Abstract
Since antiquity, numerous macrofungi are being worshiped as food and natural medicine especially in Asian tribal communities. Recent investigation has correlated these medicinal properties with bioactive components including phenols and flavonoids. However, research on mushrooms is not satisfactory; as several traditionally prized members remain undiscovered or poorly explored yet. This backdrop tempted us to unveil secondary metabolites empowered with therapeutics from an ethnic delicacy, Russula alatoreticula that was justified as a novel macrofungus in our previous publication. Accordingly, methanol extract was prepared from dried basidiocarps that was found to be enriched with phenolic compounds (pyrogallol > cinnamic acid > p-coumaric acid) and ascorbic acid. As a result, the fraction exhibited strong antioxidant activity evident by the ability of quenching free radicals, chelating Fe2+ ion and reducing components with EC50 of 263–2382 µg/ml. Besides, effective antibacterial potential against six investigated microbes was also noticed where MIC value ranged from 99 to 2673.74 µg/ml. Furthermore, the extract revealed promising anticancer property as it induced apoptosis of Hep3B cell (IC50 358.57 µg/ml) by imparting morphological changes, interfering cell cycle, depleting MMP and alleviating ROS through Bax, Bcl2, caspases 9 and 3 intrinsic mitochondrial pathway. Overall study implied that the immense bioactive potential of R. alatoreticula could possibly be utilized as a good source of natural supplement to combat against free radicals, pathogenic bacteria and hepatocellular carcinoma as well as in food safety industry.
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References
Acharya K, Bera I, Khatua S, Rai M (2015a) Pharmacognostic standardization of Grifola frondosa: a well-studied medicinal mushroom. Pharm Lett 7(7):72–78
Acharya K, Khatua S, Sahid S (2015b) Pharmacognostic standardization of Macrocybe crassa: an imminent medicinal mushroom. Res J Pharm Technol 8(7):860–866
Acharya K, Ghosh S, Khatua S, Mitra P (2016) Pharmacognostic standardization and antioxidant capacity of an edible mushroom Laetiporus sulphureus. J Verbrauch Lebensm 11(1):33–42. https://doi.org/10.1007/s00003-015-0977-1
Acharya K et al (2017a) Exploring a new edible mushroom Ramaria subalpina: chemical characterization and antioxidant activity. Pharmacogn J 9:30–34. https://doi.org/10.5530/pj.2017.1.6
Acharya K, Khatua S, Ray S (2017b) Quality assessment and antioxidant study of Pleurotus djamor (Rumph. ex Fr.) Boedijn. J Appl Pharm Sci 7(6):105–110
Alves MJ, Ferreira ICFR, Pintado M (2012) Antimicrobial activity of wild mushroom extracts against clinical isolates resistant to different antibiotics. J Appl Microbiol 113:466–475. https://doi.org/10.1111/j.1365-2672.2012.05347.x
Alves MJ, Ferreira ICFR, Froufe HJC, Abreu RMV, Martins A, Pintado M (2013) Antimicrobial activity of phenolic compounds identified in wild mushrooms, SAR analysis and docking studies. J Appl Microbiol 115:346–357. https://doi.org/10.1111/jam.12196
Barros L, Dueñas 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(6):1076–1079. https://doi.org/10.1016/j.fct.2009.01.039
Biswal D, Pramanik NR, Chakrabarti S, Drew MGB, Acharya K, Chandra S (2017) Syntheses, crystal structures, DFT calculations, protein interaction and anticancer activities of water soluble dipicolinic acid-imidazole based oxidovanadium(IV) complexes. Dalton Trans 46:16682–16702. https://doi.org/10.1039/C7DT02903A
Boeing JS, Barizão ÉO, Silva BC, Montanher PF, Almeida VC, Visentainer JV (2014) Evaluation of solvent effect on the extraction of phenolic compounds and antioxidant capacities from the berries: application of principal component analysis. Chem Cent J 8:48. https://doi.org/10.1186/s13065-014-0048-1
Chatterjee S, Chatterjee A, Chandra S, Khatua S, Saha GK, Acharya K (2016) Tricholoma giganteum ameliorates benzo[α]pyrene-induced lung cancer in mice. Int J Curr Pharm Sci Rev Res 7(5):283–290
Dundar A et al (2015) Antioxidant, antimicrobial, cytotoxic and anticholinesterase activities of seven mushroom species with their phenolic acid composition. J Hortic 2:161. https://doi.org/10.4172/2376-0354.1000161
Golbano JM, López-Aparicio P, Recio MN, Pérez-Albarsanz M (2008) Finasteride induces apoptosis via Bcl-2, Bcl-xL, Bax and caspase-3 proteins in LNCaP human prostate cancer cell line. Int J Oncol 32:919–924
Gursoy N, Sarikurkeu C, Tepe B, Solak MH (2010) Evaluation of antioxidant activities of 3 edible mushrooms: Ramaria flava (Schaef.: Fr.) Quél., Rhizopogon roseolus (Corda) T.M. Fries., and Russula delica Fr. Food Sci Biotechnol 19(3):691–696. https://doi.org/10.1007/s10068-010-0097-8
Hsu S et al (2007) Crude extracts of Euchresta formosana radix induce cytotoxicity and apoptosis in human hepatocellular carcinoma cell line (Hep3B). Anticancer Res 27:2415–2426
Ivanova TS, Krupodorova TA, Barshteyn VY, Artamonova AB, Shlyakhovenko VA (2014) Anticancer substances of mushroom origin. Exp Oncol 36(2):58–66
Kashibhatla S, Amarante-Mendes GP, Finucane D, Brunner T, Bossy-Wetzel E, Green DR (2006) Acridine orange/ethidium bromide (AO/EB) staining to detect apoptosis. Cold Spring Harb Protoc. https://doi.org/10.1101/pdb.prot4493
Khatua S, Paul S, Acharya K (2013) Mushroom as the potential source of new generation of antioxidant: a review. Res J Pharm Technol 6(5):496–505
Khatua S, Dutta AK, Acharya K (2015) Russula senecis: a delicacy among the tribes of West Bengal. PeerJ 3:e810. https://doi.org/10.7717/peerj.810.eCollection
Khatua S, Dutta AK, Chandra S, Paloi S, Das K, Acharya K (2017a) Introducing a novel mushroom from mycophagy community with emphasis on biomedical potency. PLoS ONE 12(5):e0178050. https://doi.org/10.1371/journal.pone.0178050
Khatua S, Ghosh S, Acharya K (2017b) A simplified method for microtiter based analysis of in vitro antioxidant activity. Asian J Pharm 11(2):S327–S335
Khatua S, Ghosh S, Acharya K (2017c) Chemical composition and biological activities of methanol extract from Macrocybe lobayensis. J Appl Pharm Sci 7(10):144–151
Kosanic M, Rankovic B, Dasic M (2013) Antioxidant and antimicrobial properties of mushrooms. Bulg J Agric Sci 19(5):1040–1046
Kouassi KA, Kouadio EJP, Djè KM, Dué AE, Kouamé LP (2016) Edible ectomycorrhizal mushrooms Russula spp. of Côte d’Ivoire: total phenolic content, HPLC-profiles of phenolic compounds and organic acids, antioxidant activities. J Agric Chem Environ 5:73–84. https://doi.org/10.4236/jacen.2016.52008
Kozarski M et al (2015) Antioxidants of edible mushrooms. Molecules 20(10):19489–19525. https://doi.org/10.3390/molecules201019489
Liang C, Park AY, Guan JL (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2(2):329–333. https://doi.org/10.1038/nprot.2007.30
Lin J, Liu W (2006) o-Orsellinaldehyde from the submerged culture of the edible mushroom Grifola frondosa exhibits selective cytotoxic effect against Hep3B cells through apoptosis. J Agric Food Chem 54:7564–7569. https://doi.org/10.1021/jf0616762
Liu K, Liu P, Liu R, Wu X (2015) Dual AO/EB staining to detect apoptosis in osteosarcoma cells compared with flow cytometry. Med Sci Monit Basic Res 21:15–20. https://doi.org/10.12659/MSMBR.893327
Munshi A, Hobbs M, Meyn RE (2005) Clonogenic cell survival assay. In: Blumenthal RD (ed) Chemosensitivity. Humana Press, New York, pp 21–28
Nedelkoska DN et al (2013) Screening of antibacterial and antifungal activities of selected Macedonian wild mushrooms. Zb Matice Srp Prir Nauk 124:333–340. https://doi.org/10.2298/ZMSPN1324333N
Palacios I et al (2011) Antioxidant properties of phenolic compounds occurring in edible mushrooms. Food Chem 128:674–678. https://doi.org/10.1016/j.foodchem.2011.03.085
Panda MK, Tayung K (2015) Documentation and ethnomedicinal knowledge on wild edible mushrooms among ethnic tribes of northern Odisha, India. Asian J Pharm Clin Res 8(4):139–143
Park M et al (2003) Suppression of extracellular signal-related kinase and activation of p38 MAPK are two critical events leading to caspase-8-and mitochondria-mediated cell death in phytosphingosine-treated human cancer cells. J Biol Chem 278(50):50624–50634
Pereira DM, Valentão P, Pereira JA, Andrade PB (2009) Phenolics: from chemistry to biology. Molecules 14:2202–2211. https://doi.org/10.3390/molecules14062202
Pontiki E, Hadjipavlou-Litina D, Litinas K, Geromichalos G (2014) Novel cinnamic acid derivatives as antioxidant and anticancer agents: design, synthesis and modeling studies. Molecules 19:9655–9674. https://doi.org/10.3390/molecules19079655
Preet R et al (2012) Quinacrine has anticancer activity in breast cancer cells through inhibition of topoisomerase activity. Int J Cancer 130:1660–1670. https://doi.org/10.1002/ijc.26158
Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269:337–341. https://doi.org/10.1006/abio.1999.4019
Qiu GH, Xie X, Xu F, Shi X, Wang Y, Deng L (2015) Distinctive pharmacological differences between liver cancer cell lines HepG2 and Hep3B. Cytotechnol 67:1–12. https://doi.org/10.1007/s10616-014-9761-9
Ribble D, Goldstein NB, Norris DA, Shellman YG (2005) A simple technique for quantifying apoptosis in 96-well plates. BMC Biotechnol 5:12. https://doi.org/10.1186/1472-6750-5-12
Ruan-Soto F, Ordaz-Velázquez M, García-Santiago W, Pérez-Ovando EC (2017) Traditional processing and preservation of wild edible mushrooms in Mexico. Ann Food Process Preserv 2(1):1013
Sanchez C (2017) Reactive oxygen species and antioxidant properties from mushrooms. Synth Syst Biotechnol 2:13–22. https://doi.org/10.1016/j.synbio.2016.12.001
Shiraha H, Yamamoto K, Namba M (2013) Human hepatocyte carcinogenesis (Review). Int J Oncol 42:1133–1138. https://doi.org/10.3892/ijo.2013.1829
Singdevsachan SK, Patra JK, Tayung K, Sarangi K, Thatoi H (2014) Evaluation of nutritional and nutraceutical potentials of three wild edible mushrooms from Similipal Biosphere Reserve, Odisha, India. J Verbrauch Lebensm 9:111–120. https://doi.org/10.1007/s00003-014-0861-4
Tiong JJL, Loo JSE, Mai C-W (2016) Global antimicrobial stewardship: a closer look at the formidable implementation challenges. Front Microbiol 7:1860. https://doi.org/10.3389/fmicb.2016.01860
Wang D et al (2017) A new prenylated flavonoid induces G0/G1 arrest and apoptosis through p38/JNK MAPK pathways in human hepatocellular carcinoma cells. Sci Rep 7:5736. https://doi.org/10.1038/s41598-017-05955-0
Wu JY et al (2011) Anti-cancer effects of protein extracts from Calvatia lilacina, Pleurotus ostreatus and Volvariella volvacea. Evid Based Complement Alternat Med. https://doi.org/10.1093/ecam/neq057
Xu W, Huang JJ, Cheung PCK (2012) Extract of Pleurotus pulmonarius suppresses liver cancer development and progression through inhibition of VEGF-induced PI3 K/AKT signaling pathway. PLoS ONE 7(3):e34406. https://doi.org/10.1371/journal.pone.0034406
Youn M et al (2008) Chaga mushroom (Inonotus obliquus) induces G0/G1 arrest and apoptosis in human hepatoma HepG2 cells. World J Gastroenterol 14(4):511–517. https://doi.org/10.3748/wjg.14.511
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Authors would like to acknowledge the facilities provided by Department of Botany (UGC-CAS Phase VI, VII), University of Calcutta and DST-FIST for instrumental support.
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Khatua, S., Chandra, S. & Acharya, K. Expanding knowledge on Russula alatoreticula, a novel mushroom from tribal cuisine, with chemical and pharmaceutical relevance. Cytotechnology 71, 245–259 (2019). https://doi.org/10.1007/s10616-018-0280-y
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DOI: https://doi.org/10.1007/s10616-018-0280-y