Dietary polysaccharide extracts of Agaricus brasiliensis fruiting bodies: Chemical characterization and bioactivities at different levels of purification

Food Research International

Volumn 64, Issue , 2014, Pages 53-64

  Kozarski, Maja ^a   Klaus, Anita ^a   Jakovljevic, Dragica ^b   Todorovic, Nina ^b   Niksic, Miomir ^a   Vrvic, Miroslav M ^b,c   Van Griensven, Leo J L D ^d  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b UNIVERSITY OF BELGRADE   (Serbia)

^c UNIVERSITY OF BELGRADE   (Serbia)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

A. brasiliensis; Antioxidant activity; EPR spin trapping; Immunomodulation; Polysaccharide extracts

Indexed keywords

BIOACTIVITY; ELECTRON SPIN RESONANCE SPECTROSCOPY; ETHANOL; EXTRACTION; FREE RADICALS; POLYSACCHARIDES; PURIFICATION; WATER;

A. BRASILIENSIS; AGARICUS BRASILIENSIS; ANTI OXIDATIVE ACTIVITY; ANTI-OXIDANT ACTIVITIES; ANTIOXIDATIVE PROPERTY; CHEMICAL CHARACTERIZATION; IMMUNO MODULATIONS; SPIN TRAPPING; FRUITING BODIES;

ANTIOXIDANTS;

EID: 84903193477     PISSN: 09639969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodres.2014.05.075     Document Type: Article

References (91)

1. Ali S.H. The world of β-glucans - A review of biological roles, applications and potential areas of research. Thesis for the requirement of Master of Science-Medical Biology 2009, 45. Institute of Medical Biology, Faculty of Medicine University of Tromsø, Norway.
2. Bogdanovic Pristov J., Mitrovic A., Spasojevic I. A comparative study of antioxidative activities of cell-wall polysaccharides. Carbohydrate Research 2011, 346:2255-2259.
3. Bouike G., Nishitani Y., Shiomi H., Yoshida M., Azuma T., Hashimoto T., et al. Oral treatment with extract of Agaricus blazei Murill enhanced Th1 response through intestinal epithelial cells and suppressed OVA-sensitized allergy in mice. Evidence-based complementary and alternative medicine 2011, 11. (Article ID 532180).
4. Bradford M.M. A refined and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-255.
5. Camelini C.M., Maraschin M., Matos de Mendonc M., Zucco C., Ferreira A.G., Tavares L.A. Structural characterization of b-glucans of Agaricus brasiliensis in different, stages of fruiting body maturity and their use in nutraceutical products. Biotechnology Letters 2005, 27:1295-1299.
6. Cao W., Li X.Q., Liu L., Yang T.H., Li C., Fan H.T., et al. Structure of an anti-tumor polysaccharide from Angelica sinensis (Oliv.) Diels. Carbohydrate Polymers 2006, 66:149-159.
7. Chan G.C.-F., Chan W.K., Sze D.M.-Y. The effects of β-glucan on human immune and cancer cells. Journal of Hematology & Oncology 2009, 2:25.
8. Cho S.M., Jang K.Y., Park H.J., Park J.S. Analysis of the chemical constituents of Agaricus brasiliensis. Mycobiology 2008, 36:50-54.
9. Cipriani T.R., Mellinger C.G., de Souza L.M., Baggio C.H., Freitas C.S., Marques M.C., et al. A polysaccharide from a tea (infusion) of Maytenus ilicifolia leaves with anti-ulcer protective effects. Journal of Natural Products 2006, 69:1018-1021.
10. Ciucanu I., Kerek F. A simple and rapid method for the permethylation of carbohydrates. Carbohydrate Research 1984, 131:209-217.
11. Coppens P., da Silva M.F., Pettman S. European regulations on nutraceuticals, dietary supplements and functional foods: A framework based on safety. Toxicology 2006, 221:59-74.
12. Cui W., Eskin N.A.M., Biliaderis C.G. NMR characterization of a water-soluble 1,4-linked β-d-glucan having ether groups from yellow mustard (Sinapis N.A.M. L.) mucilage. Carbohydrate Polymers 1995, 27:117-122.
13. Cui L., Sun Y., Xu H., Xu H., Cong H., Liu J. A polysaccharide isolated from Agaricus blazei Murill (ABP-AW1) as a potential Th1 immunity-stimulating adjuvant. Oncology Letters 2013, 6:1039-1044.
14. Dixon R.A., Paiva N.L. Stress-induced phenylpropanoid metabolism. The Plant Cell 1995, 7:1085-1097.
15. Du Bois M., Gilles K.A., Hamilton J.K., Rebers P.A., Smith F. Colorimetric method for determination of sugars and related substances. Analytical Chemistry 1956, 28:350-356.
16. Freimund S., Sauter M., Käppeli O., Dutler H. A new non-degrading isolation process for 1,3-β-d-glucan of high purity from baker's yeast Saccharomyces cerevisiae. Carbohydrate Polymers 2003, 54:159-171.
17. Fry S.C. Oxidative coupling of tyrosine and ferulic acid residues: Intra- and extra-protoplasmic occurrence, predominance of trimers and larger products, and possible role in inter-polymeric cross-linking. Phytochemistry Reviews 2004, 3:97-111.
18. Giavasis I. Bioactive fungal polysaccharides as potential functional ingredients in food and nutraceuticals. Current Opinion in Biotechnology 2014, 26:162-173.
19. Gill S.K., Rieder M.J. Toxicity of a traditional Chinese medicine, Ganoderma lucidum, in children with cancer. The Canadian Journal of Clinical Pharmacology 2008, 15:275-285.
20. Gonzaga M.L.C., Ricardo N.M.P.S., Heatley F., Soares S. Isolation and characterization of polysaccharides from Agaricus blazei Murill. Carbohydrate Polymers 2005, 60:43-49.
21. Gow N.A.R., Netea M.G., Munro C.A., Ferwerda G., Bates S., Mora-Montes H.M., et al. Immune recognition of Candida albicans β-glucan by dectin-1. The Journal of Infectious Diseases 2007, 196:1565-1571.
22. Guo Q., Zhao B., Shen S., Hou J., Hu J., Xin W. ESR study on the structure-antioxidant activity relationship of tea catechins and their epimers. Biochimica et Biophysica Acta 1999, 1427:13-23.
23. Hausenloy D.J., Yellon D.M. Time to take myocardial reperfusion injury seriously. The New England Journal of Medicine 2008, 359:518-520.
24. - fluxes in seawater. Analytica Chimica Acta 2010, 667:1-13.
25. Ho C.Y., Lau C.B.S., Kim C.F., Leung K.N., Fung K.P., Tse T.F., et al. Differential effect of Coriolus versicolor (Yunzhi) extract on cytokine production by murine lymphocytes in vitro. International Immunopharmacology 2004, 4:1549-1557.
26. Hong F., Yan J., Baran J.T., Allendorf D.J., Hansen R.D., Ostroff G.R., et al. Mechanism by which orally administered β-1,3-glucans enhance the tumoricidal activity of antitumor monoclonal antibodies in murine tumor models. Journal of Immunology 2004, 173:797-806.
27. Hsu T.L., Cheng S.C., Yang W.B., Chin S.W., Chen B.H., Huang M.T., et al. Profiling carbohydrate-receptor interaction with recombinant innate immunity receptor-Fc fusion proteins. Journal of Biological Chemistry 2009, 284:34479-34489.
28. Ikekawa T. Beneficial effects of edible and medicinal mushrooms on health care. International Journal of Medicinal Mushrooms 2001, 3:291-298.
29. Ismail A., Marjan Z.M., Foong C.W. Total antioxidant activity and phenolic content in selected vegetables. Food Chemistry 2004, 87:581-586.
30. Jicheng L., Chunjing Z., Yajun W., Haitao Y., Han L., Liping W., et al. Structural elucidation of a heteroglycan from the fruiting bodies of Agaricus blazei Murill. International Journal of Biological Macromolecules 2011, 49:716-720.
31. Kato M., Neil T.K., Fearnley D.B., McLellan A.D., Vuckovic S., Hart D.N.J. Expression of multilectin receptors and comparative FITC-dextran uptake by human dendritic cells. International Immunology 2000, 12:1511-1519.
32. Kawagishi H., Inagaki R., Kanao T., Mizuno T. Fraction and antitumor activity of the water-insoluble residue of Agaricus blazei fruiting bodies. Carbohydrate Research 1989, 186:267-273.
33. Kawai R., Igarashi K., Yoshida M., Kitaoka M., Samejima M. Hydrolysis of beta-1,3/1,6-glucan by glycoside hydrolase family 16 endo-1,3(4)-beta-glucanase from the basidiomycete Phanerochaete chrysosporium. Applied Microbiology and Biotechnology 2006, 71:898-906.
34. Ker Y.B., Chen K.C., Chyau C.C., Chen C.C., Guo J.H., Hsien C.L., et al. Antioxidant capability of polysaccharides fractionated from submerge-cultured Agaricus blazei Mycelia. Journal of Agricultural and Food Chemistry 2005, 53:7052-7058.
35. Keservani R.K., Kesharwani R.K., Vyas N., Jain S., Raghuvanshi R., Sharma A.K. Nutraceutical and functional food as future food: A review. Der Pharmacia Lettre 2010, 2:106-116.
36. Kishk Y.F.M., Al-Sayed H.M.A. Free-radical scavenging and antioxidative activities of some polysaccharides in emulsions. Lwt-food science and technology (Lebensmittel-Wissenschaft und Technologie) 2007, 40:270-277.
37. Klaus A., Kozarski M., Niksic M. The influence of bioactive compounds extracted from mushroom Agaricus blazei on Jurkat cells. Hrana i ishrana 2009, 50:14-17.
38. Klaus A., Kozarski M., Niksic M., Jakovljevic D., Todorovic N., Stefanoska I., et al. The edible mushroom Laetiporus sulphureus as potential source of natural antioxidants. International Journal of Food Sciences and Nutrition 2013, 64:599-610.
39. Klaus A., Kozarski M., Niksic M., Jakovljevic D., Todorovic N., Van Griensven L.J.L.D. Antioxidative activities and chemical characterization of polysaccharides extracted from the basidiomycete Schizophyllum commune. Lwt-food science and technology (Lebensmittel-Wissenschaft und Technologie) 2011, 44:2005-2011.
40. Kovacik J., Klejdus B. Dynamics of phenolic acids and lignin accumulation in metaltreated Matricaria chamomilla roots. Plant Cell Reports 2008, 27:605-615.
41. Kozarski M. Chemical characterization, antioxidative and antimicrobial properties of polysaccharide extracts from the selected mushroom species 2012, 210. Doctoral dissertation, Faculty of Chemistry, University of Belgrade, Serbia.
42. Kozarski M., Klaus A., Niksic M., Jakovljevic D., Helsper J.P.F.G., Van Griensven L.J.L.D. Antioxidative and immunomodulating activities of polysaccharide extracts of the medicinal mushrooms Agaricus bisporus, Agaricus brasiliensis, Ganoderma lucidum and Phellinus linteus. Food Chemistry 2011, 129:1667-1675.
43. Kozarski M.S., Klaus A.S., Niksic M.P., van Griensven L.J.L.D., Vrvic M.M., Jakovljevic D.M. Polysaccharides of higher fungi: Biological role, structure, and antioxidative activity. Chemical Industry 2014, (in press). 10.2298/hemind121114056k.
44. Kozarski M., Klaus A., Niksic M., Vrvic M.M., Todorovic N., Jakovljevic D., et al. Antioxidative activities and chemical characterization of polysaccharide extracts from the widely used mushrooms Ganoderma applanatum, Ganoderma lucidum, Lentinus edodes and Trametes versicolor. Journal of Food Composition and Analysis 2012, 26:144-153.
45. Laplace J.P. Health and nutrition claims made on food: What future? [article in French]. Bulletin de l Academie Nationale de Medecine (Paris) 2006, 190:1663-1680.
46. Laroche C., Michaud P. New developments and prospective applications for β (1,3) glucans. Recent Patents on Biotechnology 2007, 1:59-73.
47. Laugier O.B., Spasic S.D., Mandic V., Jakovljevic D., Vrvic M.M. The effects of repetitive alkaline/acid extractions of Saccharomyces cerevisiae cell wall on antioxidative and bifidogenic efficacy. International Journal of Food Science and Technology 2012, 47:369-375.
48. Lavi I., Friesem D., Geresh S., Hadar Y., Schwartz B. An aqueous polysaccharide extract from the edible mushroom Pleurotus ostreatus induces anti-proliferative and pro-apoptotic effects on HT-29 colon cancer cells. Cancer Letters 2006, 244:61-70.
49. Lehtovaara B.C., Gu F.X. Pharmacological, structural, and drug delivery properties and applications of 1,3-β-glucans. Journal of Agricultural and Food Chemistry 2011, 59:6813-6828.
50. Li J., Feng Z.H., Li G.Y., Mou D.L., Nie Q.H. Expression of dendritic cell-specific intercellular adhesion molecule 3 grabbing nonintegrin on dendritic cells generated from human peripheral blood monocytes. World Journal of Gastroenterology 2006, 12:453-456.
51. Lo T.C.-T., Chang C.A., Chiuc K.-H., Tsayd P.-K., Jena J.-F. Correlation evaluation of antioxidant properties on the monosaccharide components and glycosyl linkages of polysaccharide with different measuring methods. Carbohydrate Polymers 2011, 86:320-327.
52. Lockwood G.B. The quality of commercially available nutraceutical supplements and food sources. Journal of Pharmacy and Pharmacology 2011, 63:3-10.
53. Mandel S., Packer L., Youdim M.B.H., Weinreb O. Reviews: Current topics. Proceedings from the "Third International Conference on Mechanism of Action of Nutraceuticals". The Journal of Nutritional Biochemistry 2005, 16:513-520.
54. McCleary B.V., Prosky L. Advanced dietary fibre technology 2001, Blackwell Science, Oxford; Malden, MA, (Xxv, 534 pp.).
55. Mizuno T., Inagaki R., Kanao T., Hagiwara T., Nakamura T., Ito H., et al. Antitumor activity and some properties of waterinsoluble hetero-glycans from "Himematsutake", the fruiting body of Agaricus blazei Murill. Agricultural and Biological Chemistry 1990, 54:2897-2905.
56. Mizuno M., Morimoto M., Minato K., Tsuchida H. Polysaccharides from Agaricus blazei stimulate lymphocyte T-cell subsets in mice. Bioscience, Biotechnology, and Biochemistry 1998, 62:434-437.
57. Nakamura T., Matsugo S., Uzuka Y., Matsuo S., Kawagishi H. Fractionation and anti-tumor activity of the mycelia of liquid-cultured Phellinus linteus. Bioscience, Biotechology and Biochemistry 2004, 68:868-872.
58. Navegantes K.C., Albuquerque R.F.V., Dalla-Santa H.S., Soccol C.R., Monteiro M.C. Agaricus brasiliensis mycelium and its polysaccharide modulate the parameters of innate and adaptive immunity. Food and Agricultural Immunology 2013, 24:393-408.
59. Needs P.W., Selvendran R.R. Avoiding oxidative degradation during sodium hydroxide/methyl iodide-mediated carbohydrate methylation in dimethyl sulfoxide. Carbohydrate Research 1993, 245:1-10.
60. Ohno N., Furukawa M., Miura N.N., Adachi Y., Motoi M., Yadomae T. Antitumor β-glucan from the cultured fruit body of A. blazei. Biological and Pharmaceutical Bulletin 2001, 24:820-828.
61. Pericolini E., Cenci E., Monari C., De Jesus M., Bistoni F., Casadevall A., et al. Cryptococcus neoformans capsular polysaccharide component galactoxylomannan induces apoptosis of human T-cells through activation of caspase-8. Cellular Microbiology 2006, 8:267-275.
62. Pramanik M., Chakraborty I., Mondol S., Islam S.S. Stuctural analysis of a water-soluble glucan (Fr.I) of an edible mushroom, Pleurotus sajor-caju. Carbohydrate Research 2007, 342:2670-2675.
63. Pramanik M., Mondal S., Chakraborty I., Rout D., Islam S.S. Structural investigation of a polysaccharide (Fr. II) isolated from the aqueous extract of an edible mushroom, Pleurotus sajor-caju. Carbohydrate Research 2005, 340:629-636.
64. Rice P.J., Adams E.L., Ozment-Skelton T., Gonzalez A.J., Goldman M.P., Lockhart B.E., et al. Oral delivery and gastrointestinal absorption of soluble glucans stimulate increased resistance to infectious challenge. The Journal of Pharmacology and Experimental Therapeutics 2005, 314:1079-1086.
65. Sambou T., Dinadayala P., Stadthagen G., Barilone N., Bordat Y., Constant P., et al. Capsular glucan and intracellular glycogen of Mycobacterium tuberculosis: Biosynthesis and impact on the persistence in mice. Molecular Microbiology 2008, 70:762-774.
66. + T cells regulates the mucosal immune responses to Citrobacter rodentium infection. Infection and Immunity 2010, 78:2653-2666.
67. Silvestein R.M., Bassler G.C., Morrill T.C. Spectrometric identification of organic compounds 1994, Wiley, New York. 5th ed.
68. Smiderle F.R., Alquini G., Tadra-Sfeir M.Z., Iacomini M., Wichers H.J., Van Griensven L.J.L.D. Agaricus bisporus and Agaricus brasiliensis (1→6)-β-d-Glucans show immunostimulatory activity on human THP-1 derived macrophages. Carbohydrate Polymers 2013, 94:91-99.
69. Smiderle F.R., Ruthes A.C., van Arkel J., Chanput W., Iacomini M., Wichers H.J., et al. Polysaccharides from Agaricus bisporus and Agaricus brasiliensis show similarities in their structures and their immunomodulatory effects on human monocytic THP-1 cells. BMC Complementary and Alternative Medicine 2011, 11:58.
70. Smiderle F.R., Sassaki G.L., Van Arkel J., Iacomini M., Wichers H.J., Van Griensven L.J.L.D. High molecular weight of the culinary mushroom Agaricus bisporus is an α-glucan that forms complexes with low molecular weight galactan. Molecules 2010, 15:5818-5830.
71. Smith J.E., Rowan N.J., Sullivan R. Medicinal mushrooms: A rapidly developing area of biotechnology for cancer therapy and other bioactivities. Biotechnology Letters 2002, 24:1839-1845.
72. Song W., Helsper J.P.F.G., Van Griensven L.J.L.D. Phenolic compounds present in medicinal mushroom extracts generate reactive oxygen species in human cells in vitro. International Journal of Medicinal Mushrooms 2008, 10:1-13.
73. Sousa Cardozo F.T.G., Camelini C.M., Mascarello A., Rossi M.J., Nunes R.J., Monte Barardi C.R., et al. Antiherpetic activity of a sulfated polysaccharide from Agaricus brasiliensis mycelia. Antiviral Research 2011, 92:108-114.
74. Størseth T.R., Kirkvold S., Skjermoa J., Reitana K.I. A branched β-d-(1→3,1→6)-glucan from the marine diatom Chaetoceros debilis (Bacillariophyceae) characterized by NMR. Carbohydrate Research 2006, 341:2108-2114.
75. Subbiah M.T. Nutrigenetics and nutraceuticals: The next wave riding on personalized medicine. Translational Research 2007, 149:55-61.
76. Takeda T., Shimizu N., Watanabe S., Edagawa Y., Ito Y., Naraui T., et al. Further studies on the structure of polysaccharides from the lichen. Chemical and Pharmaceutical Bulletin 2003, 51:1436-1438.
77. Tsukagoshi S., Hashimoto Y., Fujii G., Kobayashi H., Nomoto K., Orita K. Krestin (PSK). Cancer Treatment Reviews 1984, 11:131-155.
78. Uyanoglu M., Canbek M., van Griensven L.J., Yamac M., Senturk H., Kartkaya K., et al. Effects of polysaccharide from fruiting bodies of Agaricus bisporus, Agaricus brasiliensis, and Phellinus linteus on alcoholic liver injury. International Journal of Food Science and Nutrition 2014, 65:482-488.
79. Van de Loosdrecht A.A., Beelen R.H., Ossenkoppele G.J., Broekhoven M.G., Langenhuijsen M.M. A tetrazolium-based colorimetric MTT assay to quantitate human monocyte mediated cytotoxicity against leukemic cells from cell lines and patients with acute myeloid leukemia. Journal of Immunological Methods 1994, 14:311-320.
80. Van Griensven L.J.L.D., Verhoeven H.A. Phellinus linteus polysaccharide extracts increase the mitochondrial membrane potential and cause apoptotic death of THP-1 monocytes. Chinese Medicine 2013, 8:25.
81. Van der Aar A.M.G., Gringhuis S.I., Geijtenbeek T.B.H. Innate recognition of HIV-1 glycans: Implications for infection, transmission, and immunity in HIV glycans in infection and immunity 2014, Springer, (217 pp.). R. Pantophlet (Ed.).
82. Wasser S.P. Medicinal mushrooms as a source of antitumor and immunomodulating polysaccharides. Applied Microbiology and Biotechnology 2002, 60:258-274.
83. Wasser S.P. Medicinal mushroom science: History, current status, future trends, and unsolved problems. International Journal of Medicinal Mushrooms 2010, 12:1-16.
84. Wasser S.P., Nevo E., Sokolov D., Reshetnikov S., Timor-Tismenetsky M. Dietary supplements from medicinal mushrooms: Diversity of types and variety of regulations. International Journal of Medicinal Mushrooms 2000, 2:1-19.
85. Wiater A., Paduch R., Pleszczynska M., Prochniak K., Choma A., Kandefer-Szerszen M., et al. α-(1→3)-d-Glucans from fruiting bodies of selected macromycetes fungi and the biological activity of their carboxymethylated products. Biotechnology Letters 2011, 33:787-795.
86. Wong D.W.S. Feruloyl esterase: A key enzyme in biomass degradation. Applied Biochemistry and Biotechnology 2006, 133:87-112.
87. Wu B., Cui J., Zhang C., Li Z. A polysaccharide from Agaricus blazei inhibits proliferation and promotes apoptosis of osteosarcoma cells. International Journal of Biological Macromolecules 2012, 50:1116-1120.
88. Yang Y., Ye L.B., Zhang J.S., Liu Y.F., Tang Q.J. Structural analysis of a bioactive polysaccharide, PISP1, from the medicinal mushroom Phellinus igniarius. Bioscience, Biotechnology, and Biochemistry 2009, 73:134-139.
89. 13C-labelled yeast-cell wall beta-glucan oligosaccharides. Journal of Biomolecular NMR 1993, 3:429-441.
90. Zhang S., He B., Ge J., Zhai C., Liu X., Liu P. Characterization of chemical composition of Agaricus brasiliensis polysaccharides and its effect on myocardial SOD activity, MDA and caspase-3 level in ischemia-reperfusion rats. International Journal of Biological Macromolecules 2010, 46:363-366.
91. Zhang W., Wang L.Z., Yu J.T., Chi Z.F., Tan L. Increased expressions of TLR2 and TLR4 on peripheral blood mononuclear cells from patients with Alzheimer's disease. Journal of Neurological Sciences 2012, 315:67-71.