Toxicological evaluation of submerged liquid culture from Phanerochaete chrysosporium mycelium on human blood cells: cytotoxicity, genotoxicity and oxidative damage

Fatime Geyikoglu, Salim Cerig, Murat Ozdal, Kübra Koc, Omer Faruk Algur, Gulsah Deniz Yildiz, Ozlem Gülmez

Abstract


Mushrooms produce a variety of bioactive antioxidant secondary metabolites including ectins, polysaccharides, pigments, phenolic compounds, sterols and terpenes. Extracellular and intracellular compounds produced by submerged liquid fermentation are important industrially and economically. Phanerochaete chrysosporium (PC) is the model white-rot fungus that easy cultivation on lignocellulose-containing substrates. PC can be used as a bioprotein source. Aims of this study were to determine the in vitro antioxidant, cytotoxic and genotoxic effects of hot water extract obtained from PC on human peripheral blood monunuclear cells (hPBMCs). Cytotoxicity was determined by lactate dehydrogenase (LDH) leakeage assay and neutral red (NR). Total antioxidant capacity (TAC) and total oxidant status (TOS) were detected to determine the oxidative damage. Genotoxicity was characterized by micronuclei and chromosome aberrations assays for specify DNA damage. PC (5-75 µg/ml) significantly increased antioxidant capacity and these doses did not cause any significant alterations to cytotoxicity on hPBMCs. The elavated doses of PC (5-250 µg/ml) did not cause increase in genotoxic. Whereas, 250 and 500 µg/ml doses of PC statistically increased TOS levels, NR uptake, LDH release, CA/cell frequency and MN formation however decreased TAC levels. This study is the first time on cytotoxicity, genotoxicity and oxidative damage of PC on hPBMCs. In conclusion, the consumption of PC can be safe for humans, but it has also exposure period and dose-dependent effects on inducing oxidative damage and toxicity on hPBMCs.


Keywords


Phanerochaete chrysosporium, human blood cells, cytotoxic, genotoxic, antioxidant

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De Silva, D. D., Rapior, S., Sudarman, E., Stadler, M., Xu, J., Alias, S. A., & Hyde, K. D. (2013). Bioactive metabolites from macrofungi: ethnopharmacology, biological activities and chemistry. Fungal Diversity, 62(1), 1-40.

Dey, T. B., Chakraborty, S., Jain, K. K., Sharma, A., & Kuhad, R. C. (2016). Antioxidant phenolics and their microbial production by submerged and solid state fermentation process: A review. Trends in Food Science & Technology, 53, 60-74.

Dundar, A., Okumus, V., Ozdemir, S., & Yildiz, A. (2013). Antioxidant properties of cultured mycelia from four Pleurotus species produced in submerged medium. International journal of food properties, 16(5), 1105-1116.

Ozen, T., Darcan, C., Aktop, O., & Turkekul, I. (2011). Screening of antioxidant, antimicrobial activities and chemical contents of edible mushrooms wildly grown in the Black Sea region of Turkey. Combinatorial Chemistry & High Throughput Screening, 14(2), 72-84.

Ajila, C. M., Brar, S. K., Verma, M., Tyagi, R. D., & Valéro, J. R. (2011). Solid-state fermentation of apple pomace using Phanerocheate chrysosporium–Liberation and extraction of phenolic antioxidants. Food Chemistry, 126(3), 1071-1080.

Marcotrigiano, V., De Giglio, O., Quaranta, A., Montagna, M. T., & Napoli, C. (2013). Mushroom consumption and toxicity, state of the art. Igiene e sanita pubblica, 69(3), 349-361.

Yu, S., Wu, X., Ferguson, M., Simmen, R. C., Cleves, M. A., Simmen, F. A., & Fang, N. (2016). Diets Containing Shiitake Mushroom Reduce Serum Lipids and Serum Lipophilic Antioxidant Capacity in Rats. The Journal of nutrition, 146(12), 2491-2496.

Ibero-Baraibar, I., Azqueta, A., Lopez de Cerain, A., Martinez, J. A., & Zulet, M. A. (2014). Assessment of DNA damage using comet assay in middle-aged overweight/obese subjects after following a hypocaloric diet supplemented with cocoa extract. Mutagenesis, 30(1), 139-146.

Erel, O. (2004). A novel automated method to measure total antioxidant response against potent free radical reactions. Clinical biochemistry, 37(2), 112-119.

Geyikoglu, F., & Turkez, H. (2008). Boron compounds reduce vanadium tetraoxide genotoxicity in human lymphocytes. Environmental toxicology and pharmacology, 26(3), 342-347.

Vergaro, V., Aldieri, E., Fenoglio, I., Marucco, A., Carlucci, C., & Ciccarella, G. (2016). Surface reactivity and in vitro toxicity on human bronchial epithelial cells (BEAS-2B) of nanomaterials intermediates of the production of titania-based composites. Toxicology in Vitro, 34, 171-178.

Fields, W., Fowler, K., Hargreaves, V., Reeve, L., & Bombick, B. (2017). Development, qualification, validation and application of the neutral red uptake assay in Chinese Hamster Ovary (CHO) cells using a VITROCELL® VC10® smoke exposure system. Toxicology in Vitro, 40, 144-152.

Turkez, H., Geyikoğlu, F., Dirican, E., & Tatar, A. (2012). In vitro studies on chemoprotective effect of borax against aflatoxin B1-induced genetic damage in human lymphocytes. Cytotechnology, 64(6), 607-612.

Akbaba, B. G., Turkez, H., Sonmez, E., & Akbaba, U. (2016). In vitro genotoxicity evaluation of tungsten (VI) oxide nanopowder using human lymphocytes. Biomedical Research.

Liu, N., Guan, Y., Xue, L., Yu, Y., Xiao, J., Chang, Z., ... & Guan, W. (2017). Assessment of DNA/Chromosome Damage in the Peripheral Blood Lymphocytes of Workers Exposed to Indium Compounds. Toxicological Sciences, 157(1), 41-49.

Fenech, M., Holland, N., Zeiger, E., Chang, W. P., Burgaz, S., Thomas, P., ... & Bonassi, S. (2011). The HUMN and HUMNxL international collaboration projects on human micronucleus assays in lymphocytes and buccal cells—past, present and future. Mutagenesis, 26(1), 239-245.

Vamanu, E. (2012). In vitro antimicrobial and antioxidant activities of ethanolic extract of lyophilized mycelium of Pleurotus ostreatus PQMZ91109. Molecules, 17(4), 3653-3671. [18] Kim, I. S., Yang, M. R., Lee, O. H., & Kang, S. N. (2011). Antioxidant activities of hot water extracts from various spices. International journal of molecular sciences, 12(6), 4120-4131.

] Guideline, O. T. (1997). 475: mammalian bone marrow chromosomal aberration test.

Fenech, M. (1993). The cytokinesis-block micronucleus technique and its application to genotoxicity studies in human populations. Environmental health perspectives, 101(Suppl 3), 101.

Surrallés, J., Antoccia, A., Creus, A., Degrassi, F., Peris, F., Tanzarella, C., ... & Marcos, R. (1994). The effect of cytochalasin-B concentration on the frequency of micronuclei induced by four standard mutagens. Results from two laboratories. Mutagenesis, 9(4), 347-353.

Boonsong, S., Klaypradit, W., & Wilaipun, P. (2016). Antioxidant activities of extracts from five edible mushrooms using different extractants. Agriculture and Natural Resources, 50(2), 89-97.

Kosanić, M., Ranković, B., Rančić, A., & Stanojković, T. (2016). Evaluation of metal concentration and antioxidant, antimicrobial, and anticancer potentials of two edible mushrooms Lactarius deliciosus and Macrolepiota procera. journal of food and drug analysis, 24(3), 477-484.

Taofiq, O., González-Paramás, A. M., Martins, A., Barreiro, M. F., & Ferreira, I. C. (2016). Mushrooms extracts and compounds in cosmetics, cosmeceuticals and nutricosmetics—A review. Industrial Crops and Products, 90, 38-48.

Lee, Y. L., Huang, G. W., Liang, Z. C., & Mau, J. L. (2007). Antioxidant properties of three extracts from Pleurotus citrinopileatus. LWT-Food Science and Technology, 40(5), 823-833.

González-Palma, I., Escalona-Buendía, H. B., Ponce-Alquicira, E., Téllez-Téllez, M., Gupta, V. K., Díaz-Godínez, G., & Soriano-Santos, J. (2016). Evaluation of the Antioxidant Activity of Aqueous and Methanol Extracts of Pleurotus ostreatus in Different Growth Stages. Frontiers in microbiology, 7.

Gregori, A., Švagelj, M., & Pohleven, J. (2007). Cultivation techniques and medicinal properties of Pleurotus spp. Food Technology & Biotechnology, 45(3).

Jayasuriya, W. J. A., Wanigatunge, C. A., Fernando, G. H., Abeytunga, D. T. U., & Suresh, T. S. (2015). Hypoglycaemic activity of culinary Pleurotus ostreatus and P. cystidiosus mushrooms in healthy volunteers and type 2 diabetic patients on diet control and the possible mechanisms of action. Phytotherapy research, 29(2), 303-309.

Panthong, S., Boonsathorn, N., & Chuchawankul, S. (2016). Antioxidant activity, anti-proliferative activity, and amino acid profiles of ethanolic extracts of edible mushrooms. Genetics and molecular research: GMR, 15(4).

Jiang, J., Liu, H., Li, Q., Gao, N., Yao, Y., & Xu, H. (2015). Combined remediation of Cd–phenanthrene co-contaminated soil by Pleurotus cornucopiae and Bacillus thuringiensis FQ1 and the antioxidant responses in Pleurotus cornucopiae. Ecotoxicology and environmental safety, 120, 386-393.

Abidin, M. H. Z., Abdullah, N., & Abidin, N. Z. (2016). Protective effect of antioxidant extracts from grey oyster mushroom, Pleurotus pulmonarius (Agaricomycetes), against human low-density lipoprotein oxidation and aortic endothelial cell damage. International journal of medicinal mushrooms, 18(2).

Lin, S. Y., Chien, S. C., Wang, S. Y., & Mau, J. L. (2016). Nonvolatile taste components and antioxidant properties of fruiting body and mycelium with high ergothioneine content from the culinary-medicinal golden oyster mushroom Pleurotus citrinopileatus (Agaricomycetes). International journal of medicinal mushrooms, 18(8).

Zhang, J., Meng, G., Zhang, C., Lin, L., Xu, N., Liu, M., ... & Jia, L. (2015). The antioxidative effects of acidic-, alkalic-, and enzymatic-extractable mycelium zinc polysaccharides by Pleurotus djamor on liver and kidney of streptozocin-induced diabetic mice. BMC complementary and alternative medicine, 15(1), 440.

Dundar, A., Okumus, V., Ozdemir, S., Celik, K. S., Boga, M., Ozcagli, E., ... & Yildiz, A. (2015). Antioxidant, antimicrobial, cytotoxic and anticholinesterase activities of seven mushroom species with their phenolic acid composition. J Hortic, 2, 161.

Yang, Y., Fan, C., Wang, B., Ma, Z., Wang, D., Gong, B., ... & Yang, Z. (2017). Pterostilbene attenuates high glucose-induced oxidative injury in hippocampal neuronal cells by activating nuclear factor erythroid 2-related factor 2. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease, 1863(4), 827-837.

Ryu, T. H., Kim, J. H., & Kim, J. K. (2016). Chromosomal aberrations in human peripheral blood lymphocytes after exposure to ionizing radiation. Genome integrity, 7.

Guo, X., Ni, J., Xue, J., & Wang, X. (2017). Extract of bulbus Fritillaria cirrhosa perturbs spindle assembly checkpoint, induces mitotic aberrations and genomic instability in human colon epithelial cell line. Experimental and Toxicologic Pathology, 69(3), 163-171.

Radakovic, M., Djelic, N., Stevanovic, J., Sokovic, M., Radovic, D., Van Griensven, L. J. L. D., & Stanimirovic, Z. (2015). Evaluation of the antigenotoxic effects of the royal sun mushroom, Agaricus brasiliensis (Higher basidiomycetes) in human lymphocytes treated with thymol in the comet assay. International journal of medicinal mushrooms, 17(4).


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