Abstract
Trametes versicolor (L.) Lloyd and Lepista nuda (Bull.) Cooke, known as an edible and medicinal mushroom, draws attention as a source of functional food development. Investigation of these fungal species on blood cultures in terms of human health will supplement the literature. In this study, the biomass of T. versicolor and L. nuda were used to prepare hot aqueous mycelium extracts (HAMEs). HAMEs were evaluated for antioxidant activity and cytotoxicity on human blood cultures (HBCs) in vitro. HBCs were initially incubated with HAMEs in 0.01-2 g/L dose ranges for 1 and 2 days and then analyzed. Firstly, the antioxidant activity on blood serum was determined by using Rel Assay kits with TAC (total antioxidant capacity), TOS (total oxidant status), and OSI (oxidative stress index) values. Secondly, cytotoxicity on lymphocytes was determined using neutral red uptake (NRU) and lactate dehydrogenase (LDH) assays. Doses of 0.05 to 0.5 g/L of T. versicolor and L. nuda increased TAC levels and decreased TOS values. 0.01 and 1 g/L did not change the TOS values but increased it by 2 g/L. In the second case, the dose range 0.01-1 g/L did not offer cytotoxic data. However, 2 g/L caused a 2 % increase in LDH and a 7 % decrease in NRU. As a result, this study presented that any evident signs of toxicity did not accompany T. versicolor and L. nuda HAMEs applications at 0.01-1 g/L dose ranges and 1–2 days on HBCs. The lack of toxicity supports the potential usage of T. versicolor and L. nuda in specified doses as a food or dietary supplement.
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Abbreviations
- Abs:
-
Absorbance
- C6H8O6 :
-
L-ascorbic acid
- DNA:
-
Deoxyribonucleic acid
- DPPH:
-
2,2-Diphenyl-1-picrylhydrazyl
- ePSP:
-
Extracellular polysaccharopeptides
- ELISA:
-
Enzyme-linked immunosorbent assay
- HAMEs:
-
Hot aqueous mycelium extracts
- HBCs:
-
Human blood cultures
- H2O2 :
-
Hydrogen peroxide
- KH2PO4 :
-
Potassium dihydrogen phosphate
- LDH:
-
Lactate dehydrogenase
- L. nuda :
-
Lepista nuda (Bull.) Cooke
- MgSO4 :
-
Magnesium sulfate
- MEA:
-
Malt extract agar
- Min:
-
Minute or minutes
- NRU:
-
Neutral red uptake
- Nm:
-
Nanometer
- OSI:
-
Oxidative stress index
- PDA:
-
Potato dextrose agar
- PSP:
-
Polysaccharopeptides
- ROS:
-
Reactive oxygen species
- rpm:
-
Revolutions per minute
- SOD:
-
Superoxide dismutase
- SPSS:
-
Statistical Package for Social Sciences
- SD:
-
Standard deviation
- TAC:
-
Total antioxidant capacity
- TOS:
-
Total oxidant status
- T. versicolor :
-
Trametes versicolor (L.) Lloyd.
References
Bach F, Helm CV, Bellettini MB, Maciel GM, Haminiuk CWI (2017) Edible mushrooms: a potential source of essential amino acids, glucans, and minerals. Int J Food Sci Technol 52:2382–2392. https://doi.org/10.1111/ijfs.13522
Bal C, Sevindik M, Akgul H, Selamoglu Z (2019) Oxidative stress index and antioxidant capacity of Lepista nuda collected from Gaziantep/Turkey. Sigma 37:1–5
Barros L, Dueñas M, Ferreira ICFR, Baptista P, Santos-Buelga C (2009) Phenolic acids determination by HPLC-DAD-ESI/MS in sixteen different Portuguese wild mushrooms species. Food Chem Toxicol 47:1076–1079. https://doi.org/10.1016/j.fct.2009.01.039
Beattie KD, Ulrich R, Grice ID, Uddin SJ, Blake TB, Wood KA, Steele J, Fontaine I, May TW, Tiralongo E (2011) Ethanolic and aqueous extracts derived from Australian fungi inhibit cancer cell growth in vitro. Mycologia 103:458–465. https://doi.org/10.3852/10-121
Bhattacharya S, Zhang Q, Carmichael PL, Boekelheide K, Andersen ME (2011) Toxicity testing in the 21 st century: defining new risk assessment approaches based on perturbation of intracellular toxicity pathways. PloS One 6:e20887. https://doi.org/10.1371/journal.pone.0020887
Ceri̇g S (2021) In vitro cytotoxic assessment of chitosan oligosaccharide lactate on human blood and lymphocyte cells. Eskişehir Tech Univ J Sci Technol C-Life Sci Biotechnol 10:79–89. https://doi.org/10.18036/estubtdc.798520
Cerig S, Geyikoglu F, Akpulat P, Colak S, Turkez H, Bakir M, Hosseinigouzdagani M, Koc K (2016) Carvacrol attenuates lung injury in rats with severe acute pancreatitis. Int J Bioeng Life Sci 10:301–308
Chaturvedi VK, Agarwal S, Gupta KK, Ramteke PW, Singh MP (2018) Medicinal mushroom: boon for therapeutic applications. 3 Biotech 8:334. https://doi.org/10.1007/s13205-018-1358-0
Chen HP, Liu JK (2017) Secondary metabolites from higher fungi. Prog Chem Org Nat Prod 106:1–201. https://doi.org/10.1007/978-3-319-59542-9_1
Chen MH, Lin CH, Shih CC (2014) Antidiabetic and antihyperlipidemic effects of Clitocybe nuda on glucose transporter 4 and AMP-activated protein kinase phosphorylation in high-fat-fed mice. Evid-Based Compl Alt Med 981046. https://doi.org/10.1155/2014/981046
Cheung PCK (2010) The nutritional and health benefits of mushrooms. Nutr Bull 35:292–299. https://doi.org/10.1111/j.1467-3010.2010.01859.x
Collins RA, Ng TB (1997) Polysaccharopeptides from Coriolus versicolor has potential for use against human immunodeficiency virus type 1 infection. Life Sci 60:383–387. https://doi.org/10.1016/S0024-3205(97)00294-4
Dudhatra GB, Mody SK, Awale MM, Patel HB, Modi CM, Kumar A, Kamani DR, Chauhan BN (2012) A comprehensive review on pharmacotherapeutics of herbal bio-enhancers. Sci World J 637953. https://doi.org/10.1100/2012/637953
Erel O (2004) A novel automated method to measure total antioxidant response against potent free radical reactions. Clin Biochem 37:112–119. https://doi.org/10.1016/j.clinbiochem.2003.10.014
Erel O (2005) A new automated colorimetric method for measuring total oxidant status. Clin Biochem 38:1103–1111. https://doi.org/10.1016/j.clinbiochem.2005.08.008
Ferreira ICFR, Barros L, Abreu RMV (2009) Antioxidants in wild mushrooms. Curr Med Chem 16:1543–1560. https://doi.org/10.2174/092986709787909587
Fisher RA (1918) The correlation between relatives on the supposition of Mendelian inheritance. Trans R Soc Edinb 52:399–433
Gallo A, Ferrara M, Perrone G (2013) Phylogenetic study of polyketide synthases and nonribosomal peptide synthetases involved in the biosynthesis of mycotoxins. Toxins 5:717–742. https://doi.org/10.3390/toxins5040717
Geyikoglu F, Cerig S, Ozdal M, Koc K, Algur OF, Yıldız GD, Gulmez O (2017) Toxicological evaluation of submerged liquid culture from Phanerochaete chrysosporium mycelium on human blood cells: cytotoxicity, genotoxicity, and oxidative damage. Int J Sec Metab 4:319–329. https://doi.org/10.21448/ijsm.373809
Godic A, Poljšak B, Adamic M, Dahmane R (2014) The role of antioxidants in skin cancer prevention and treatment. Oxid Med Cell Longev. https://doi.org/10.1155/2014/860479
Guo J, Liu X (2011) Comparison between liquid culture and solid culture technologies for edible mushroom spawn production and analysis on their economic benefits. Sci Agric Sin 44:835–841
Hor SY, Ahmad M, Farsi E, Lim CP, Asmawi MZ, Yam MF (2011) Acute and subchronic oral toxicity of Coriolus versicolor standardized water extract in Sprague-Dawley rats. J Ethnopharmacol 137:1067–1076. https://doi.org/10.1016/j.jep.2011.07.007
Hsieh TC, Kunicki J, Darzynkiewicz Z, Wu JM (2002) Effects of extracts of Coriolus versicolor (I’m-Yunity™) on cell-cycle progression and expression of interleukins – 1β, -6, and – 8 in Promyelocytic HL-60 leukemic cells and mitogenically stimulated and nonstimulated human lymphocytes. J Altern Complement Med 8:591–602. https://doi.org/10.1089/107555302320825101
Hsu JH, Li IC, Jiang Y, Chen CC (2015) Toxicological evaluation of Lepista nuda (Bull. ex Fr.) cooke mycelium produced by an in vitro culture methodology. Int J Pharm Sci 7:363–370
Hyde KD, Bahkali AH, Moslem MA (2010) Fungi-an unusual source for cosmetics. Fungal Divers 43:1–9. https://doi.org/10.1007/s13225-010-0043-3
Jedinak A, Sliva D (2008) Pleurotus ostreatus inhibits proliferation of human breast and colon cancer cells through p53-dependent as well as p53-independent pathway. Int J Oncol 33:1307–1313. https://doi.org/10.3892/ijo_00000122
Ju Y, Zhuo J, Liu B, Long C (2013) Eating from the wild: Diversity of wild edible plants used by Tibetans in Shangri-la region, Yunnan, China. J Ethnobiol Ethnomed 9:28. https://doi.org/10.1186/1746-4269-9-28
Kidd PM (2000) The use of mushroom glucans and proteoglycans in cancer treatment. Altern Med Rev 5:4–27
Klaus A, Kozarski M, Vunduk J, Todorovic N, Jakovljevic D, Zikzak Z, Pavlovic V, Levic S, Niksic M, Van Griensen LJ (2015) Biological potential of extracts of the wild edible Basidiomycete mushroom Grifola frondosa. Food Res Int 67:272–283. https://doi.org/10.1016/j.foodres.2014.11.035
Kobayashi Y, Kariya K, Saigenji K, Nakamura K (1994) Enhancement of anticancer activity of cis-diamine-dichloro platinum by the protein-bound polysaccharide of Coriolus versicolor QUEL (PS-K) in vitro. Cancer Biother 9:351–358. https://doi.org/10.1089/cbr.1994.9.351
Kolanjiappan K, Manoharan S, Kayalvizhi M (2002) Measurement of erythrocyte lipids, lipid peroxidation, antioxidants and osmotic fragility in cervical cancer patients. Clin Chim Acta 326:143–149. https://doi.org/10.1016/S0009-8981(02)00300-5
Lai CH, Teng JF, Hsu TH, Lin FY, Yang PW, Lo HC (2011) 28-day oral safety evaluation of extracellular polysaccharopeptides produced in submerged culture from the turkey tail medicinal mushroom Trametes versicolor (L.: Fr.) Pilát LH-1 in mice. Int J Med Mushrooms 13:3. https://doi.org/10.1615/IntJMedMushr.v13.i3.20
Lau CC, Abdullah N, Shuib AS, Aminudin N (2012) Proteomic analysis of antihypertensive proteins in edible mushrooms. J Agric Food Chem 60:12341–12348. https://doi.org/10.1021/jf3042159
Lau BF, Abdullah N, Aminudin N, Lee HB (2013) Chemical composition and cellular toxicity of ethnobotanical-based hot and cold aqueous preparations of the tiger′ s milk mushroom (Lignosus rhinocerotis). J Ethnopharmacol 150:252–262. https://doi.org/10.1016/j.jep.2013.08.034
Lee YS, Han JY, Joo EY, Shin SR, Kim NW (2005) Study on the anti-tumor effects of extracts from Lepista nuda mushroom. J Korean Soc Food Sci Nutr 34:317–322. https://doi.org/10.3746/jkfn.2005.34.3.317
Matkowski A (2008) Plant in vitro culture, for the production of antioxidants. Biotechnol Adv 26:584–560. https://doi.org/10.1016/j.biotechadv.2008.07.001
Mercan N, Duru ME, Turkoglu A, Gezer K, Kivrak I, Turkoglu H (2006) Antioxidant and antimicrobial properties of ethanolic extract from Lepista nuda (Bull.) Cooke. Ann Microbiol 56:339–344. https://doi.org/10.1007/BF03175028
Nogueira DR, Mitjans M, Rolim C, Vinardell MP (2014) Mechanisms underlying cytotoxicity induced by engineered nanomaterials: a review of in vitro studies. Nanomaterials 4:454–484. https://doi.org/10.3390/nano4020454
Ozdal M, Gülmez O, Ozdal OG, Algur OF (2019) Antibacterial and antioxidant activity of mycelial extracts of different Pleurotus species. Food Health 5:12–18. https://doi.org/10.3153/FH19002
Park YK, Lee HB, Jeon EJ, Jung HS, Kang MH (2004) Chaga mushroom extract inhibits oxidative DNA damage in human lymphocytes as assessed by comet assay. Biofactors 21:109–112
Phan CW, David P, Sabaratnam V (2017) Edible and medicinal mushrooms: emerging brain food for the mitigation of neurodegenerative diseases. J Med Food 20:1–10. https://doi.org/10.1089/jmf.2016.3740
Rathore H, Prasad S, Sharma S (2017) Mushroom nutraceuticals for improved nutrition and better human health: A review. PharmaNutrition 5:35–46. https://doi.org/10.1016/j.phanu.2017.02.001
Reis FS, Martins A, Vasconcelos MH, Morales P, Ferreira IC (2017) Functional foods based on extracts or compounds derived from mushrooms. Trends Food Sci Technol 66:48–62. https://doi.org/10.1016/j.tifs.2017.05.010
Repetto G, del Peso A, Zurita JL (2008) Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc 3:1125. https://doi.org/10.1038/nprot.2008.75
Sevindik M (2019) The novel biological tests on various extracts of Cerioporus varius. Fresenius Environ Bull 28:3713–3717
Sevindik M (2020) Antioxidant and antimicrobial capacity of Lactifluus rugatus and its antiproliferative activity on A549 cells. Indian J Tradit Know 19:423–427
Sevindik M, Akgul H, Bal C, Selamoglu Z (2018) Phenolic contents, oxidant/antioxidant potential and heavy metal levels in Cyclocybe cylindracea. Indian J Pharm Educ Res 52:437–441. https://doi.org/10.5530/ijper.52.3.50
Sevindik M, Akgul H, Selamoglu Z, Braidy N (2020) Antioxidant and antigenotoxic potential of infundibulicybe geotropa mushroom collected from Northwestern Turkey. Oxid Med Cell Longev 2020. https://doi.org/10.1155/2020/5620484
Souilem F, Fernandes Â, Calhelha RC, Barreira JC, Barros L, Skhiri F, Martins A, Ferreira ICFR (2017) Wild mushrooms and their mycelia as sources of bioactive compounds: Antioxidant, anti-inflammatory, and cytotoxic properties. Food Chem 230:40–48. https://doi.org/10.1016/j.foodchem.2017.03.026
Standish LJ, Wenner CA, Sweet ES, Bridge C, Nelson A, Martzen M, Novack J, Torkelson C (2008) Trametes versicolor mushroom immune therapy in breast cancer. J Soc Integr Oncol 6:122
Suparmin A, Kato T, Takemoto H, Park EY (2019) Metabolic comparison of aerial and submerged mycelia formed in the liquid surface culture of Cordyceps militaris. Microbiologyopen 8:9. https://doi.org/10.1002/mbo3.836
Wasser SP (2010) Medicinal mushroom science: history, current status, future trends, and unsolved problems. Int J Med Mushrooms 12:1. https://doi.org/10.1615/IntJMedMushr.v12.i1.10
Wei WS, Tan JQ, Guo F, Ghen HS, Zhou ZY, Zhang ZH, Gui L (1996) Effects of Coriolus versicolor polysaccharides on superoxide dismutase activities in mice. Acta Pharmacol Sin 17:174–178
Weidmann E, Brieger J, Jahn B, Hoelzer D, Bergmann L, Mitrou PS (1995) Lactate dehydrogenase-release assay: a reliable, nonradioactive technique for analysis of cytotoxic lymphocyte-mediated lytic activity against blasts from acute myelocytic leukemia. Ann Hematol 70:153–158. https://doi.org/10.1007/BF01682036
Wong CK, Tse PS, Wong ELY, Leung PC, Fung KP, Lam T. VERSİCOLOR K (2004) Immunomodulatory effects of Yun Zhi and danshen capsules in health subjects-a randomized, double-blind, placebo-controlled, crossover study. Int Immunopharmacol 4:201–211. https://doi.org/10.1016/j.intimp.2003.12.003
Zhang BB, Guan YY, Hu PF, Chen L, Xu GR, Liu L, Cheung PC (2019) Production of bioactive metabolites by submerged fermentation of the medicinal mushroom Antrodia cinnamomea: recent advances and future development. Crit Rev Biotechnol 39:541–554. https://doi.org/10.1080/07388551.2019.1577798
Zhao Y, Li J, Chen Y, Hang H (2009) Response to oxidative stress of Coriolus versicolor induced by exogenous hydrogen peroxide and paraquat. Ann Microbiol 59:221. https://doi.org/10.1007/BF03178320
Zhong JJ, Xiao JH (2009) Secondary metabolites from higher fungi: discovery, bioactivity, and bioproduction. Adv Biochem Eng Biotechnol 113:79–150. https://doi.org/10.1007/10_2008_26
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Cerig, S. A safety assessment of hot aqueous mycelium extracts from Trametes versicolor and Lepista nuda as a food supplement. Biologia 76, 2381–2391 (2021). https://doi.org/10.1007/s11756-021-00761-6
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DOI: https://doi.org/10.1007/s11756-021-00761-6