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Antioxidant activity of partially characterized polysaccharides from the edible mushroom Pleurotus djamor var. roseus

  • Received : 2021.08.02
  • Accepted : 2021.09.01
  • Published : 2021.09.30

Abstract

Mushroom-derived polysaccharides, which are the primary bioactive constituents, are beneficial for human health. Polysaccharides have immuno-modulation, antitumor, and antioxidant properties. Additionally, they have antiviral properties and protect against chronic radiation stress. In this study, high yield water-soluble polysaccharides were obtained from Pleurotus djamor var. roseus basidiocarps. The crude polysaccharide (CP) was extracted sequentially by hot water and ethanol precipitation. The yield of the brown CPs was 5.6% dw. Diethylaminoethyl cellulose and Sepharose-6B column chromatography of CPs generated several fractions. Total glucan content was determined in all the fractions. The F1 fraction displayed the highest sugar content and was considered as a purified polysaccharide (PP). The total glucan and β-glucan content in the four fractions ranged between 76.85-2.95% and 75.08-1.46%, respectively. The yield of the PPs was 300 mg, and it was obtained as a white powder. The PPs were characterized by Fourier-transform infrared spectroscopy (FTIR) and thin-layer chromatography. The FTIR spectral details confirmed the presence of a xylopentose polysaccharide. The antioxidant activity of the PPs was evaluated using in vitro 1,1-diphenyl-2-picryl-hydrazyl (DPPH) free radical scavenging assay and superoxide radical scavenging assay. The PPs showed strong DPPH free radical and superoxide anion radical scavenging activities in a dose-dependent manner. Purified PPs free of phenolics, protein, and carbohydrates were mainly responsible for the radical scavenging activity. The data suggest the potential of PPs as natural antioxidants.

버섯 다당류는 면역 조절 기능, 항암 및 항산화 활성을 비롯하여 항바이러스 활성과 방사선스트레스의 경감등 인체에 유익한 다양한 생리활성을 나타낸다. 본 연구에서는 분홍느타리버섯 (Pleurotus djamor var. roseus Corner)으로부터 뜨거운 물과 에탄올 침전을 이용하여 5.6%의 수율로 갈색을 띠는 경화된 다당류(CPs)를 순차적으로 추출하였다. 이렇게 추출된 CP는 Diethylaminoethyl cellulose(DEAE) 및 sepharose-6B 컬럼 분리를 통해 4개의 분획을 얻었고 각 분획의 총 글루칸 함량은 각각 76.85%, 2.95%, 75.08%, 1.46%로 밝혀졌다. 이중 가장 높은 수율의 분획(PP)으로부터 300 mg의 백색 분말이 얻어 졌으며, 박층 크로마토그래피(TLC)와 푸리에 변환 적외선 분광법(FTIR)의 결과로부터 자일로펜토스 유형의 화합물과 함께 다당류 부분의 존재를 확인하였다. PP의 항산화 활성은 1,1-diphenyl-2-picryl-hydrazyl(DPPH) 자유라디칼 소거 분석 및 슈퍼옥사이드 라디칼 소거 분석을 통하여 높은 활성을 나타냄을 확인하였다. PP분획에는 페놀, 단백질 및 단순 탄수화물이 없는 정제된 베타글루칸이 주 구성성분으로, 정제된 다당류가 천연 항산화제로 사용될 수 있음을 알 수 있었다.

Keywords

Acknowledgement

The first author thanks the Department of Chemical Engineering, Graduate School of Chosun University and Korea Forest Service (Korea Forestry Promotion Institute - Project no. 2020191B10-2022-BA01), Republic of Korea, for the postdoctoral fellowships.

References

  1. Akhigbe R, Ajayi A. 2021. The impact of reactive oxygen species in the development of cardiometabolic disorders: a review. Lipids Health Dis 20: 23. https://doi.org/10.1186/s12944-021-01435-7
  2. Assis IS, Chaves MB, Silveira MLL, Gern RMM, Wisbeck E, Junior AF, Furlan SA. 2013. Production of bioactive compounds with antitumor activity against Sarcoma 180 by Pleurotus sajor-caju. J Med Food 16: 1004-1012. https://doi.org/10.1089/jmf.2012.0267
  3. Benov L. 2001. How superoxide radical damages the cell. Protoplasma 217: 33-36. https://doi.org/10.1007/BF01289410
  4. Bobek P, Ozdin L, Kuniak L. 1997. Effect of oyster mushroom and isolated beta-glucan on lipid peroxidation and on the activities of antioxidative enzymes in rats fed the cholesterol diet. J Nutr Biochem 8: 469-471. https://doi.org/10.1016/S0955-2863(97)00058-2
  5. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  6. Brand-Williams W, Cuvelier ME, Berset C. 1995. Use of a free radical method to evaluate antioxidant activity. Lebensm Wiss Technol 28: 25-30. https://doi.org/10.1016/S0023-6438(95)80008-5
  7. Camelini CM, Rossi MJ, Cardozo FTGS, Gomes A, Sales-Campos C, Giachini AJ. 2014. Fungal cultivation and production of polysaccharides. In: K.G. Ramawat & J.M. Merillon (ed.), Polysaccharides. Springer. Switzerland.
  8. Chen P, Yong Y, Gu Y, Wang Z, Zhang S, Lu L. 2015. Comparison of antioxidant and antiproliferation activities of polysaccharides from eight species of medicinal mushrooms. Int J Med Mushrooms 17: 287-295. https://doi.org/10.1615/IntJMedMushrooms.v17.i3.80
  9. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Anal Chem 28: 350-356. https://doi.org/10.1021/ac60111a017
  10. Fan L, Li J, Deng K, Ai L. 2012. Effects of drying methods on the antioxidant activities of polysaccharides extracted from Ganoderma lucidum. Carbohydr Polym 87: 1849-1854. https://doi.org/10.1016/j.carbpol.2011.10.018
  11. Figueiro SD, Goes JC, Moreira RA, Sombra ASB. 2004. On the physico-chemical and dielectric properties of glutaraldehyde crosslinked galactomannan-collagen films. Carbohydr Polym 56: 313-320. https://doi.org/10.1016/j.carbpol.2004.01.011
  12. Friedman M. 2015. Chemistry and anticarcinogenic mechanisms of glycoalkaloids produced by eggplants, potatoes, and tomatoes. J Agric Food Chem 63: 3323-3337. https://doi.org/10.1021/acs.jafc.5b00818
  13. Galichet A, Sockalingum GD, Belarbi A, Manfait M. 2001. FTIR spectroscopic analysis of Saccharomyces cerevisiae cell walls: study of an anomalous strain exhibiting a pink-colored cell phenotype. FEMS Microbiol Lett 197: 179-186. https://doi.org/10.1111/j.1574-6968.2001.tb10601.x
  14. Gamar L, Blondeau K, Simonet JM. 1997. Physiological approach to extracellular polysaccharide production by Lactobacillus rhamnosus strain C83. J Appl Microbiol 83: 281-287. https://doi.org/10.1046/j.1365-2672.1997.00228.x
  15. Gonzaga MLC, Ricardo NMPS, Heatley F, Soares SDA. 2005. Isolation and characterization of polysaccharides from Agaricus blazei Murill. Carbohydr Polym 60: 43-49. https://doi.org/10.1016/j.carbpol.2004.11.022
  16. He L, Wu X, Cheng J, Li H, Lu X. 2010. Purification, composition analysis, and antioxidant activity of exopolysaccharides from mycelial culture of Paecilomyces cicadae (Miquel) Samson (Ascomycetes). Int J Med Mushrooms 12: 51-62. https://doi.org/10.1615/IntJMedMushr.v12.i1.50
  17. Hereher F, ElFallal A, Toson E, Abou-Dobara M, Abdelaziz M. 2018. Pilot study: tumor suppressive effect of crude polysaccharide substances extracted from some selected mushroom. Beni Seuf Univ J Basic Appl Sci 7: 767-775.
  18. Jagadeesh R, Babu G, Lakshmanan H, Oh OMJ, Jang JKY, Kong KWS, Raaman N. 2020. Bioactive sterol derivatives isolated from the Pleurotus djamor var. roseus induced apoptosis in cancer cell lines. Cardiovasc Hematol Agents Med Chem 18: 124-134. https://doi.org/10.2174/1871525718666200303123557
  19. Jegadeesh R, Lakshmanan H, Kab-Yeul J, Sabaratnam V, Raaman N. 2018. Cultivation of pink oyster mushroom Pleurotus djamor var. roseus on various agro-residues by low cost technique. J Mycopathol Res 56: 213-220.
  20. Kanagasabapathy G, Kuppusamy UR, Malek SNA, Abdulla MA, Chua KH, Sabaratnam V. 2012. Glucan-rich polysaccharides from Pleurotus sajor-caju (Fr.) Singer prevents glucose intolerance, insulin resistance, and inflammation in C57BL/6J mice fed a high-fat diet. BMC Complement Altern Med 12: 261. https://doi.org/10.1186/1472-6882-12-261
  21. Khan AA, Gani A, Shah A, Masoodi FA, Hussain PR, Wani IA, Khanday FA. 2015. Effect of γ-irradiation on structural, functional, and antioxidant properties of β-glucan extracted from button mushroom (Agaricus bisporus). Innov Food Sci Emerg Technol 31: 123-130. https://doi.org/10.1016/j.ifset.2015.05.006
  22. Khatua S, Paul S, Acharya, K. 2013. Mushroom as the potential source of new generation of antioxidant: a review. Res J Pharm Technol 6: 496-505.
  23. Li Z, Nie K, Wang Z, Luo D. 2016. Quantitative structure activity relationship models for the antioxidant activity of polysaccharides. PLoS One 11: e0163536. https://doi.org/10.1371/journal.pone.0163536
  24. Liu F, Ooi VEC, Chang ST. 1997. Free radical scavenging activity of mushroom polysaccharide extracts. Life Sci 60: 763-771. https://doi.org/10.1016/S0024-3205(97)00004-0
  25. Liu X, Wang L, Zhang C, Wang H, Zhang X, Li Y. 2015. Structure characterization and antitumor activity of a polysaccharide from the alkaline extract of king oyster mushroom. Carbohydr Polym 118: 101-106. https://doi.org/10.1016/j.carbpol.2014.10.058
  26. Meng X, Liang H, Luo L. 2016. Antitumor polysaccharides from mushrooms: a review on the structural characteristics, antitumor mechanisms, and immunomodulating activities. Carbohydr Res 424: 30-41. https://doi.org/10.1016/j.carres.2016.02.008
  27. Ozsoy N, Can A, Yanardag R, Akev N. 2008. Antioxidant activity of Smilax excelsa L.leaf extracts. Food Chem 110: 571-583. https://doi.org/10.1016/j.foodchem.2008.02.037
  28. Patel Y, Naraian R, Singh VK. 2012. Medicinal properties of Pleurotus species (oyster mushroom): a review. World Journal of Fungal Plant Biology 3: 1-12.
  29. Piska K, Sulkowksa-Ziaja K, Muszynska B. 2017. Edible mushroom Pleurotus ostreatus (oyster mushroom): its dietary significance and biological activity. Acta Scientiarum Polonorum Hortorum Cultus 16: 151-161. https://doi.org/10.24326/asphc.2017.3.15
  30. Radzki W, Ziaja-Soltys M, Nowak J, Rzymowska J, Topolska J, Slawinska A, Michalak-Majewska M, Zalewska-Korona M, Kuczumow A. 2016. Effect of processing on the content and biological activity of polysaccharides from Pleurotus ostreatus mushroom. Lebensm Wiss Technol 66: 27-33. https://doi.org/10.1016/j.lwt.2015.10.016
  31. Radzki W, Ziaja-Soltys M, Nowak J, Topolska J, Bogucka-Kocka A, Slawinska A, Michalak-Majewska M, Jablonska-Rys E, Kuczumow A. 2019. Impact of processing on polysaccharides obtained from button mushroom (Agaricus bisporus). Int J Food Sci Technol 54: 1405-1412. https://doi.org/10.1111/ijfs.14084
  32. Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24: 981-990. https://doi.org/10.1016/j.cellsig.2012.01.008
  33. Ren D, Jiao Y, Yang X, Yuan L, Guo J, Zhao Y. 2015. Antioxidant and antitumor effects of polysaccharides from Pleurotus abalonus. Chem Biol Interact 237: 166-174. https://doi.org/10.1016/j.cbi.2015.06.017
  34. Rodrigues Barbosa J, Dos Santos Freitas MM, da Silva Martins LH, de Carvalho RN. 2020. Polysaccharides of mushroom Pleurotus spp.: new extraction techniques, biological activities, and development of new technologies. Carbohydr Polym 229: 115550. https://doi.org/10.1016/j.carbpol.2019.115550
  35. Rop O, Mlcek J, Jurikova T. 2009. Beta-glucans in higher fungi and their health effects. Nutr Rev 67: 624-631. https://doi.org/10.1111/j.1753-4887.2009.00230.x
  36. Santos Arteiro JM, Rosario Martins M, Salvador C, Fatima Candeias M, Karmali A, Teresa Caldeira A. 2012. Protein-polysaccharides of Trametes versicolor: production and biological activities. Med Chem Res 21: 937-943. https://doi.org/10.1007/s00044-011-9604-6
  37. Seedevi P, Ganesan AR, Mohan K, Raguraman V, Sivakumar M, Sivasankar P, Loganathan S, Rajamalar P, Vairamani S, Shanmugam A. 2019. Chemical structure and biological properties of a polysaccharide isolated from Pleurotus sajorcaju. RSC Adv 9: 20472-20482. https://doi.org/10.1039/C9RA02977J
  38. Sermwittayawong D, Patninan K, Phothiphiphit S, Boonyarattanakalin S, Sermwittayawong N, Hutadilok-Towatana N. 2018. Purification, characterization, and biological activities of purified polysaccharides extracted from the gray oyster mushroom (Pleurotus sajor-caju (Fr.) Sing.]. J Food Biochem 42: e12606. https://doi.org/10.1111/jfbc.12606
  39. Singleton VL, Orthofer R, Lamuela-Raventos RM. 1999. [14] Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol 299: 152-178. https://doi.org/10.1016/S0076-6879(99)99017-1
  40. Siu KC, Chen X, Wu JY. 2014. Constituents actually responsible for the antioxidant activities of crude polysaccharides isolated from mushrooms. J Funct Foods 11: 548-556. https://doi.org/10.1016/j.jff.2014.08.012
  41. Socrates G. 2001. Infrared and Raman Characteristic Group Frequencies: Tables and Charts, 3rd ed. Wiley, Chichester, United Kingdom.
  42. Staub AM. 1965. Removal of protein: sevag method. Methods in Carbohydrate Chemistry 5: 5-6.
  43. Szwengiel A, Stachowiak B. 2016. Deproteinization of water-soluble β-glucan during acid extraction from fruiting bodies of Pleurotus ostreatus mushrooms. Carbohydr Polym 146: 310-319. https://doi.org/10.1016/j.carbpol.2016.03.015
  44. Uddin Pk MM, Islam MS, Pervin R, Dutta S, Talukder RI, Rahman M. 2019. Optimization of extraction of antioxidant polysaccharide from Pleurotus Ostreatus (Jacq.) P. Kumm and its cytotoxic activity against a murine lymphoid cancer cell line. PLoS One 14: e0209371. https://doi.org/10.1371/journal.pone.0209371
  45. Wiater A, Paduch R, Pleszczynska M, Prochniak K, Choma A, Kandefer-Szerszen M, Szczodrak J. 2011. α-(1 → 3)-D-glucans from fruiting bodies of selected macromycetes fungi and the biological activity of their carboxymethylated products. Biotechnol Lett 33: 787-795. https://doi.org/10.1007/s10529-010-0502-7
  46. Wong SM, Wong KK, Chiu LCM, Cheung PCK. 2007. Nonstarch polysaccharides from different developmental stages of Pleurotus tuber-regium inhibited the growth of human acute promyelocytic leukemia HL-60 cells by cell-cycle arrest and/or apoptotic induction. Carbohydr Polym 68: 206-217. https://doi.org/10.1016/j.carbpol.2006.12.018
  47. Xia F, Fan J, Zhu M, Tong H. 2011. Antioxidant effects of a water-soluble proteoglycan isolated from the fruiting bodies of Pleurotus ostreatus. J Taiwan Inst Chem Eng 42: 402-407. https://doi.org/10.1016/j.jtice.2010.08.012
  48. Zeng D, Zhu S. 2018. Purification, characterization, antioxidant, and anticancer activities of novel polysaccharides extracted from Bachu mushroom. Int J Biol Macromol 107: 1086-1092. https://doi.org/10.1016/j.ijbiomac.2017.09.088