Assessment of antioxidant and anticancer attributes of crude extracts from edible mushrooms Lycoperdon molle and Apioperdon pyriforme

Abstract

The study analyzed extracts from two mushroom species, Lycoperdon molle and Apioperdon pyriforme, for their phenolic and flavonoid compound contents, antioxidant capacities, enzyme activities, and cytotoxic effects against human colorectal and breast cancer cells. LM extract was found to contain higher levels of phenolic compounds, including catechin, gallic acid, and myricetin. While AP extract had a higher concentration of gallic acid. Both extracts exhibited antioxidant activity, with LM showing slightly higher DPPH radical scavenging rates. However, their activities were weaker compared to standard antioxidants like gallic acid and quercetin. Enzyme assays revealed that both extracts inhibited CAT activity, activated GPx activity, and induced SOD activity. LM extract also inhibited GST activity, while AP extract showed activation at a certain concentration. In terms of cytotoxicity against cancer cells, LM extract displayed greater efficacy than AP, with lower IC50 values for both HT-29 colon cancer cells and MCF-7 breast cancer cells. Overall, the study highlights the potential differential bioactive properties of LM and AP extracts, with LM demonstrating stronger antioxidant and anti-cancer effects.

Keywords

• Antioxidant
• anticancer
• bioactive compounds
• Lycoperdon mole
• Apioperdon pyriforme

References

1. [1]Chun S, Gopal J, Muthu M. Antioxidant Activity of mushroom extracts /polysaccharides -their antiviral properties and plausible AntiCOVID-19 properties. Antiox. 2021; 10(12):1899. https://doi.org/10.3390/antiox10121899
2. [2]Nowakowski P, Markiewicz-Żukowska R, Bielecka J, Mielcarek K, Grabia M, Socha K. Treasures from the forest: Evaluation of mushroom extracts as anti-cancer agents. Biomed Pharmacother. 2021; 143:112106. https://doi.org/10.1016/j.biopha.2021.112106.
3. [3]Chang ST, Wasser SP. Current and future research trends in agricultural and biomedical applications of medicinal mushrooms and mushroom products. Int J Med Mushrooms. 2018; 20(12):1121-1133. http://dx.doi.org/10.1615/IntJMedMushrooms.2018029378.
4. [4]Venturella G, Ferraro V, Cirlincione F, Gargano ML. Medicinal mushrooms: Bioactive compounds, use, and clinical trials. Int J Mol Sci. 2021;22(2):634. https://doi.org/10.3390/ijms22020634
5. [5]Dizeci N, Onar O, Karaca B, Demirtas N, Coleri Cihan A, Yildirim O. Comparison of the chemical composition and biological effects of Clitocybe nebularis and Infundibulicybe geotropa. Mycologia. 2021; 113(6):1156-1168. https://doi.org/10.1080/00275514.2021.1951076
6. [6]Dimopoulou M, Kolonas A, Mourtakos S, Androutsos O, Gortzi O. Nutritional composition and biological properties of sixteen edible mushroom species. Appl Sci. 2022; 12: 8074. https://doi.org/10.3390/app12168074
7. [7]Onar O, Telkoparan-Akillilar P, Yildirim O. Clitocybe nebularis extract and 5‑fluorouracil synergistically inhibit the growth of HT-29 colorectal cancer cells by inducing the S phase arrest. 3 Biotech. 2023; 13(2):48. https://doi.org/10.1007/s13205-023-03471-9
8. [8]Kirk PF, Cannon PF, Minter DW, Stalpers JA, Dictionary of the fungi, 10th ed, CAB International. Wallingford, USA, 2008, pp.784.

9. [9]Pegler DN, Laessøe T, Spooner BM. British puffballs, earthstars end stinkhorns. An account of the British Gasteroid fungi. –mRoyal Botanic Gardens: Kew, 1995.
10. [10]Calonge FD. Gasteromycetes, I. Lycoperdales, Nidulariales, Phallales, Sclerodermatales, Tulostomatales. Real Jardin Botanico, Stuttgart, 1998.
11. [11]He MQ, Zhao RL, Hyde KD, Begerow D, Kemler M, Yurkov A, Kirk PM. Notes, outline and divergence times of Basidiomycota. Fungal Divers. 2019; 99(1): 105-367. https://doi.org/10.1007/s13225-023-00529-0
12. [12]Onar O, Akata I, Celep GS, Yildirim O. Antioxidant activity of extracts from the red-belt conk medicinal mushroom, Fomitopsis pinicola (Agaricomycetes), and its modulatory effects on antioxidant enzymes. Int J Med Mushrooms. 2016; 186:501–508. https://doi.org/10.1615/IntJMedMushrooms.v18.i6.4
13. [13]Dizeci N, Karaca B, Onar O, Cihan AC, Akata I, Yildirim O. The remarkable antibiofilm activity of the sweet tooth mushroom, Hydnum repandum (Agaricomycetes), displaying synergetic ınteractions with antibiotics. Int J Med Mushrooms. 2021; 23(10):45-60. 10.1615/IntJMedMushrooms.2021040148
14. [14]Sharma OP, Bhat TK. DPPH antioxidant assay revisited. Food Chem. 2009; 113:1202–1205. https://doi.org/10.1016/j.foodchem.2008.08.008
15. [15]Shomali Moghaddam N, Isgor BS, Isgor YG, Geven F, Yildirim O. The evaluation of inhibitory effects of selected plant extracts on antioxidant enzymes. Fresenius Environ Bull. 2015; 24(1):63–70.
16. [16]Aebi H. Catalase in vitro. Methods Enzymol. 1984; 105:121–126.
17. [17]Habig WH, Pabst MJ, Jakoby WB. Glutathione-S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem. 1974; 249:7130–7139.
18. [18]Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med. 1967; 70:158–169.
19. [19]Geller ΒL, Winge DR. Subcellular distribution of superoxide dismutases in rat liver. Methods Enzymol. 1984; 105:105–114.
20. [20]van Meerloo J, Kaspers GJ, Cloos J. Cell sensitivity assays: The MTT assay. Methods Mol Biol. 2011; 731:237–245. https://doi.org/10.1007/978-1-61779-080-5_20.
21. [21]Cosme P, Rodríguez AB, Espino J, Garrido M. Plant phenolics: Bioavailability as a key determinant of their potential health-promoting applications. Antioxidants (Basel). 2020;9(12):1263. https://doi.org/10.3390/antiox9121263
22. [22]Kahkeshani N, Farzaei F, Fotouhi M, Alavi SS, Bahramsoltani R, Naseri R, Momtaz S, Abbasabadi Z, Rahimi R, Farzaei MH, Bishayee A. Pharmacological effects of gallic acid in health and diseases: A mechanistic review. Iran J Basic Med Sci. 2019; 22(3):225-237. https://doi.org/10.22038/ijbms.2019.32806.7897
23. [23]Barros L, Venturini BA, Baptista P, Estevinho LM, Ferreira IC. Chemical composition and biological properties of Portuguese wild mushrooms: a comprehensive study. J Agr Food Chem. 2008; 56(10): 3856-3862. https://doi.org/10.1021/jf8003114
24. [24]Altaf U, Lalotra P, Sharma YP. Nutritional and mineral composition of four wild edible mushrooms from Jammu and Kashmir, India. Indian Phytopath. 2020; 73: 313–320. https://doi.org/10.1007/s42360-020-00230-1.
25. [25]Singh P, Singh A, D'Souza L, Roy U, Singh S. Chemical constituents and antioxidant activity of the Arctic mushroom Lycoperdon molle Pers. Polar Res. 2012; 31(1): 17329. https://doi.org/10.3402/polar.v31i0.17329
26. [26]Bal C, Akgül H, Sevindik M. The Antioxidant potential of ethanolic extract of edible mushroom Lycoperdon molle Pers. (Agaricomycetes). Eur J Forest Sci. 2019; 7 (3):277-283. https://doi.org/10.31195/ejejfs.591432
27. [27]Kıvrık M, Süfer Ö, Bozok F. A Research on quality evaluation of eight wild edible macrofungi collected from east Mediterranean region of Turkey. Chem Biodivers. 2022; 19(3): e202100967. https://doi.org/10.1002/cbdv.202100967
28. [28]Kozarski M, Klaus A, Jakovljevic D, Todorovic N, Vunduk J, Petrović P, Niksic M, Vrvic MM, van Griensven L. Antioxidants of edible mushrooms. Molecules. 2015; 20(10): 19489-19525. https://doi.org/10.3390/molecules201019489.
29. [29]Liuzzi GM, Petraglia T, Latronico T, Crescenzi A, Rossano R. Antioxidant compounds from edible mushrooms as potential candidates for treating age-related neurodegenerative diseases. Nutrients. 2023; 15(8):1913. https://doi.org/10.3390/nu15081913
30. [30]Emsen B, Güven B, Kaya A. Yabani yenilebilir bir mantar olan Lycoperdon molle Pers.'nin antioksidan ve antigenotoksik potansiyeli. KSÜ Tarım ve Doğa Derg. 2019; 22(5): 724-732. https://doi.org/10.18016/ksutarimdoga.v22i45606.523756
31. [31]Huang WY, Cai YZ, Zhang Y. Natural phenolic compounds from medicinal herbs and dietary plants: Potential use for cancer prevention. Nutr Cancer. 2009; 62:1–20. https://doi.org/10.1080/01635580903191585
32. [32]Haque MA, Islam MAU. Pleurotus highking mushroom ınduces apoptosis by altering the balance of proapoptotic and antiapoptotic genes in breast cancer cells and ınhibits tumor sphere formation. Medicina. 2019; 55(11):716. https://doi.org/10.3390/medicina55110716
33. [33]Pathak MP, Pathak K, Saikia R, Gogoi U, Ahmad MZ, Patowary P, Das A. Immunomodulatory effect of mushrooms and their bioactive compounds in cancer: A comprehensive review. Biomed Pharmacother. 2022; 149:112901. https://doi.org/10.1016/j.biopha.2022.112901