agaricus bisporus) in their diet. Poult. Sci., 2010, 89(2), 303-311.
[http://dx.doi.org/10.3382/ps.2009-00207] [PMID: 20075283]
Younis, A.; Stewart, J.; Wu, F.S.; El Shikh, H.; Hassan, F.; Elaasser, M. Cytotoxic Activity of edible mushrooms extracts against tumor cell lines. Int. J. Sci. Technol., 2014, 3(11), 736-749.
Fogarasi, M.; Socaci, S.A.; Dulf, F.V.; Diaconeasa, Z.M.; Fărcaș, A.C.; Tofană, M.; Semeniuc, C.A. Bioactive compounds and volatile profiles of five transylvanian wild edible mushrooms. Molecules, 2018, 23(12) E3272https://www.mdpi.com/1420-3049/23/12/3272
[PMID: 30544917]
Wang, J.C.; Hu, S.H.; Liang, Z.C.; Yeh, C.J. Optimization for the production of water-soluble polysaccharide from Pleurotus citrinopileatus in submerged culture and its antitumor effect. Appl. Microbiol. Biotechnol., 2005, 67(6), 759-766.
[http://dx.doi.org/10.1007/s00253-004-1833-x] [PMID: 15703910]
Novakovic, A.; Karaman, M.; Kaisarevic, S.; Radusin, T.; Llic, N. Antioxidant and antiproliferative potential of fruiting bodies of the wild-growing king bolete mushroom, Boletus edulis (Agaricomycetes), from Western Serbia. Int. J. Med. Mushrooms, 2017, 19(1), 27-34.
[http://dx.doi.org/10.1615/IntJMedMushrooms.v19.i1.30] [PMID: 28322144]
Giannenasa, I.; Tsalieb, E.; Chronisc, E.; Mavridisd, S.; Tontisb, D.; Kyriazakis, I. Consumption of Agaricus bisporus mushroom affects the performance, intestinal microbiota composition and morphology, and antioxidant status of turkey poults. Anim. Feed Sci. Technol., 2011, 165, 218-229.
Bodoira, R.; Velez, A.; Andreatta, A.E.; Martínez, M.; Maestri, D. Extraction of bioactive compounds from sesame (Sesamum indicum L.) defatted seeds using water and ethanol under sub-critical conditions. Food Chem., 2017, 237, 114-120.
[http://dx.doi.org/10.1016/j.foodchem.2017.05.102] [PMID: 28763962]
Younis, A.M.; Yosri, M.; Stewart, J.K. In vitro evaluation of pleiotropic properties of wild mushroom Laetiporus sulphureus; Ann. Agricult. Sci, 2019.
Merdivan, S Lindequist U Ergosterol Peroxide: A Mushroom-Derived Compound with Promising Biological Activities-A Review. Int. J. Med. Mushrooms, 2017, 19(2), 93-105.
[http://dx.doi.org/Doi: 10.1615/IntJMedMushrooms.v19. i2.10] [PMID: 28436318]
van Heijenoort, J. Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology, 2001, 11(3), 25R-36R.
[http://dx.doi.org/10.1093/glycob/11.3.25R] [PMID: 11320055]
Farkaš, V. Structure and biosynthesis of fungal cell walls: Methodological approaches. Folia Microbiol. (Praha), 2003, 48(4), 469-478.
[http://dx.doi.org/10.1007/BF02931327] [PMID: 14533477]
Vamanu, E.; Nita, S. Antioxidant capacity and the correlation with major phenolic compounds, anthocyanin, and tocopherol content in various extracts from the wild edible Boletus edulis mushroom. BioMed Res. Int., 2013, 2013 313905
[http://dx.doi.org/10.1155/2013/313905] [PMID: 23509707]
Hu, S.H.; Wang, J.C.; Lien, J.L.; Liaw, E.T.; Lee, M.Y. Antihyperglycemic effect of polysaccharide from fermented broth of Pleurotus citrinopileatus. Appl. Microbiol. Biotechnol., 2006, 70(1), 107-113.
[http://dx.doi.org/10.1007/s00253-005-0043-5] [PMID: 16001252]
Gross, P. New roles for polyphenols: A 3-part report on current regulations & the state of science: FDA’s antioxidant guidance: Is this the end of the road for marketing polyphenols as antioxidants?; Nutraceuticals World, 2019. https://www.thefreelibrary.com/New+roles+ for+ polyphenols% 3a+a+3-part+report+on+current+regulations+%26...-a0196242906
Williams, R.J.; Spencer, J.P.; Rice-Evans, C. Flavonoids: Antioxidants or signalling molecules? Free Radic. Biol. Med., 2004, 36(7), 838-849.
[http://dx.doi.org/10.1016/j.freeradbiomed.2004.01.001] [PMID: 15019969]
Tajik, N.; Tajik, M.; Mack, I.; Enck, P. The potential effects of chlorogenic acid, the main phenolic components in coffee, on health: A comprehensive review of the literature. Eur. J. Nutr., 2017, 56(7), 2215-2244.
[http://dx.doi.org/10.1007/s00394-017-1379-1] [PMID: 28391515]
Libin, S.; We, H.; Guang, X.; Pengju, C.; Yin, Z.; Zhiyong, Z.; Yunyun, W.I.; Bingxin, S.; Xiaowen, W. Volatile components, total phenolic compounds, and antioxidant capacities of worm-infected Gomphidius rutilus. Food Sci. Hum. Wellness, 2018, 7(2), 148-155.
Chen, J.N.; de Mejia, E.G.; Wu, J.S. Inhibitory effect of a glycoprotein isolated from golden oyster mushroom (Pleurotus citrinopileatus) on the lipopolysaccharide-induced inflammatory reaction in RAW 264.7 macrophage. J. Agric. Food Chem., 2011, 59(13), 7092-7097.
[http://dx.doi.org/10.1021/jf201335g] [PMID: 21627087]
Reis, F.S.; Barros, L.; Calhelha, R.C.; Cirić, A.; van Griensven, L.J.; Soković, M.; Ferreira, I.C.; Isabel, C.F. The methanolic extract of Cordyceps militaris (L.) Link fruiting body shows antioxidant, antibacterial, antifungal and antihuman tumor cell lines properties. Food Chem. Toxicol., 2013, 62, 91-98.
[http://dx.doi.org/10.1016/j.fct.2013.08.033] [PMID: 23994083]
Patell, S.; Goyal, A. Recent developments in mushrooms as anticancer therapeutics. A review. 3 Biotech, 2012, 2(1), 1-15.
Li, Y.R.; Liu, Q.H.; Wang, H.X.; Ng, T.B. A novel lectin with potent antitumor, mitogenic and HIV-1 reverse transcriptase inhibitory activities from the edible mushroom Pleurotus citrinopileatus. Biochim. Biophys. Acta, 2008, 1780(1), 51-57.
[http://dx.doi.org/10.1016/j.bbagen.2007.09.004] [PMID: 17961926]
Lemieszek, M.K.; Cardoso, C.; Ferreira Milheiro Nunes, F.H.; Ramos, N.A.; Barros, A.I. Marques, G.; Pożarowski, P.; Rzeski, W. Boletus edulis biologically active biopolymers induce cell cycle arrest in human colon adenocarcinoma cells. Food Funct., 2013, 4(4), 575-585.
Sun, Y.S.; Lv, L.X.; Zhao, Z.; He, X.; You, L.; Liu, J.K.; Li, Y.Q. Cordycepol C induces caspase-independent apoptosis in human hepatocellular carcinoma HepG2 cells. Biol. Pharm. Bull., 2014, 37(4), 608-617.
[http://dx.doi.org/10.1248/bpb.b13-00877] [PMID: 24694607]

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Page: [1309 - 1320]
Pages: 12
DOI: 10.2174/1389201020666190904162403
Price: $65

Article Metrics

PDF: 26
PRC: 1