<<

View metadata, citation and similar papers at core.ac.uk brought to you by CORE

provided by Jagiellonian Univeristy Repository

Acta Sci. Pol. Hortorum Cultus, 16(1) 2017, 151–161 www.acta.media.pl ISSN 1644-0692

ORIGINAL PAPER Accepted: 28.09.2016

EDIBLE ostreatus ( MUSHROOM) – ITS DIETARY SIGNIFICANCE AND BIOLOGICAL ACTIVITY

Kamil Piska, Katarzyna Sułkowska-Ziaja, Bożena Muszyńska

Jagiellonian University Medical College in Kraków

ABSTRACT (Jacq.) P. Kumm. () – known as the oyster mushroom – is a mushroom species distributed on all continents, except for Antarctica. Since World War I it has been commercially cultivated on a large scale. Pleurotus ostreatus is a valuable mushroom of dietary importance. It is rich in primary and secondary metabolites and chemical elements of physiological significance. One hundred grams of fresh fruiting bodies contains 15% of the recommended daily intake of C, 40% of , , and thiamin, and 0.5 mg of vitamin B12. This species is also characterized by a high content of oleic acid (40%), linolenic acid (55%), and substances responsible for decreasing serum cholesterol levels. High contents of lovastatin, an approved hypolipidemic , and pleuran, an immunomodulating polysac- charide, have been found in fruiting bodies of this species. It exhibits antiatherosclerotic, hypoglycemic, an- tioxidant, anticancer and immunomodulatory properties. Due to its wide spectrum of biological activities, P. ostreatus is considered a medicinal mushroom. Fruiting bodies and extracts of P. ostreatus have found applications in the treatment of civilization – related , especially diabetes, arteriosclerosis and can- cer. It is also a potential source of active ingredients in cosmetics and topically applied preparations. Key words: antioxidant activity, , lovastatin, Pleurotus ostreatus, pleuran

INTRODUCTION

Pleurotus ostreatus (Jacq.) P. Kumm. (Basidio- ing trees, especially hornbeam (Carpinus sp.), beech mycota), of the family, comes from (Fagus sp.), (Salix sp.), poplar (Populus sp.), ; however, nowadays it is distributed all over birch-tree (Betula sp.) and common walnut (Juglans the world, except for the north-west Pacific because regia). This species produces different sized, grouped of the arctic climate. Cultivation methods were de- fruiting bodies in forms resembling a colony of oys- veloped in Germany during World War I and then ters, which has led to its given name of P. ostreatus. successfully applied on a large scale. This was the Fruiting bodies are pink, gray to dark-brown in color, result of the search for new food sources, due to the ranging in a size from 4 to 15 cm (phot. 1). In the problem of hunger in Germany. In , P. os- wild, its fruiting bodies generally appear in autumn treatus is a common species [Wojewoda 2003]. (October–November); however, they may be encoun- It is found on dead wood and the branches of liv- tered during mild winters or in early, warm springs.

[email protected]

© Copyright by Wydawnictwo Uniwersytetu Przyrodniczego w Lublinie Piska, K., Sułkowska-Ziaja, K., Muszyńska, B. (2017). Edible mushroom Pleurotus ostreatus (Oyster mushroom) – its dietary significance and biological activity. Acta Sci. Pol. Hortorum Cultus, 16(1), 151–161.

Pleurotus ostreatus is tolerant of low temperatures; species of dietary and medical significance [Anandhi however, it has high requirements for light – under et al. 2013, Muszyńska et al. 2014, Caz et al. 2015]. low light conditions it does not produce fruiting bod- ies, or produces very small ones [Wojewoda 2003]. Chemical composition of Pleurotus ostreatus After bisporus, P. ostreatus is the sec- The content of water in fresh fruiting bodies of ond most cultivated edible mushroom and is of great Pleurotus ostreatus is about 80–90% similarly as is eco-nomic significance [Sanches 2010]. It has a bit- the case in other fungi. From 100 g , 10 g tersweet smell of benzaldehyde, characteristic of dried fruits are obtained, consisting of 2.5 g and almonds [Beltran-Garcia et al. 1997]. In and about 5 g polysaccharides – mainly starch and many countries, especially in Asia it is considered a others such as mannitol and trehalose. The mycelium delicacy, while in the Czech Republic and Slovakia it of P. ostreatus has great nutritional value, due to the is used as a meat substitute [Beltran-Garcia et al. presence of high contents of amino acids (arginine, 1997, Sanches 2010]. It is cultivated on straw – its alanine, glutamine, glutamic acid). In 100 g of fresh mycelium is able to decompose, transform and use mycelia, the level of vitamin C represents 15% of the biomass of lignin-cellulose crop wastes for growth. recommended daily intake for humans. This species This process also has significance in the waste bio- also contains 0.1–0.2 g , including oleic acid degradation. (40%), linolenic acid (55%), and other compounds This species has been shown to have a higher with hypocholesterolemic action. The content of yield and growth than other cultivated mushrooms. saturated fatty acid is relatively small (≈10%) [Barros In recent decades a great increase in the international et al. 2007]. cultivation of P. ostreatus has been noted due to its One of the most important compounds in P. os- significant tolerance of varied agroclimatic condi- treatus is lovastatin – an approved to market drug tions [Sanches 2010, Kholoud et al. 2014]. used in the treatment of dyslipidemia – that acts as an inhibitor of HMG-CoA reductase (see section Bio- logical activity of P. ostreatus). The highest content of lovastatin was found in of mature mush- rooms [Gunde-Cimerman and Cimerman 1995]. Var- iable amounts of lovastatin have been demonstrated for samples coming from different countries. Pleuro- tus ostreatus from , Taiwan, and Korea con- tained 606.5 µg, 216.4 µg and 165.3 µg (per 1 g of DW), respectively. Variability was found in terms of the contents of ergothioneine (944.1–1829 µg) and γ-aminobutyric acid – GABA (0–23.6 µg) [Shin-Yu et al. 2012]. Ergothioneine was detected in cultivated P. ostreatus from Ethiopia: 3.78 µg g-1 DW [Wolde- giorgis et al. 2014]. Ergothioneine is a compound Phot. 1. Pleurotus ostreatus Jacq.: Fr. Kummer (Basidiomycota) – Oyster mush- which is accumulated in animal cells and tissues exposed to oxidative stress; however, it is not endog- room. Photo by B. Muszyńska enously synthetized. It plays a role not only as an antioxidant, but also as an antimutagenic, chemo- and Because of its contents of readily digest- radioprotective agent; hence, ergothioneine is consid- ible proteins, salts, , and compounds ered a compound suitable in adjuvant treatment of with potent pharmacological activities, e.g. lovastatin strokes, neurodegeneration, and cardio-vascular dis- and pleuran, P. ostreatus is an important mushroom eases [Cheah and Halliwell 2012, Woldegiorgis et al. 2014].

152 www.acta.media.pl Piska, K., Sułkowska-Ziaja, K., Muszyńska, B. (2017). Edible mushroom Pleurotus ostreatus (Oyster mushroom) – its dietary significance and biological activity. Acta Sci. Pol. Hortorum Cultus, 16(1), 151–161.

In extracts of P. ostreatus, researchers have found humans include acceleration of wound healing, an an active β-glucan, named pleuran (fig. 1). This is increase in mental performance, protection of eye characterized as an immunomodulatory agent with yellow macula against degeneration, and antioxidant potential applications in the treatment of cancer, in- properties [Powell 2000, Noormagi et al. 2010]. fections and immune system disorders [Devi et al. Among the phenolic content, flavonoids and phe- 2013, Devi et al. 2015]. Pleuran is a branched poly- nolic acids have been found. The phenolic com- saccharide, where the backbone consists of β-D- pounds include p-hydroxybenzoic, synapic, ferulic, glucopyra- nosyl linked with (1→3) bonds, and every p-coumaric, protocatechuic, vanillic, caffeic, gallic, fourth residue is substituted with a (1→6) D- homogentisic, gentisic and chlorogenic acids glucopyranosyl group [Karácsonyi and Kuniakb [Meetoo et al. 2007, Kim et al. 2008, Alam et al. 1994]. It may contain a small proportion of interior 2010, Palacios et al. 2011, Muszyńska et al. 2013, (1→6) and (1→4)-linked residues [Karácsonyi and Woldegiorgis et al. 2014, Gąsecka et al. 2015], while Kuniakb 1994, Fričová and Koval’akovà 2013]. the flavonoids are myricetin, naringenin, hesperidin, formononetin and biochanin A [Alam et al. 2010, Palacios et al. 2011, Muszyńska et al. 2013, Wolde- giorgis et al. 2014, Gąsecka et al. 2015]. The levels of individual phenolic compounds are presented in Table 1. Indicated differences among studies may be the result of different methods of mushroom cultiva- tion, preparation, extraction, as well as geographical variability [Alam et al. 2010, Palacios et al. 2011, Muszyńska et al. 2013, Woldegiorgis et al. 2014, Gąsecka et al. 2015].

Fig. 1. Pleuran (author: B. Muszyńska) Biological activity of P. ostreatus Pleurotus ostreatus showed a wide spectrum of High contents of mineral salts of potassium, biological activities, among which its hypoglycemic , calcium, iron, copper, , magnesium, properties are the focus of great interest. Diabetes and selenium were found in mycelium of P. ostreatus mellitus is one of the most common civilization – [Muszyńska et al. 2016]. Because of the increasing related diseases, found both in developed and devel- interest in mushrooms as a source of macro- and oping countries. Prognoses indicate an increase in microelements, release of zinc ions (ZnII) from morbidity from year to year [Meetoo et al. 2007]. P. ostreatus to artificial gastric juice was determined, progress is associated with a number of using differential pulse anodic stripping voltammetry. complications, and leads to premature death. The amount of zinc in artificial saliva, stomach and Many are available on the market, including intestinal juices, ranged from 1.88 to 2.83 mg, 1.14– compounds derived from nature, e.g. the recently 8.33 mg and 0.41–1.59 mg per 100 g DW, respective- approved dapagliflozin, an inhibitor of sodium- ly. Fruiting bodies of P. ostreatus after thermal pro- glucose transport proteins (SGLT2), the structure of cessing imitating culinary preparation were extracted which is based on phlorizin. Diabetes leads to choles- in artificial saliva, stomach and intestinal juices, with terol and lipid disorders; therefore, patients are forced zinc contents recorded at: 0.41–4.95 mg, 0.78– to treat both ailments [Nesto 2008]. Pleurotus os- 2.65 mg and 2.18–2.23 mg per 100 g DW, respective- treatus has shown beneficial activity not only in ly [Muszyńska et al. 2016]. This microelement is regulating blood glucose levels, but also in regulating essential for synthesis, insulin homeostasis lipid metabolism. This direction of action is associat- and it acts as a cofactor of over 300 enzymes, includ- ed with the occurrence in this species of many types ing superoxide dismutase. Its beneficial effects in of compounds; however, one of the most significant

www.acta.media.pl 153 Piska, K., Sułkowska-Ziaja, K., Muszyńska, B. (2017). Edible mushroom Pleurotus ostreatus (Oyster mushroom) – its dietary significance and biological activity. Acta Sci. Pol. Hortorum Cultus, 16(1), 151–161.

chemicals found is lovastatin, a drug approved in catalyzing reduction of 3-hydroxy-3-methylgluta- 1987 by the US Food and Drug Agency (FDA) and ryl-CoA to mavalonate, which is the first step in the widely used in current of dyslipidemia. It acts endogenous synthesis of cholesterol. Inhibition of as an inhibitor of HMG-CoA reductase an enzyme

Table 1. Levels of phenolic compounds in P. ostreatus mycelium

Levels of phenolic compounds among various studies Phenolic compound Woldegiorgis Muszyńska Kim Palacios Gąsecka Alam et al. [2014]b et al. [2013]a et al. [2008]b et al. [2011]b et al. [2015]b et al. [2010]b p-hydroxybenzoic 1.25 3.60 – 4.69 5.30 – acid Synapic acid – 2.11 – – – – Cinnamic acid* – 1.09 – – – – Ferulic acid – 0.46 – 20.16 30.00 – p-coumaric acid – – – 11.15 10.54 – Protocatechic acid – 2.52 18.0 19.32 0.21 81.0 Vanillic acid – – – – 0.34 – Caffeic acid 7.80 – – – 0.35 – Gallic acid 13.00 – 7.0 290.34 – 36.0 Homogentisic acid – – 16.0 629.86 – – Chlorogenic acid – – 19.0 – 27.0 Genstisic acid – – – 292.62 – – Myricetin 1.67 – 21.0 21.99 – – Naringenin – – 9.0 – 0.18 10.0 Hesperidin – – – – – 10.0 Formononetin – – – – – 14.0 Biochanin A – – – – – 10.0 a – mg/kg DW, b– μg/g DW; * precursor of selected phenolic compounds

this process leads to a decrease in cholesterol levels this hypolypidemic effect in P. ostreatus is also asso- in the liver, and an increase in the expression of low- ciated with the presence of other compounds, e.g. density lipoproteins receptors on hepatocyte cell chrisin, or β-glucans [Anandhi et al. 2013, Caz et al. membranes and finally to an increased uptake of 2015]. Another aspect of P. ostreatus activity is its LDL and VLVD from the blood [Bobek et al. 1995]. antioxidant action – this mushroom beneficial effects Beyond their specific mechanism of action, statins in preventing progression of diabetes associated with exhibited pleiotropic activities, including stabilization oxidative stress [Kaneto et al. 2010]. of artherosclerotic plaque, as well as anti-inflamma- Hypoglycemic activity of P. ostreatus. The hy- tory, anticoagulation, immunomodulatory, and prolif- poglycemic activity of P. osteratus has been indicat- eration inhibiting properties with regard to the muscle ed in alloxan-induced diabetic mice. Ethanolic extract of the left ventricle [Kavalipati et al. 2015]. However, decreased serum glucose levels, improved serum

154 www.acta.media.pl Piska, K., Sułkowska-Ziaja, K., Muszyńska, B. (2017). Edible mushroom Pleurotus ostreatus (Oyster mushroom) – its dietary significance and biological activity. Acta Sci. Pol. Hortorum Cultus, 16(1), 151–161.

lipid profiles and kidney function [Ravi et al. 2013]. [Bobek et al. 1998, Alam et al. 2009]. In studies In the same model of diabetes hypoglycemic activity comparing the hypolipidemic effect of three Pleuro- was shown in rats fed with 500 mg kg-1 BW of pul- tus species (P. ostreatus, P. sajorcaju, and verized mushroom. The efficacy of P. ostreatus was P. florida), P. ostreatus showed the greatest influ- comparable with that of metformin or glibenclamide ence on the reduction of blood cholesterol and tri- [Jayasuriya et al. 2012]. Pleurotus ostreatus also glyceride levels, while in terms of decreasing showed hypoglycemic, hypolipidemic and hypocho- LDL/HDL ratios, P. sajor-caju was shown to be lesterolemic activity in streptozotocin-induced diabe- more effective [Alam et al. 2009]. tes in rats [Chorváthová et al. 1993]. Hypoglycemic An eight-week study with 20 patients treated with efficacy has also been studied in human subjects. an antiretroviral therapy, which results in dyslipidem- In 27 patients with diabetes and hypertension, ia as an adverse drug reaction, showed a positive 3-month supplementation of their diet with 3 grams effect of P. ostreatus on lipid profiles only in 3 sub- of pulverized mushroom lead to a decrease in diastol- jects [Abrams et al. 2011]. However, Slovak re- ic and systolic blood tension, fasting glucose level searchers indicated a significant effect from six-week and glycated hemoglobin (HbAc1) [Choudhury et al. supplementation with pulverized P. ostreatus on 2013]. Pulverized P. ostreatus administered to a decrease in triglyceride and cholesterol levels in 22 healthy persons decreased fasting glucose levels dyslipidemic patients, without any influence on HDL after oral administration of glucose solution. A simi- [Kajaba et al. 2008]. A study including 30 diabetics lar effect was observed in 14 diabetic patients, with showed the influence of a diet containing mushrooms an additional increase in insulin level. No changes in on a decrease in glucose, triglyceride and cholesterol aminotransferase activity or creatinine levels were levels, combined with an additional blood pressure observed, indicating a lack of hepato- or nephrotoxic reducing effect. No adverse effects to the liver or effects [Jayasuriya et al. 2015]. The hypoglycemic kidneys were recorded [Khatun et al. 2007]. activity of P. ostreatus seems to be a complex pro- The mechanism of hypolipidemic activity of the cess including many mechanisms. Jayasuriya et al. species probably also includes many pathways. One [2015] showed a potential for decreasing glycemia possible mechanism is the decrease in lipid absorp- using P. ostreatus through the activation of glucoki- tion from the gastrointestinal tract and their increased nase, stimulation of insulin burst and inhibition of elimination with feces [Bobek et al., 1996 Alam et al. glycogen synthase kinase, resulting in increased gly- 2009]. Another mechanism is connected with the cogen synthesis [Jayasuriya et al. 2015]. inhibition of HMG-CoA reductase by lovastatin Hypolipidemic activity. This mode of action of [Bobek et al. 1995]. More recent studies have also P. ostreatus has been studied in in vitro models in shown an influence on the expression of genes asso- rodents, as well as human subjects. In rats with Tri- ciated with lipid metabolism. Water extract standard- ton WR-1339-induced hypercholesterolemia, etha- ized for β-glucans affected expression of Dgat1 (di- nol extract at a daily dose of 500 mg kg-1 BW (body glyceride acyltransferase), which is responsible for weight) significantly decreased levels of VLDL, triglyceride synthesis. In mice fed with P. ostreatus, LDL, total cholesterol, aminotransferases, lactate an increase in the expression of genes associated with dehydrogenase and glucose, while increased HDL lipid transport and β-oxidation was observed [Sato et levels were observed. [Anandhi et al. 2013]. A diet al. 2011]. consisting of 10% of dried mushroom, and 1% cho- Antineoplastic activity. Among the medical lesterol in rabbits resulted in a 65% decrease in properties of mushrooms, anticancer activity is one of serum cholesterol levels and in some animals pre- the most attractive for researchers. Neoplasms pose vented the development of arteriosclerosis, com- a significant civilizational – related problem and also pared to the control group not supplemented with leading causes of death globally. Currently available P. ostreatus [Bobek and Galbavý 1999]. In similar drugs and therapy methods have not been sufficiently studies including rats, results were analogous efficacious to significantly decrease the scale of prob-

www.acta.media.pl 155 Piska, K., Sułkowska-Ziaja, K., Muszyńska, B. (2017). Edible mushroom Pleurotus ostreatus (Oyster mushroom) – its dietary significance and biological activity. Acta Sci. Pol. Hortorum Cultus, 16(1), 151–161.

lem; therefore, the search for novel anticancer agents a concentration range of 10–100 µg ml-1 showed is continuing [Siegel et al. 2015]. From fungi, nu- cytotoxicity against sarcoma 180 cells. Also, an in merous compounds of varied chemical structures vitro immunomodulatory effect was observed – pro- have been isolated and shown to possess desirable teoglycans increased proliferation of splenocytes and activities. Special significance is given to polysaccha- activated macrophages and NK cells [Sarangi et al. rides which are used in standard cancer treatments, 2006]. e.g. [Patel and Goyal 2012]. The anticancer A protein complex isolated from P. ostreatus in- activities of P. ostreatus extracts and isolated com- duced apoptosis in a SW480 cell line, probably pounds have been studied in cancer cell lines and in through induction of oxidative stress, decrease in rodents. intracellular glutathione and a reduced mitochondrial Water extract from pulverized P. ostreatus showed transmembrane potential [Wu et al. 2011]. A protein cytotoxicity against colon cancer cell lines COLO-205, complex obtained by another method at a dose of 5 -1 with an IC50 of 81.2 µg ml . The extract decreased and 10 mg per kg BW reduced growth of tumors in cells ability to form colonies and alters cell migra- Dalton lymphoma bearing mice by 35.68 and tion. Moreover, induction of apoptosis is observed in 51.43%, respectively. The above doses also pro- treated cells. Increased expression of Bax, caspases 3 longed survival time of Dalton lymphoma, Sarcoma- and 9, and decreased Bcl-2 mRNA was recorded, and 180 and B16F0 melanoma bearing mice. Induction of cell cycle arrest in G0/G1 was demonstrated [Arora apoptosis was observed in cancer cells [Maiti et al. and Tandon 2015]. Intracellular and extracellular 2011]. Another isolated antineoplastic compound was polysaccharide fractions from P. ostreatus cultivated dimeric lectin, with subunit weights of 40 and in conditions of submerged fermentation, inhibited 41 kDa. Lectin prolonged survival time of mice bear- proliferation of HCT15, HCT116, RL 95, and SW480 ing sarcoma S-180 and hepatoma H-22 and reduced cell lines [Silva et al. 2012]. Pleurotus ostreatus glu- tumor growth [Wanga et al. 2000 a]. can at a dose of 10 mg and 20 mg per kg BW de- The results of studies have shown the anticancer creased Sarcoma 180 tumor weight by 37.30 and potential of P. ostreatus. This species contains vari- 51.89%, respectively. No cytotoxic effect has been ous compounds with such modes of action; however, observed in vitro; however, increased proliferation of especially important is the presence of polysaccha- lymphocytes has been shown, which may suggest rides, including glucans, and proteins with cytotoxic immunomodulatory properties as a possible anti- properties. Divergent results in terms of the cytotoxic tumor mechanism [Devi et al. 2013]. Devi et al. activity of glucans in vitro suggest a different mecha- [2015] also showed a lack of direct cytotoxic activity nism of action of P. ostreatus glucans. Some may act of glucan against Dalton lymphoma cells. Glucan by direct cytotoxicity against cancer cells, while oth- exhibited immunomodulating activity via an increase ers may act by immunomodulatory properties, or by in lymphocytes proliferation and macrophages activa- a combination of both mechanisms. tion. Also, induction of the cytotoxicity of NK cells Antioxidative properties. A significant role in and macrophages against cancer cells was shown. the pathogenesis of diabetes and its complications, After administration of glucan to Dalton lymphoma arteriosclerosis, carcinogenesis, neurodegeneration bearing mice at a dose of 20 mg kg-1 BW, inhibition diseases and numerous other diseases, is played by of tumor growth was more than 70%. Moreover, oxidative stress induced by reactive oxygen species rodents’ survival period increased. An isolated poly- (ROS). Therefore, antioxidants are considered as saccharide POMP2 of 29 kDa molecular weight in- compounds preventing disease development, but also hibited proliferation and migration and decreased with potential application in treatment [Hajhashemi formation of colonies in BGC-823 cell lines, while in et al. 2010]. Extracts from P. ostreatus showed direct rodents it significantly decreases the volume and antioxidant properties comparable with BHA and weight of tumors [Cao et al. 2015]. Sarangi et al. vitamin C, in DPPH, ABTS, FRAP, and β-carotene isolated three fractions of proteoglycans, which at bleaching assays [Yim et al. 2010, Arbaayah and

156 www.acta.media.pl Piska, K., Sułkowska-Ziaja, K., Muszyńska, B. (2017). Edible mushroom Pleurotus ostreatus (Oyster mushroom) – its dietary significance and biological activity. Acta Sci. Pol. Hortorum Cultus, 16(1), 151–161.

Kalsom 2013, Chowdhury et al. 2015]. Elbatrawy et Antimicrobial activity. Water and alcoholic ex- al. [2015] examined antioxidant properties of seven tracts from P. ostreatus mycelium have been used in extracts obtained with seven different solvents. studies on antimicrobial activities against numerous In DPPH assays, the most potent was the water ex- types of microbes. The highest potency was shown tract. This mode of action of P. ostreatus may be by water extract, especially towards fungi: Candida related to the content of phenolic acids, flavonoids, albicans, Cryptococcus humicola, Trichosporon cu- vitamins C and E and polysaccharides [Yim et al. taneum; and bacteria: Staphylococcus aureus and 2010, Muszyńska et al. 2013]. However, the species Escherichia coli. In the extract the active substance not only has the capacity for direct interaction with was identified as 3-(2-aminophenyl-1-thio)-3-hydro- ROS, but can also increase the activity of antioxidant xypropanoic acid, with MIC 30 µg mL-1 and enzymes in tissues. In rats treated with ethanolic 20 µg mL-1, against fungi and bacteria, respectively extract of P. ostreatus an increase in CAT (catalase) [Younis et al. 2015]. Methanolic extract from gene expression was observed in the liver and kid- P. ostreatus mycelium showed activity against gram neys with a simultaneous decrease in protein car- positive and negative bacteria with MIC in the range bonylation in these organs [Jayakumar et al. 2010]. of 4–8 µg mL-1 [Chowdhury et al. 2015]. Ethanolic Ethanol extract in diabetic rats increased the activity extract inhibited growth of Pseudomonas aeruginosa, of catalase, superoxide dismutase (SOD), and gluta- Salmonella typhi, Staphylococcus aureus, Bacillus thione peroxidase (GPx). It also increased the levels subtilis, Bacillus atropaeus, Klebsiella pneumoniae, of vitamins C and E in the liver and decreased the and at the highest potency level: Candida albicans levels of malonyldialdehyde (MDA) [Tahrani and and Agrobacterium tumifaciens [Ahmad et al. 2014]. Barnett 2010]. Antioxidative and protective effects Additionally, ergosterole peroxide was found in the were also observed against toxicity induced by para- species and it acted in a toxic manner against Trypan- cetamol (acetaminophen) and carbon tetrachloride somona cruzi as well as showed an amoebicidal ef- [Jayakumar et al. 2006, 2008, Naguib et al. 2014]. fect [Ramos-Ligonio et al. 2012, Meza-Menchaca et Antiviral activity. There are individual reports al. 2015]. The above studies clearly showed the anti- concerning the antiviral properties of P. ostreatus. microbial activity of P. ostreatus; however, due to Wanga and Ng [2000 b] found a protein of 12.5 kDa the high concentration required to achieve it this which inhibited translation in a rabbit reticulocyte effect seems to be insignificant in comparison to lysate system and exhibited low ribonuclease activity other activities of the mushroom. toward yeast tRNA. It also inhibited reverse transcrip- Pleurotus ostreatus as a potential source of ac- tase of the HIV-1 virus. Laccase (58 kDa) inhibited tive substances in cosmetology. The fruiting bodies entry of the hepatitis C virus into peripheral blood are a good source of previously described antioxidant cells and hepatoma cells. The enzyme also had the and antiageing substances such as ergothioneine, ability to inhibit intracellular replication of a virus in phenolic compounds, and the indole compounds: HepG2 cell lines at concentration of 0.75–1.5 mg ml-1 melatonin, serotonin, and selenium [Kim et al. 2008, [El-Fakharany et al. 2010]. Water extract of Muszyńska et al. 2011, Mohamed and Farghaly 2014, P. ostreatus exhibited antiviral activity against influ- Woldegiorgis et al. 2014]. The selenium content was enza A virus and herpes simplex virus 2 in cell lines determined to be 58.24 mg kg-1 and 100.31 mg kg-1 infected by the above viruses [Krupodorova et al. in fresh and dried mushroom, respectively [Mohamed 2014]. Water and methanolic extracts as well as poly- and Farghaly 2014]. Moreover, fifty five aroma com- saccharide fractions were assayed against HSV-1. pounds were demonstrated in mycelium, including The highest potency was shown by a polysaccharide 27 esters, 9 ketones, 7 thiols, 5 alcohols, 4 terpe- -1 fraction with IC50 = 4.80 µg mL . Acyclovir was noids, 2 phenols and 1 aldehyde [Mohamed and Far- used as a reference agent, and this showed IC50 = ghaly 2014]. Aroma compounds play a significant 0.20 µg mL-1 [Santoyo et al. 2012]. role in the perfume industry and in the production of cosmetics. A cream based on β-glucans, and also

www.acta.media.pl 157 Piska, K., Sułkowska-Ziaja, K., Muszyńska, B. (2017). Edible mushroom Pleurotus ostreatus (Oyster mushroom) – its dietary significance and biological activity. Acta Sci. Pol. Hortorum Cultus, 16(1), 151–161.

containing pleuran, showed a significant positive tioxidative effects of an extract of the oyster mush- effect in supportive therapy for atopic dermatitis in room, Pleurotus ostreatus, and its major constituent, a study including 105 patients, of which 80 complet- chrysin, in Triton WR-1339-induced hypercholester- ed the trial [Jesenak et al. 2015]. olemic rats. J. Physiol. Biochem., 69, 313–323. Arbaayah, H.H., Kalsom, Y.U. (2013). Antioxidant proper- ties in the oyster mushrooms (Pleurotus spp.) and split CONCLUSIONS gill mushroom (Schizophyllum commune) ethanolic ex- tracts. Mycosphere, 4, 661–673. Pleurotus ostreatus is a widely distributed and Arora, S., Tandon, S. (2015). Mushroom extracts induce cultivated mushroom with medical significance. human colon cancer cell (COLO-205) death by trig- It has a broad spectrum of biological activities and gering the mitochondrial apoptosis pathway and potential in the prevention and treatment of diseases. Go/G1-Phase cell cycle arrest. Arch. Iran. Med., 18, Due to the high contents of mineral salts and organic 284–295. compounds essential for humans, it is of great dietary Barros, L., Baptista, P., Correia, D.M., Casal, S., Oliveira, importance. Its activity is especially confirmed in B., Ferreira, I.C.F.R. (2007). Fatty acid and sugar com- decreasing blood sugar levels and in improving lipid positions, and nutritional value of five wild edible profiles. Additionally, it has antiatherogenic, antioxi- mushrooms from Northeast . Food Chem., 105, dant and antineoplastic properties. Detection of 140–145. lovastatin and pleuran in fruiting bodies has partially Beltran-Garcia, M.J., Estarron-Espinosa, M., Ogura T. explained its activities and has made this species (1997). Volatile compounds secreted by the oyster a significant mushroom of medical and nutritional mushroom (Pleurotus ostreatus) and their antibacterial value. activities. J. Agric. Food Chem., 45, 4049–4052. Bobek, P., Galbavý, S. (1999). Hypocholesterolemic and antiatherogenic effect of oyster mushroom (Pleurotus REFERENCES ostreatus) in rabbits. Nahrung, 43, 339–342. Bobek, P., Hromadová, M., Ozdín, L. (1995). Oyster Abrams, D.I., Couey, P., Shade, S.B., Kelly, M.E, mushroom (Pleurotus ostreatus) reduces the activity of Kamanu-Elias, N., Stamets, P. (2011). Antihyper- 3-hydroxy-3-methylglutaryl CoA reductase in rat liver lipidemic effects of Pleurotus ostreatus (oyster mush- microsomes. Experientia, 51, 589–591. rooms) in HIV-infected individuals taking antiretroviral Bobek, P., Ozdín, L., Galbavý, S. (1998). Dose- and time- therapy. BMC Complement. Altern. Med., 11, 60. dependent hypocholesterolemic effect of oyster mush- Ahmad, N., Mahmood, F., Khalil, S.A., Zamir, R., Fazal, room (Pleurotus ostreatus) in rats. , 14, 282– H., Abbasi, B.H. (2014). Antioxidant activity via 286. DPPH, gram-positive and gram-negative antimicrobial Bobek, P., Ozdín, L., Kuniak, L. (1996). Effect of oyster potential in edible mushrooms. Toxic. Ind. Health., 30, mushroom (Pleurotus ostreatus) and its ethanolic ex- 826–834. tract in diet on absorption and turnover of cholesterol in Alam, N., Amin, R., Khan, A., Ara, I., Shim, M.J., Lee, hypercholesterolemic rat. Nahrung, 40, 222–224. M.W., Lee, U.Y., Lee, T.S. (2009). Comparative ef- Cao, X.Y., Liu, J.L., Yang, W., Hou, X., Li, Q.J. (2015). fects of oyster mushrooms on lipid profile, liver and Antitumor activity of polysaccharide extracted from kidney function in hypercholesterolemic rats. Mycobi- Pleurotus ostreatus mycelia against gastric cancer in ology, 37, 37–42. vitro and in vivo. Mol. Med. Rep., 12, 2383–2389. Alam, N., Yoon, K.N., Lee, K.R., Shin, P.G., Cheong, J.C., Caz, V., Gil-Ramírez, A., Largo, C., Tabernero, M., San- Yoo, Y.B., Shim, J.M., Lee, M.W., Lee, U.Y., Lee, tamaría, M., Martín-Hernández, R., Marín, F.R., Reg- T.S. (2010). Antioxidant activities and tyrosinase inhib- lero, G., Soler-Rivas, C. (2015). Modulation of choles- itory effects of different extracts from Pleurotus os- terol-related gene expression by dietary fiber fractions treatus fruiting bodies. Mycobiology, 38, 295–301. from edible mushrooms. J. Agric. Food. Chem., 63, Anandhi, R., Annadurai, T., Anitha, T.S., Muralidharan, 7371–7380. A.R., Najmunnisha, K., Nachiappan, V., Thomas, P.A., Geraldine, P. (2013). Antihypercholesterolemic and an-

158 www.acta.media.pl Piska, K., Sułkowska-Ziaja, K., Muszyńska, B. (2017). Edible mushroom Pleurotus ostreatus (Oyster mushroom) – its dietary significance and biological activity. Acta Sci. Pol. Hortorum Cultus, 16(1), 151–161.

Cheah, I.K., Halliwell, B. (2012). Ergothioneine; antioxi- methylglutaryl-coenzyme a reductase-lovastatin. Exp. dant potential, physiological function and role in dis- Mycol., 19, 1–6. ease. Biochim. Biophys. Acta. Mol. Basis Dis., 1822, Hajhashemi, V., Vaseghi, G., Pourfarzam, M., Abdollahi, 784–793. A. (2010). Are antioxidants helpful for disease preven- Chorváthová, V., Bobek, P., Ginter, E., Klvanová, J. tion? Res. Pharm. Sci., 5, 1–8. (1993). Effect of the oyster on glycaemia and Jayakumar, T., Sakthivel, M., Thomas, P.A., Geraldine, P. cholesterolaemia in rats with insulin-dependent diabe- (2006). Antioxidant activity of the oyster mushroom tes. Physiol. Res., 42, 175–179. Pleurotus ostreatus, on CCl(4)-induced liver injury in Choudhury, M.B.K., Rahman, T., Kakon, A.J., Hoque, N., rats. Food Chem. Toxic., 44, 1989–1996. Akhtaruzzaman, M., Begum, M.M., Choudhuri, Jayakumar, T., Thomas, P.A., Isai, M., Geraldine, P. M.S.K., Hossain, M.S. (2013). Effects of Pleurotus os- (2008). Pleurotus ostreatus, an oyster mushroom, de- treatus on blood pressure and glycemic status of hyper- creases the oxidative stress induced by carbon tetra- tensive diabetic male volunteers Bangladesh. J. Med. chloride in rat kidneys, heart and brain. Chem. Biol. In- Biochem., 6, 5–10. teract., 176, 108–120. Chowdhury, M.M.H., Kubra, K., Ahmed, S.R. (2015). Jayakumar, T., Thomas, P.A., Isai, M., Geraldine, P. Screening of antimicrobial, antioxidant properties and (2010). An extract of the oyster mushroom, Pleurotus bioactive compounds of some edible mushrooms culti- ostreatus, increases catalase gene expression and re- vated in Bangladesh. Ann. Clin. Microbiol. Antimi- duces protein oxidation during aging in rats. Chin. crob., 14, 8–13. J. Integr. Med., 8, 774–780. Devi, K.S., Behera, B., Mishra, D., Maiti, T.K. (2015). Jayasuriya, W.J., Suresh, T.S., Abeytunga, D., Fernando, Immune augmentation and Dalton’s Lymphoma tumor G.H., Wanigatunga, C.A. (2012). Oral hypoglycemic inhibition by glucans/glycans isolated from the mycelia activity of culinary-medicinal mushrooms Pleurotus and fruit body of Pleurotus ostreatus. Int. Im- ostreatus and P. cystidiosus (higher basidiomycetes) in munopharmacol., 25, 207–217. normal and alloxan-induced diabetic Wistar rats. Int. Devi, K.S., Roy, B., Patra, P., Sahoo, B., Islam, S.S., Maiti, J. Med. Mushrooms, 14, 347–355. T.K. (2013). Characterization and lectin microarray of Jayasuriya, W.J., Wanigatunge, C.A., Fernando, G.H., an immunomodulatory heteroglucan from Pleurotus os- Abeytunga, D.T., Suresh, T.S. (2015). Hypoglycaemic treatus mycelia. Carbohydr. Polym., 94, 857–865. activity of culinary Pleurotus ostreatus and P. cystidio- Elbatrawy, E.N., Ghonimy, E.A., Alassar, M.M., Wu, F.S. sus mushrooms in healthy volunteers and type 2 diabet- (2015). Medicinal mushroom extracts possess differen- ic patients on diet control and the possible mechanisms tial antioxidant activity and cytotoxicity to cancer cells. of action. Phytother. Res., 29, 303–309. Int. J. Med. Mushrooms, 17, 471–479. Jesenak, M., Urbancek, S., Majtan, J., Banovcin, P., El-Fakharany, E.M., Haroun, B.M., Ng, T.B., Redwan, Hercogova, J. (2015). β-Glucan-based cream (contain- E.R. (2010). Oyster mushroom laccase inhibits hepati- ing pleuran isolated from Pleurotus ostreatus) in sup- tis C virus entry into peripheral blood cells and hepa- portive treatment of mild-to-moderate atopic dermati- toma cells. Prot. Pept. Lett., 17, 1031–1039. tis. J. Derm. Treat., 10,1–4. Fričová, O., Koval’aková, M. (2013). Solid-State 13C CP Kajaba, I., Simoncic, R., Frecerova, K., Belay, G. (2008). MAS NMR spectroscopy as a tool for detection of Clinical studies on the hypolipidemic and antioxidant (1→3, 1→6)-β-D-Glucan in products prepared from effects of selected natural substances. Bratisl. Lek Li- Pleurotus ostreatus. ISRN Anal. Chem., vol. 2013, Ar- sty, 109, 267–272. tic. ID 248164, 4 p. Kaneto, H., Katakami, N., Matsuhisa, M., Matsuoka, T. Gąsecka, M., Mleczek, M., Siwulski, M., Niedzielski, P. (2010). Role of reactive oxygen species in the progres- (2015). Phenolic composition and antioxidant proper- sion of type 2 diabetes and atherosclerosis. Mediat. In- ties of Pleurotus ostreatus and en- flamm., ID 453892, doi: 10.1155/2010/453892. riched with selenium and zinc. Eur. Food Res. Tech- Karácsonyi, Š., Kuniakb, Ľ. (1994). Polysaccharides of nol., 226, 737–743. Gunde-Cimerman, N., Cimerman, A. (1995). Pleurotus Pleurotus ostreatus: Isolation and structure of pleuran, fruiting bodies contain the inhibitor of 3-hydroxy-3- an alkali-insoluble β-d-glucan. Carbohydr. Polym., 24, 107–111.

www.acta.media.pl 159 Piska, K., Sułkowska-Ziaja, K., Muszyńska, B. (2017). Edible mushroom Pleurotus ostreatus (Oyster mushroom) – its dietary significance and biological activity. Acta Sci. Pol. Hortorum Cultus, 16(1), 151–161.

Kavalipati, N., Shah, J., Ramakrishan, A., Vasnawala, H. Muszyńska, B., Sułkowska-Ziaja, K., Ekiert, H. (2013). (2015). Pleiotropic effects of statins. Indian J. Endo- Phenolic acids in selected edible basidio-mycota species: crinol. Metab., 19, 554–562. Armillaria mellea, Boletus badius, , Can- Khatun, K., Mahtab, H., Khanam, P.A., Sayeed, M.A., tharellus cibarius, deliciosus and Pleurotus os- Khan, K.A. (2007). Oyster mushroom reduced blood treatus. Acta Sci. Pol. Hortorum Cultus, 12, 107–116. glucose and cholesterol in diabetic subjects. Mymens. Naguib, Y.M., Azmy, R.M., Samaka, R.M., Salem, M.F. Med. J., 16, 94–99. (2014). Pleurotus ostreatus opposes mitochondrial dys- Kholoud, M.A., Nahla, A.B., Nadia, S., Al., K. (2014). function and oxidative stress in acetaminophen-induced Cultivation of oyster mushroom Plerotus ostreatus on hepato-renal injury. BMC Complement. Altern. Med., date-palm leaves mixed with other agro-wastes in Sau- 14, 494. di Arabia. Saudi J. Biol. Sci., 21, 616–625. Nesto, R.W. (2008). LDL cholesterol lowering in type 2 Kim, M.Y., Seguin, P., Ahn, J.K., Kim, J.J., Chun, S.C., diabetes: What is the optimum approach? Clin. Diab., Kim, E.H., Seo, S.H., Kang, E.Y., Kim, S.L., Park, 26, 8–13. Y.J., Ro, H.M., Chung, I.M. (2008). Phenolic com- Noormagi, A., Gavrilova, J., Smirnova, J., Tougu, V., pound concentration and antioxidant activities of edible Palumaa, P. (2010). Zn(II) ions co-secreted with insulin and medicinal mushrooms from Korea. J. Agric. Food suppress inherent amyloidogenic properties of mono- Chem., 56, 7265–7270. meric insulin. Biochem. J., 430, 511–518. Krupodorova, T., Rybalko S., Barshteyn, V. (2014). Anti- Palacios, I., Lozano, M., Moro, C., D’Arrigo, M., Rostag- viral activity of Basidiomycete mycelia against influ- no, M.A., Martínez, J.A., García-Lafuente, A., Guil- enza type A (serotype H1N1) and herpes simplex virus lamón, E., Villares, A. (2011). Antioxidant properties type 2 in cell culture. Virol Sin., 29, 284–290. of phenolic compounds occurring in edible mushrooms Maiti, S., Mallick, S.K., Bhutia, S.K., Behera, B., Mandal, Food Chem., 128, 674–678. M., Maiti, T.K. (2011). Antitumor effect of culinary- Patel, S., Goyal, A. (2012). Recent developments in mush- medicinal oyster mushroom, Pleurotus ostreatus (Jacq.: rooms as anti-cancer therapeutics: a review. Biotech, 2, Fr.) P. Kumm., derived protein fraction on tumor- 1–15. bearing mice models. Int. J. Med. Mushrooms, 13, Powell, S.R. (2000). The antioxidant properties of zinc. 427–440. J. Nutr., 130, 1447–1454. Meetoo, D., McGovern, P., Safadi, R. (2007). An epidemi- Ramos-Ligonio, A., López-Monteon, A., Trigos, A. ological overview of diabetes across the world. Br. (2012). Trypanocidal activity of peroxide J. Nurs., 16, 1002–1007. from Pleurotus ostreatus. Phytother. Res., 26, 938– Meza-Menchaca, T., Suárez-Medellín, J., Del Ángel-Piña, 943. C., Trigos, Á. (2015). The amoebicidal effect of ergos- Ravi, B., Renitta, R.E., Prabha, M.L., Issac, R., Naidu, S. terol peroxide isolated from Pleurotus ostreatus. Phy- (2013). Evaluation of antidiabetic potential of oyster tother. Res., 29, 1982–1986. mushroom (Pleurotus ostreatus) in alloxan-induced dia- Mohamed, E.M., Farghaly, F.A. (2014). Bioactive com- betic mice. Immunopharm. Immunotoxic., 35, 101–109. pounds of fresh and dried Pleurotus ostreatus mush- Sanches, C. (2010). Cultivation of Pleurotus ostreatus and room. Int. J. Biotech. Well. Indus., 3, 4–14. other edible mushrooms. Appl. Microbial. Biotechnol.,

Muszyńska, B., Komendacki, P., Kała, K., Opoka, W. 85, 1321–13377. (2014). L-Tryptophan and its derivatives in edible Santoyo, S., Ramírez-Anguiano, A.C., Aldars-García, L., mushrooms species. Med. Inter. Rev., 103, 82–86. Reglero, G., Soler-Rivas, C. (2012). Antiviral activities Muszyńska, B., Zając, M., Kała, K., Opoka, W., Rojowski, of Boletus edulis, Pleurotus ostreatus and Lentinus J. (2016). Thermal processing can affect zinc availabil- edodes extracts and polysaccharide fractions against ity in some edible mushrooms. LWT – Food Sci. Tech- Herpes simplex virus type 1. J. Food Nutr. Res., 51, nol., 69, 424–429. 225–235. Muszyńska, B., Sułkowska-Ziaja, K., Ekiert, H. (2011). Sarangi, I., Ghosh, D., Bhutia, S.K., Mallick, S.K., Maiti, Indole compounds in some culinary – medicinal higher T.K. (2006). Anti-tumor and immunomodulating ef- basidiomycetes from Poland. Int. J. Med. Mushrooms, fects of Pleurotus ostreatus mycelia-derived proteogly- 13, 449–454. cans. Int. Immunopharm., 6, 1287–1297.

160 www.acta.media.pl Piska, K., Sułkowska-Ziaja, K., Muszyńska, B. (2017). Edible mushroom Pleurotus ostreatus (Oyster mushroom) – its dietary significance and biological activity. Acta Sci. Pol. Hortorum Cultus, 16(1), 151–161.

Sato, M., Tokuji, Y., Yoneyama, S., Fujii-Akiyama, K., Wanga, H.X., Ng, T.B. (2000 b). Isolation of a novel ubiq- Kinoshita, M., Ohnishi, M. (2011). Profiling of hepatic uitin-like protein from Pleurotus ostreatus mushroom gene expression of mice fed with edible japanese with anti-human immunodeficiency virus, translation- mushrooms by DNA microarray analysis: comparison inhibitory, and ribonuclease activities. Biochem. Bio- among Pleurotus ostreatus, , and Hyp- phys. Res. Comm., 276, 587–593. sizigus marmoreus. J. Agric. Food Chem., 59, 10723– Wojewoda, W. (2003). Checklist of Polish Larger Basidi- 10731. omycetes. W. Szafer Institute of Botany, Polish Acad. Shin-Yu, C., Kung-Jui, H., Yun-Jung, H., Li-Ting, W., of Sci. Kraków. Jeng-Leun, M. (2012). Contents of lovastatin, Woldegiorgis, A.Z., Abate, D., Haki, G.D., Ziegler, G.R. g-aminobutyric acid and ergothioneine in mushroom (2014). Antioxidant property of edible mushrooms col- fruiting bodies and mycelia. Food Sci. Technol-Leb., lected from Ethiopia. Food Chem., 157, 30–36. 47, 274–278. Wu, J.Y., Chen, C.H., Chang, W.H., Chung, K.T., Liu, Siegel, R.L., Miller, K.D., Jemal, A. (2015). Cancer statis- Y.W., Lu, F.J. Chen, C.H. (2011). Anti-cancer effects tics, 2015. CA Can. J. Clin., 65, 5–29. of protein extracts from Calvatia lilacina, Pleurotus os- Silva, S., Martins, S., Karmali, A., Rosa, E. (2012). Pro- treatus and volvacea. Evid. Based Compl. duction, purification and characterisation of polysac- Alternat. Med., ID 982368, 10 p. charides from Pleurotus ostreatus with antitumour ac- Yim, H.S., Chye, F.Y., Tan, C.T., Ng, Y.C., Ho, C.W. tivity. J. Sci. Food Agric., 92, 1826–1832. (2010). Antioxidant activities and total phenolic con- Tahrani, A.A., Barnett, A.H. (2010). Dapagliflozin: a sodi- tent of aqueous extract of Pleurotus ostreatus (cultivat- um glucose cotransporter 2 inhibitor in development ed oyster mushroom). Mal. J. Nutr., 16, 281–291. for type 2 diabetes. Diab. Ther., 1, 45–56. Younis, A.M., Wu, F.S., El Shikh, H.H., (2015). Antimi- Wanga, H., Gaoa, J., Ng, T.B. (2000 a). A new lectin with crobial activity of extracts of the oyster culinary medic- highly potent antihepatoma and antisarcoma activities inal mushroom Pleurotus ostreatus (higher basidiomy- from the oyster mushroom Pleurotus ostreatus. Bio- cetes) and identification of a new antimicrobial com- chem. Biophys. Res. Comm., 276, 587–593. pound. Int. J. Med. Mushrooms, 17, 579–590.

www.acta.media.pl 161