Skip to main content

Advertisement

SpringerLink
Log in

Screening of mushrooms bioactivity: piceatannol was identified as a bioactive ingredient in the order Cantharellales

  • Original Paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

Abstract

Wild edible mushroom species are appreciated for consumption due to their high nutritional value. The aim of the present study was to examine in vitro beneficial bioactivity of mushroom extracts and to investigate the molecular identity of the active ingredients. In this regard, methanol extracts of 29 different wild edible mushroom species, that are traditionally consumed by residents in the National Park of North Pindos in North-Western Greece, were examined for antioxidant, antiproliferative, cytotoxic, and pro-apoptotic activities towards a human lung adenocarcinoma cell line A549 by the MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) assay and by flow cytometry. Certain mushroom species exhibited high antioxidant activity, which was related to their high content in total phenols and flavonoids. Methanol extracts of Cantharellus cibarius, Cantharellus cinereus, Craterellus cornucopioides and Hydnum repandum, which belong to the order Cantharellales, exhibited high cytotoxicity and induced apoptosis–necrosis to A549 cells. High Performance Liquid Chromatography (HPLC) coupled with Mass Spectrometry analysis revealed as an active ingredient piceatannol ((E)-4-[2-(3,5-dihydroxyphenyl)ethenyl]1,2-benzenediol-3,3′,4,5′-tetrahydroxy-trans-stilbene). Piceatannol, according to our best knowledge, is identified for the first time in wild edible mushrooms. Experiments with authentic piceatannol confirmed the potent antiproliferative activity of this compound. Tested mushrooms are promising sources of bioactive compounds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Wasser SP (2002) Medicinal mushrooms as a source of antitumor and immunomodulating polysaccharides. Appl Microb Biotec 60:258–274

    Article  CAS  Google Scholar 

  2. Zervakis G, Dimou D, Polemis Ε (2004) Fungal diversity and conservation in the Mediterranean area: recent advances in the inventory of Greek macromycetes. Mycol Balc 1:31–34

    Google Scholar 

  3. Barros L, Baptista P, Correia DM, Morais JS, Ferreira ICFR. (2007) Effects of conservation treatment and cooking on the chemical composition and antioxidant activity of Portuguese wild edible mushrooms. J Agric Food Chem 55:4781–4788

    Article  CAS  Google Scholar 

  4. Cheung PCK (2008) Nutritional value and health benefits of mushrooms. In: Mushrooms as functional foods, John Wiley and Sons, Inc., Hoboken, pp 71–109

    Chapter  Google Scholar 

  5. Mattila P, Konko K, Eurola M, Pihlava J-M, Astola J, Vahteristo L, Hietaniemi V, Kumpulainen J, Valtonen M, Piironen V (2001) Contents of vitamins, mineral elements, and some phenolic compounds in cultivated mushrooms. J Agric Food Chem 49:2343–2348

    Article  CAS  Google Scholar 

  6. Cheung LM, Cheung PCK, Ooi VEC (2003) Antioxidant activity and total phenolic of edible mushroom extracts. Food Chem 81:249–255

    Article  CAS  Google Scholar 

  7. Mau J, Huang P, Huang S, Chen C (2004) Antioxidant properties of methanolic extracts from Grifola frondosa, Morchella esculenta and Termitomyces albuminosus mycelia. Food Chem 87:111–118

    Article  CAS  Google Scholar 

  8. Barros L, Falcao S, Baptista P, Freire C, Vilas-Boas M, Ferreira ICFR. (2008) Antioxidant activity of Agaricus sp. mushrooms by chemical, biochemical and electrochemical assays. Food Chem 111:61–66

    Article  CAS  Google Scholar 

  9. Mizuno T (1999) The extraction and development of antitumor active polysaccharides from medicinal mushrooms in Japan. Int J Med Mushrooms 1:9–29

    Article  CAS  Google Scholar 

  10. Reshetnikov SV, Wasser SP, Tan KK (2001) Higher Basidiomycota as a source of antitumor and immunostimulating polysaccharides. Int J Med Mushrooms 3:361–394

    CAS  Google Scholar 

  11. King F, King T, Godson D, Manning L (1956) The chemistry of extractives from hardwoods. Part XXVIII. The occurrence of 3:4:3ʹ:5ʹ-tetrahydroxy- and 3:4:5:3΄:5-pentahydroxy-stilbene in Vouacapoua species. J Chem Soc 4477–4480

  12. Ferrigni NR, Mclaughlin JL, Powell RG, Smith CR (1984) Isolation of piceatannol as the antileukaemic principle from the seeds of Euphorbia lagascae. J Nat Prod 47:347–352

    Article  CAS  Google Scholar 

  13. Bavaresco L, Fregoni M, Trevisan M, Mattivi F, Vrhovsek U, Flachetti R (2002) The occurrence of the stilbene piceatannol in grapes. Vitis 41:133–136

    CAS  Google Scholar 

  14. Rimando AM, Kalt W, Magee JB, Dewey J, Ballington J (2004) Resveratrol, pterostilbene and piceatannol in Vaccinium berries. J Agr Food Chem 52:4713–4719

    Article  CAS  Google Scholar 

  15. Ku KL, Chang PS, Cheng YC, Lien CY (2005) Production of stilbenoids from the callus of Arachis hypogaea. A novel source of the anticancer compound piceatannol. J Agr Food Chem 53:3877–3881

    Article  CAS  Google Scholar 

  16. Piotrowska H, Kucinska M, Murias M (2012) Biological activity of piceatannol: leaving the shadow of resveratrol. Mutat Res 750:60–82

    Article  CAS  Google Scholar 

  17. Kuo PL, Hus YL (2008) The grape and wine constituent piceatannol inhibits proliferation of human bladder cancer cells via blocking cell cycle progression and inducing Fas/membrane bound Fas ligand-mediated apoptotic pathway. Mol Nutr Food Res 52:408–418

    Article  CAS  Google Scholar 

  18. Ko YJ, Kim HH, Kim EJ, Katakura Y, Lee WS, Ryu CH (2013) Piceatannol inhibits mast cell-mediated allergic inflammation. Int J Mol Med 31:951–958

    Article  CAS  Google Scholar 

  19. Kahkonen MP, Hopia AI, Vuorela HJ, Rauha J, Pihlaja K, Kujala TS, Heinonen M (1999) Antioxidant activity of plant extracts containing phenolic compounds. J Agric Food Chem 47:3954–3962

    Article  CAS  Google Scholar 

  20. Mossman T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    Article  Google Scholar 

  21. Engeland M, Ramaekers FCS, Schutte B, Reutelingsperger CP (1996) A novel assay to measure loss of plasma membrane asymmetry during apoptosis of adherent cells in culture. Cytometry 24:131–139

    Article  Google Scholar 

  22. Sanchez-Moreno C, Larrauri JA, Saura-Calixto F (1998) A procedure to measure the antiradical efficiency of polyphenols. J Sci Food Agric 76:270–276

    Article  CAS  Google Scholar 

  23. Slinkard K, Singleton VL (1977) Total phenol analysis, automation and comparison with manual methods. Am J Enol Vitic 28:49–55

    CAS  Google Scholar 

  24. Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559

    Article  CAS  Google Scholar 

  25. Meyers KJ, Watkins CB, Pritts MP, Liu RH (2003) Antioxidant and antiproliferative activities of strawberries. J Agric Food Chem 51:6887–6892

    Article  CAS  Google Scholar 

  26. Yfanti P, Batistatou A, Manos G, Lekka ME (2015) The aromatic plant Satureja horvatii ssp. macrophylla Induces apoptosis and cell death to the A549 cancer cell line. Am J Plant Sci 6:2092–2103

    Article  CAS  Google Scholar 

  27. Kim MY, Seguin P, Ahn JK, Kim JJ, Chun SC, Kim EH, Seo SH, Kang EY, Kim SL, Park YJ, Ro HM, Chung IM (2008) Phenolic compound concentration and antioxidant activities of edible and medicinal mushrooms from Korea. J Agric Food Chem 56:7265–7270

    Article  CAS  Google Scholar 

  28. Keckes S, Gasic U, Cirkovic-Velickovic T, Milojkovic-Opsenica D, Natic M, Tesic Z (2013) The determination of phenolic profiles of Serbian unifloral honeys using ultra-high-performance liquid chromatography/high resolution accurate mass spectrometry. Food Chem 138:32–40

    Article  CAS  Google Scholar 

  29. Barros L, Ferreira M-J, Queiros B, Ferreira ICFR., Baptista P (2007) Total phenols, ascorbic acid, b-carotene and lycopene in Portuguese wild edible mushrooms and their antioxidant activities. Food Chem 103:413–419

    Article  CAS  Google Scholar 

  30. Barros L, Duenas M, Ferreira IC, 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

    Article  CAS  Google Scholar 

  31. Vaz J, Barros L, Martins A, Santos-Buelga C, Vasconcelos H, Ferreira I (2011) Chemical composition of wild edible mushrooms and antioxidant properties of their water soluble polysaccharidic and ethanolic fractions. Food Chem 126:610–616

    Article  CAS  Google Scholar 

  32. Elmastas M, Isildak O, Turkekul I, Temur N (2007) Determination of antioxidant activity and antioxidant compounds in wild edible mushrooms. J Food Comp Anal 20:337–345

    Article  CAS  Google Scholar 

  33. Tsai S-Y, Tsai H-L, Mau J-L (2007) Antioxidant properties of Agaricus blazei, Agrocybe cylindracea and Boletus edulis. LWT 40:1392–1402

    Article  CAS  Google Scholar 

  34. Vidovic S, Mujic I, Zekovic Z, Lepojevic Z, Tumbas V, Mujic A (2010) Antioxidant properties of selected Boletus mushrooms. Food Biophys 5:49–58

    Article  Google Scholar 

  35. Heleno SA, Barros L, Sousa MJ, Martins A, Ferreira ICFR. (2010) Tocopherols composition of Portuguese wild mushrooms with antioxidant capacity. Food Chem 119:1443–1450

    Article  CAS  Google Scholar 

  36. Puttaraju NG, Venkateshaiah SU, Dharmesh SM, Urs SMN, Somasundaram R (2006) Antioxidant activity of indigenous edible mushrooms. J Agric Food Chem 54:9764–9772

    Article  CAS  Google Scholar 

  37. Gursoy N, Sarikurkcu C, Cengiz M, Solak MH (2016) Antioxidant activities, metal contents, total phenolics and flavonoids of seven Morchella species. Food Chem Toxicol 47:2381–2388

    Article  Google Scholar 

  38. Tahidul I, Xiaoming Y, Baojun X (2016) Phenolic profiles, antioxidant capacities and metal chelating ability of edible mushrooms commonly consumed in China. LWT 72:423–431

    Article  Google Scholar 

  39. Woldegiorgis AZ, Abate D, Haki GD, Ziegler GR (2014) Antioxidant property of edible mushrooms collected from Ethiopia. Food Chem 157:30–36

    Article  CAS  Google Scholar 

  40. Palacios Ι, Lozano Μ, Moro C, D’Arrigo M, Rostagno M, Martνnez J, Garcνa-Lafuente A, Guillamon E, Villares A (2011) Antioxidant properties of phenolic compounds occurring in edible mushrooms. Food Chem 128:674–678

    Article  CAS  Google Scholar 

  41. Josiana A (2010) Wild mushrooms Clitocybe alexandri and Lepista inversa: In vitro antioxidant activity and growth inhibitor of human tumour cell line. Food Chem Toxicol 48:2881–2884

    Article  Google Scholar 

  42. Ren D, Jiao Y, Yang X, Yuan L, Guo J, Zhao Y (2015) Antioxidant and antitumor effects of polysaccharides from the fungus Pleurotus abalonus. Chem Biol Interact 237:166–674

    Article  CAS  Google Scholar 

  43. Larrosa M, Tomas-Barberan FA, Espin JC (2004) The grape and wine polyphenol piceatannol is a potent inducer of apoptosis in human SK-Mel-28 melanoma cells. Eur J Nutr 43:275–284

    Article  CAS  Google Scholar 

  44. Rossi M, Caruso F, Opazo C, Salciccioli J (2008) Crystal and molecular structure of piceatannol; scavenging features of resveratrol and piceatannol on hydroxyl and peroxyl radicals and docking with transthyretin. J Agric Food Chem 56:10557–10566

    Article  CAS  Google Scholar 

  45. Kim Y, Park C, Lee J, Kim G, Lee W, Choi Y, Ryu C (2008) Induction of apoptosis by piceatannol in human leukemic U937 cells through down-regulation of Bcl-2 and activation of caspases. Oncol Rep 19:961–967

    CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Unit of Environmental, Organic and Biochemical high-resolution analysis-ORBITRAP-LC–MS of the University of Ioannina for providing access to the facilities. The authors would like to thank the Unit for technical infrastructure, characterization and testing of bioactive substances of the University of Ioannina for providing access to the facilities. The authors would like to thank the OPENSCREEN-GR network for providing access to the facilities.

Author information

Authors and Affiliations

  1. Department of Chemistry, Laboratory of Biochemistry, University of Ioannina, 45110, Ioannina, Greece

    Efstathios P. Vasdekis, Athanassios Karkabounas, Ioannis Giannakopoulos & Marilena E. Lekka

  2. Department of Crop Science, Laboratory of Vegetable Crops, Agricultural University of Athens, 11855, Athens, Greece

    Dimitrios Savvas

Authors
  1. Efstathios P. Vasdekis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Athanassios Karkabounas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ioannis Giannakopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dimitrios Savvas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marilena E. Lekka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marilena E. Lekka.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Compliance with ethics requirements

This article does not contain any studies with human or animal subjects.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vasdekis, E.P., Karkabounas, A., Giannakopoulos, I. et al. Screening of mushrooms bioactivity: piceatannol was identified as a bioactive ingredient in the order Cantharellales. Eur Food Res Technol 244, 861–871 (2018). https://doi.org/10.1007/s00217-017-3007-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-017-3007-y

Keywords

Search

Navigation