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Extracts of Hypsizygus tessellatus (white var.) caps inhibited MCF-7 and MDA-MB-231 cell lines proliferation

  • C. I. Ukaegbu
  • S. R. Shah
  • H. A. Hamid
  • Z. Normaiza
  • O. R. Alara
Original Paper
  • 22 Downloads

Abstract

Cancer management is associated with serious side-effects due to the harmful nature of radiation and chemotherapy on the body cells. These side-effects have necessitated the need for diversifying the alternative or complementary sources of cancer therapy. Natural products have been on the front line as alternative sources of anticancer agents and have attracted much attention in recent times. In this study, the anticancer activity of Hypsizygus tessellatus (white var.) caps (also known as Bunapi shimeji) extracted with acetone and ethyl acetate was evaluated in vitro against MDA-MB-231 and MCF-7 (breast cancer cell lines) and MCF-10a (Vero or normal breast cells). Likewise, the free radical scavenging and metal reducing activities of the extract were evaluated through in vitro chemical-based methods. Furthermore, the phytochemical compositions of the extracts were determined through LC–MS-QTOF-assisted mass spectroscopy. The results of this study indicated that acetone fraction had better radical scavenging activity against DPPH (IC50 = 0.76 mg/mL) and H2O2 (IC50 = 0.84 mg/mL) than ethyl acetate fraction against DPPH (IC50 = 1.10 mg/mL) and H2O2 (IC50 = 1.26 mg/mL) (p < 0.05). Additionally, the acetone fraction was observed to have more antiproliferative effects against MCF-7 (IC50 = 0.051–0.055 mg/mL) and MDA-MB-231 (IC50 = 0.122–0.131 mg/mL) compared to the ethyl acetate fraction against MCF-7 (IC50 = 0.075–0.096 mg/mL) and MDA-MB-231 (IC50 = 0.161–0.164 mg/mL) (p < 0.05). Both extracts generally had less effect on MCF-10a cells. Thus, these results suggested that Bunapi shimeji caps is a potential good natural source of anticancer agents.

Keywords

MCF-7 MDA-MB-231 Antioxidant Antiproliferation Bunapi shimeji H. tessellatus Mushroom phytochemicals 

Notes

Acknowledgements

This work was supported by the Universiti Malaysia Pahang under Grant Numbers PGRS1703102 and RDU160156.

References

  1. 1.
    S. Kusavadee, B. Benjaporn, N. Khwanyuruan, J. Piyanoot, S. Aphidech, Antibacterial and anti-breast cancer cell line activities of Sanghuangporus sp.1 extracts. Trop. J. Pharm. Res. 16(3), 613–620 (2017)CrossRefGoogle Scholar
  2. 2.
    K. Marijana, R.A.R. Branislav, T. Stanojkovic, Evaluation of metal concentration and antioxidant, antimicrobial, and anticancer potentials of two edible mushrooms Lactarius deliciosus and Macrolepiota procera. J. Food Drug Anal. 24, 477–484 (2016)CrossRefGoogle Scholar
  3. 3.
    N. Nowacka, R. Nowak, M. Drozd, M. Olech, R. Los, A. Malm, Antibacterial, antiradical potential and phenolic compounds of thirty-one polish mushrooms. PLoS ONE. 10, 0140355 (2015)CrossRefGoogle Scholar
  4. 4.
    B. Naser, S.-H. Mohammad, M. Mojtaba, F. Mostafa, Phytochemical components, total phenol and mineral contents and antioxidant activity of six major medicinal plants from Rayen, Iran. Nat. Prod. Res. 32(5), 564–567 (2018)CrossRefGoogle Scholar
  5. 5.
    M. Khan, M.A. Rahman, M. Sardar, N. Arman, S.I. Islam, B. Khandakar, J.A. Rashid, A.H.M. Sadik, G. Khurshid Alam, Comparative investigation of the free radical scavenging potential and anticancer property of Diospyros blancoi (Ebenaceae). Asian Pac. J. Trop. Biomed. 6(5), 410–417 (2016)CrossRefGoogle Scholar
  6. 6.
    L.M. Cheung, P.C.K. Cheung, V.E.C. Ooi, Antioxidant activity and total phenolics of edible mushroom extracts. Food Chem. 81, 249–255 (2003)CrossRefGoogle Scholar
  7. 7.
    W. Breene, Nutritional and medical value of specialty mushrooms. J. Food Protect. 53, 883–894 (1990)CrossRefGoogle Scholar
  8. 8.
    C. Ramesh, G. Manohar, Antimicrobial properties, antioxidant activity and bioactive compounds from six wild edible mushrooms of Western Ghats of Karnataka, India. Pharmacognosy Res. 2(2), 107–112 (2010)CrossRefGoogle Scholar
  9. 9.
    Z. Sroka, W. Cisowski, Hydrogen peroxide scavenging, antioxidant and anti-radical activity of some phenolic acids. Food Chem. Toxicol. 41(6), 753–758 (2003)CrossRefGoogle Scholar
  10. 10.
    M.Y. Kim, P. Seguin, J.K. Ahn, J.J. Kim, S.C. Chun, E.H. Kim, S.H. Seo, E.Y. Kang, S.L. Kim, Y.J. Park, H.M. Ro, Phenolic compound concentration and antioxidant activities of edible and medicinal mushrooms from Korea. J. Agric. Food Chem. 56, 7265–7270 (2008)CrossRefGoogle Scholar
  11. 11.
    K. Liu, X. Xiao, J. Wang, C.O. Chen, H. Hu, Polyphenolic composition and antioxidant, antiproliferative, and antimicrobial activities of mushroom Inonotus sanghuang. LWT Food Sci. Technol. 82, 154–161 (2017)CrossRefGoogle Scholar
  12. 12.
    H.A. Hamid, M. Roziasyahira, M.Y. Mashitah, A.A.F. Nurul, Comparative analysis of antioxidant and antiproliferative activities of Rhodomyrtus tomentosa extracts prepared with various solvents. Food Chem. Toxicol. 108(Part B), 451–457 (2016)Google Scholar
  13. 13.
    US Breast Cancer Statistics, Breast cancer reports (2018)Google Scholar
  14. 14.
    H. Seonwook, K. Jeong, I.H. Kim, H. Young, Inhibitory effect of ethanolic extract of Ramulus mori on adipogenic differentiation of 3T3-L1 cells and their antioxidant activity. J. Food Biochem. 42(2), e12469 (2017)Google Scholar
  15. 15.
    S. Muhammad, R. Allah, S. Masood, A. Muhammad, Investigating the antioxidant potential of licorice extracts obtained through different extraction modes, J. Food Biochem. 42(2), e12466 (2017)Google Scholar
  16. 16.
    B.M.A. Hajdari, G. Annamaria, B. Giangiacomo, G. Fabrizio, B. Susanna, B. Simona, M. Anna, M. Xhavit, K. Shqipe, B.P. Daniela, Phytochemical and sensorial characterization of Hyssopus officinalis subsp. aristatus (godr.) Nyman (Lamiaceae) by GC–MS, HPLC–UV–DAD, spectrophotometric assays and e-nose with aid of chemometric techniques. Eur. Food Res. Technol. (2018). doi. https://doi.org/10.1007/s00217-018-3046-z CrossRefGoogle Scholar
  17. 17.
    O. Odeja, C. Ogwuche, E. Elemike, G. Obi, Phytochemical screening, antioxidant and antimicrobial activities of Acalypha ciliata plant. Clin. Phytosci. 2(1), 12 (2017)CrossRefGoogle Scholar
  18. 18.
    V. Maruthamuthu, K. Ruckmani, Ferric reducing anti-oxidant power assay in plant extract. Bangladesh J. Pharmacol. 11, 570–572 (2016)CrossRefGoogle Scholar
  19. 19.
    A. Mftah, H. Fatah, S. Mothanna, E. Mohamed, J. Thomas, S. Mohammed, R. Abdullah, H. Yun, S. Rashid, Physicochemical properties, cytotoxicity, and antimicrobial activity of sulphated zirconia nanoparticles. Int. J. Nanomed. 10, 765–774 (2015)CrossRefGoogle Scholar
  20. 20.
    N. de Carvalho, S. Neves, R. Dias, L. Valverde, C. Sales, C. Rocha, M. Soares, E. dos Santos, R. Oliveira, R. Carlos, P. Nogueira, D. Bezerra, A novel ruthenium complex with xanthoxylin induces S-phase arrest and causes ERK1/2-mediated apoptosis in HepG2 cells through a p53-independent pathway. Cell Death Dis.  https://doi.org/10.1038/s41419-017-0104-6 (2018)CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    J. Guan, C. Lai, S. Li, A rapid method for the simultaneous determination of 11 saponins in Panax notoginseng using ultra performance liquid chromatography. J. Pharm. Biomed. Anal. 44(4), 996–1000 (2007)CrossRefGoogle Scholar
  22. 22.
    S.R. Shah, C.I. Ukaegbu, H.A. Hamid, O.R. Alara, Evaluation of antioxidant and antibacterial activities of the stems of Flammulina velutipes and Hypsizygus tessellatus (white and brown var.) extracted with different solvents. Food Meas. (2018).  https://doi.org/10.1007/s11694-018-9810-8 CrossRefGoogle Scholar
  23. 23.
    M. Kumara, M. Shylajab, P. Nazeemc, 6-Gingerol is the most potent anticancerous compound in ginger (Zingiber officinale Rosc.). J. Dev. Drugs.  https://doi.org/10.4172/2329-6631.1000167 (2017)CrossRefGoogle Scholar
  24. 24.
    A. Ataie, M. Sabetkasaei, A. Haghparast, A. Moghaddam, B. Kazeminejad, Neuroprotective effects of the polyphenolic antioxidant agent, Curcumin, against homocysteine-induced cognitive impairment and oxidative stress in the rat. Pharmacol. Biochem. Behav. 96, 378–385 (2010)CrossRefGoogle Scholar
  25. 25.
    S.A. Addai, Z.R. Abdullah, A. Mutalib, Effect of extraction solvents on the phenolic content and antioxidant properties of two papaya cultivars. J. Med. Plants Res. 7, 3354–3359 (2013)Google Scholar
  26. 26.
    A.N. Dar, B.N. Savita, S. Gulzar, Effect of storage period on physiochemical, total phenolic content and antioxidant properties of bran enriched snacks. Food Meas. 10, 755–761 (2016)CrossRefGoogle Scholar
  27. 27.
    S. Visht, S. Chaturvedi, Isolation of natural products. Curr. Pharma Res. 2, 584–599 (2012)Google Scholar
  28. 28.
    A. Hazrulrizawati, N. Aizi, Z. Normaiza, M. Mashitah, UPLC-QTOF/MS-based phenolic profiling of Melastomaceae, their antioxidant activity and cytotoxic effects against human breast cancer cell MDA-MB-231. Food Chem. 265, 253–259 (2018)CrossRefGoogle Scholar
  29. 29.
    M.N. Alam, N.J. Bristi, M. Rafiquzzaman, Review on in vivo and in vitro methods evaluation of antioxidant activity. Saudi Pharm. J. 21, 143–152 (2013)CrossRefGoogle Scholar
  30. 30.
    M.H. Baratzadeh, A. Asoodeh, J. Chamani, Antioxidant peptides obtained from goose egg white proteins by enzymatic hydrolysis. Int. J. Food Sci. Technol. 48, 1603–1609 (2013)CrossRefGoogle Scholar
  31. 31.
    D. Susanti, H. Sirat, F. Ahmad, R. Ali, N. Aimi, M. Kitajima, Antioxidant and cytotoxic flavonoids from the flowers of Melastoma malabathricum L. Food Chem. 103(3), 710–716 (2007)CrossRefGoogle Scholar
  32. 32.
    L. Lespade, S. Bercion, Theoretical investigation of the effect of sugar substitution on the antioxidant properties of flavonoids. Free Radical Res. 46(3), 346–358 (2012)CrossRefGoogle Scholar
  33. 33.
    P. Siddhuraju, K. Becker, Antioxidant properties of various solvent extracts of total phenolic constituents from three different agroclimatic origins of drumstick tree (Moringa oleifera Lam.) leaves. J. Agric. Food Chem. 51, 2144–2155 (2003)CrossRefGoogle Scholar
  34. 34.
    C.I. Ukaegbu, S.R. Shah, Biological characterization of water extracts from the caps and stalks of white Hypsizygus tessellatus (Bunapi shimeji) and Flammulina velutipes (Enoki) mushrooms. Innov. Int. J. Med. Pharm. Sci. 2(3), 1–5 (2017)Google Scholar
  35. 35.
    Z. Hodzic, H. Pasalic, A. Memisevic, M. Scrabovic, M. Saletovic, M. Poljakovic, The influence of total phenols content on antioxidant capacity in the whole grain extracts. Eur. J. Sci. Res. 28, 471–477 (2009)Google Scholar
  36. 36.
    F. Schafer, G. Buettner, Redox environment of the cell as viewed through the redox state of the gluthathione disulfide/gluthathione couple. Free Radical Biol. Med. 30(11), 1191–1212 (2001)CrossRefGoogle Scholar
  37. 37.
    A. Moure, D. Franco, J. Sineiro, H. Domĭngguez, M. Nūňez, J. Lema, Antioxidant activity of extracts from Gevuina avellana and Rosa rubiginosa defatted seeds. Food Res. Int. 34(2), 103–109 (2001)CrossRefGoogle Scholar
  38. 38.
    C.I. Ukaegbu, S.R. Shah, A.H. Hazrulrizawati, O.R. Alara, Acetone extract of Flammulina velutipes caps: a promising source of antioxidant and anticancer agents. Beni-Suef Univ. J. Basic Appl. Sci. (2018).  https://doi.org/10.1016/j.bjbas.2018.07.012 CrossRefGoogle Scholar
  39. 39.
    T.Y. Forbes-hernández, F. Giampieri, M. Gasparrini, L. Mazzoni, J.L. Quiles, J.M. Alvarez-suarez, M. Battino, The effects of bioactive compounds from plant foods on mitochondrial function: a focus on apoptotic mechanisms. Food Chem. Toxicol. 68, 154–182 (2014)CrossRefGoogle Scholar
  40. 40.
    H. Youn, J.C. Jeong, Y.S. Jeong, E.J. Kim, S.J. Um, Quercetin potentiates apoptosis by inhibiting nuclear factor-kappaB signaling in H460 lung cancer cells. Biol. Pharm. Bull. 36, 944–951 (2013)CrossRefGoogle Scholar
  41. 41.
    K. Bishayee, S. Ghosh, A. Mukherjee, R. Sadhukhan, J. Mondal, A.R. Khuda-Bukhsh, Quercetin induces cytochrome-c release and ROS accumulation to promote apoptosis and arrest the cell cycle in G2/M, in cervical carcinoma: signal cascade and drug–DNA interaction. Cell. Prolif. 46, 153–163 (2013)CrossRefGoogle Scholar
  42. 42.
    P.E. Sugantha, K. Selvakumar, S. Bavithra, P. Elumalai, R. Arunkumar, S.P. Raja, M.A. Brindha, J. Arunakaran, Anti-cancer activity of quercetin in neuroblastoma: an in vitro approach. Neurol. Sci. 35, 163–170 (2014)CrossRefGoogle Scholar
  43. 43.
    S. Banerjee, Y. Zhang, Z. Wang, M. Che, P.J. Chiao, J.L. Abbruzzese, F.H. Sarkar, In vitro and in vivo molecular evidence of genistein action in augmenting the efficacy of cisplatin in pancreatic cancer. Int. J. Cancer 120, 906–917 (2007)CrossRefGoogle Scholar
  44. 44.
    C. Tophkhane, S. Yang, W. Bales, L. Archer, A. Osunkoya, A.D. Thor, X. Yang, Bcl-2 overexpression sensitizes MCF-7 cells to genistein by multiple mechanisms. Int. J. Oncol. 31, 867–874 (2007)PubMedGoogle Scholar
  45. 45.
    S.M. Shin, I.J. Cho, S.G. Kim, Resveratrol protects mitochondria against oxidative stress through AMP-activated protein kinase-mediated glycogen synthase kinase-3beta inhibition downstream of poly(ADPribose) polymerase-LKB1 pathway. Mol. Pharmacol. 76, 884–895 (2009)CrossRefGoogle Scholar
  46. 46.
    H. Itoh, H. Ito, H. Hibasami, Blazein of a new steroid isolated from Agaricus blazei Murrill (himematsutake) induces cell death and morphological change indicative of apoptotic chromatin condensation in human lung cancer LU99 and stomach cancer KATO III cells. Oncol. Rep. 20, 1359–1361 (2008)PubMedGoogle Scholar
  47. 47.
    K. Marijana, R. Branislav, T. Stanojkovic, Evaluation of metal concentration and antioxidant, antimicrobial, and anticancer potentials of two edible mushrooms Lactarius deliciosus and Macrolepiota procera. J. Food Drug Anal. 24, 477–484 (2016)CrossRefGoogle Scholar
  48. 48.
    D. Kim, K. Han, K. Song, K. Lee, S. Jo, S. Lee, T. Yoon, Activation of Innate Immunity by Lepiota procera enhances antitumor activity. Korean J. Pharmacogn. 41, 115–121 (2010)Google Scholar
  49. 49.
    T. Xu, R. Beelman, J. Lambert, The cancer preventive effects of edible mushrooms. Anticancer Agents Med. Chem. 12, 1255–1263 (2012)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of Industrial Sciences & TechnologyUniversiti Malaysia PahangGambangMalaysia
  2. 2.Faculty of Chemical & Natural Resources EngineeringUniversiti Malaysia PahangGambangMalaysia

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