Abstract
Mushroom polysaccharides are potent substances that exhibit antitumor and immunomodulatory properties. Studies comparing the chemical composition and antitumor-related activities of polysaccharides released by fungal strains under different growth conditions are not available. Thus, the present study compared polysaccharides extracts produced by Pleurotus pulmonarius from mycelium grown in liquid culture (ME) or fruiting bodies (FBE). Polysaccharides of both ME and FBE had a relatively high molecular mass. NMR spectroscopy indicated that ME glucan is an α-glucan whereas FBE glucan is a mixture of both α- and β-glucans. Glucose and galactose where the most prominent monosaccharide in both glucans. Treatment of several colon cancer cell lines expressing varying amounts of galectin-3 with the two fungal glucans inhibited their viability and significantly reduced their ability to adhere to the key component of the extracellular matrix, fibronectin, and to a human umbilical vein endothelial cell monolayer, in a time- and dose-dependent manner mainly in those cell lines expressing high amounts of galectin-3. We conclude that ME and FBE glucans may exert a direct antiproliferative effect on cancer cells expressing high galectin-3 concentrations and concomitantly downregulate tumor cell adherence, the latter being directly related to cancer progression and metastasis.
Similar content being viewed by others
References
Adachi Y, Okazaki M, Ohno N, Yadomae T (1994) Enhancement of cytokine production by macrophages stimulated with (1– > 3)-β-d-glucan, grifolan (GRN), isolated from Grifola frondosa. Biol Pharm Bull 17:1554–1560
Berry G (1966) Thermodynamic and conformational properties of polystyrene. I. Light-scattering studies on dilute solutions of linear polystyrenes. J Chem Phys 44:4550
Beuth J, Ko HL, Schirrmacher V, Uhlenbruck G, Pulverer G (1988) Inhibition of liver tumor cell colonization in two animal tumor models by lectin blocking with D-galactose or arabinogalactan. Clin Exp Metastasis 6:115–120
Borchers AT, Keen CL, Gershwin ME (2004) Mushrooms, tumors, and immunity: an update. Exp Biol Med (Maywood) 229:393–406
Chen W, Zhao Z, Chen SF, Li YQ (2008) Optimization for the production of exopolysaccharide from Fomes fomentarius in submerged culture and its antitumor effect in vitro. Bioresour Technol 99:3187–3194
Chihara G (1992) Recent progress in immunopharmacology and therapeutic effects of polysaccharides. Dev Biol Stand 77:191–197
Dallas SL, Chen Q, Sivakumar P (2006) Dynamics of assembly and reorganization of extracellular matrix proteins. Curr Top Dev Biol 75:1–24
Gao QP, Jiang RZ, Chen HQ, Jensen E, Seljelid R (1996) Characterization and cytokine stimulating activities of heteroglycans from Tremella fuciformis. Planta Med 62:297–302
Glinsky GV, Mossine VV, Price JE, Bielenberg D, Glinsky VV, Ananthaswamy HN, Feather MS (1996) Inhibition of colony formation in agarose of metastatic human breast carcinoma and melanoma cells by synthetic glycoamine analogs. Clin Exp Metastasis 14:253–267
Gutierrez A, Prieto A, Martinez AT (1996) Structural characterization of extracellular polysaccharides produced by fungi from the genus Pleurotus. Carbohydr Res 281:143–154
Hadar Y, Cohen-Arazi E (1986) Chemical composition of the edible mushroom Pleurotus ostreatus produced by fermentation. Appl Environ Microbiol 51:1352–1354
Ho JC, Konerding MA, Gaumann A, Groth M, Liu WK (2004) Fungal polysaccharopeptide inhibits tumor angiogenesis and tumor growth in mice. Life Sci 75:1343–1356
Honjo Y, Nangia-Makker P, Inohara H, Raz A (2001) Down-regulation of galectin-3 suppresses tumorigenicity of human breast carcinoma cells. Clin Cancer Res 7:661–668
Honjo Y, Inohara H, Akahani S, Yoshii T, Takenaka Y, Yoshida J, Hattori K, Tomiyama Y, Raz A, Kubo T (2000) Expression of cytoplasmic galectin-3 as a prognostic marker in tongue carcinoma. Clin Cancer Res 6:4635–4640.
Hu SH, Wang JC, Lien JL, Liaw ET, Lee MY (2006) Antihyperglycemic effect of polysaccharide from fermented broth of Pleurotus citrinopileatus. Appl Microbiol Biotechnol 70:107–113
Inufusa H, Nakamura M, Adachi T, Aga M, Kurimoto M, Nakatani Y, Wakano T, Miyake M, Okuno K, Shiozaki H, Yasutomi M (2001) Role of galectin-3 in adenocarcinoma liver metastasis. Int J Oncol 19:913–919
Kiho T, Yoshida I, Katsuragawa M, Sakushima M, Usui S, Ukai S (1994) Polysaccharides in fungi. XXXIV. A polysaccharide from the fruiting bodies of Amanita muscaria and the antitumor activity of its carboxymethylated product. Biol Pharm Bull 17:1460–1462
Kodama N, Yamada M, Nanba H (2001) Addition of Maitake D-fraction reduces the effective dosage of vancomycin for the treatment of Listeria-infected mice. Jpn J Pharmacol 87:327–332
Kuster B, Wheeler SF, Hunter AP, Dwek RA, Harvey DJ (1997) Sequencing of N-linked oligosaccharides directly from protein gels: in-gel deglycosylation followed by matrix-assisted laser desorption/ionization mass spectrometry and normal-phase high-performance liquid chromatography. Anal Biochem 250:82–101
Lavi I, Friesem D, Geresh S, Hadar Y, Schwartz B (2006) An aqueous polysaccharide extract from the edible mushroom Pleurotus ostreatus induces anti-proliferative and pro-apoptotic effects on HT-29 colon cancer cells. Cancer Lett 244:61–70
Lavi I, Levinson D, Peri I, Nimri L, Hadar Y, Schwartz B (2009) Orally administered glucans from the edible mushroom Pleurotus pulmonarius reduce acute inflammation in dextran sulfate sodium-induced experimental colitis. Br J Nutr Sep 22:1–10
Lee YW, Eum SY, Chen KC, Hennig B, Toborek M (2004) Gene expression profile in interleukin-4-stimulated human vascular endothelial cells. Mol Med 10:19–27
Li G, Kim DH, Kim TD, Park BJ, Park HD, Park JI, Na MK, Kim HC, Hong ND, Lim K, Hwang BD, Yoon WH (2004) Protein-bound polysaccharide from Phellinus linteus induces G2/M phase arrest and apoptosis in SW480 human colon cancer cells. Cancer Lett 216:175–181
Mizuno M, Minato K, Ito H, Kawade M, Terai H, Tsuchida H (1999) Anti-tumor polysaccharide from the mycelium of liquid-cultured Agaricus blazei mill. Biochem Mol Biol Int 47:707–714
Nangia-Makker P, Hogan V, Honjo Y, Baccarini S, Tait L, Bresalier R, Raz A (2002) Inhibition of human cancer cell growth and metastasis in nude mice by oral intake of modified citrus pectin. J Natl Cancer Inst 94:1854–1862
Petrova RD, Mahajna J, Reznick AZ, Wasser SP, Denchev CM, Nevo E (2007) Fungal substances as modulators of NF-κΒ activation pathway. Mol Biol Rep 34:145–154
Rice PJ, Adams EL, Ozment-Skelton T, Gonzalez AJ, Goldman MP, Lockhart BE, Barker LA, Breuel KF, Deponti WK, Kalbfleisch JH, Ensley HE, Brown GD, Gordon S, Williams DL (2005) Oral delivery and gastrointestinal absorption of soluble glucans stimulate increased resistance to infectious challenge. J Pharmacol Exp Ther 314:1079–1086
Rosado FR, Germano S, Carbonero ER, Da Costa SM, Iacomini M, Kemmelmeier C (2003) Biomass and exopolysaccharide production in submerged cultures of Pleurotus ostreatoroseus Sing. and Pleurotus ostreatus “florid” (Jack.: Fr.) Kummer. J Basic Microbiol 43:230–237
Rout D, Mondal S, Chakraborty I, Pramanik M, Islam SS (2005) Chemical analysis of a new (1– > 3)-, (1– > 6)-branched glucan from an edible mushroom, Pleurotus florida. Carbohydr Res 340:2533–2539
Saito H, Ohki T, Yoshioka Y, Fukuoka F (1976) A 13C nuclear magnetic resonance study of a gel-forming branched (1 leads to 3)-β-d-glucan, A3, from Pleurotus ostreatus (Fr.) Quel: determination of side-chains and conformation of the polymer-chain in relation to gel-structure. FEBS Lett 68:15–18
Sarangi I, Ghosh D, Bhutia SK, Mallick SK, Maiti TK (2006) Anti-tumor and immunomodulating effects of Pleurotus ostreatus mycelia-derived proteoglycans. Int Immunopharmacol 6:1287–1297
Schwartz B, Bresalier RS, Kim YS (1992) The role of mucin in colon-cancer metastasis. Int J Cancer 52:60–65
Tao Y, Zhang L, Cheung PC (2006) Physicochemical properties and antitumor activities of water-soluble native and sulfated hyperbranched mushroom polysaccharides. Carbohydr Res 341:2261–2269
Valent BS, Darvill AG, McNeil M, Robertsen BK, Albersheim P (1980) A general and sensitive chemical method for sequencing the glycosyl residues of complex carbohydrates. Carbohydr Res 79:165–192
Wasser SP (2002) Medicinal mushrooms as a source of antitumor and immunomodulating polysaccharides. Appl Microbiol Biotechnol 60:258–274
Wasser SP, Weis AL (1999) Therapeutic effects of substances occurring in higher Basidiomycetes mushrooms: a modern perspective. Crit Rev Immunol 19:65–96
Xie JT, Wang CZ, Wicks S, Yin JJ, Kong J, Li J, Li YC, Yuan CS (2006) Ganoderma lucidum extract inhibits proliferation of SW 480 human colorectal cancer cells. Exp Oncol 28:25–29
Yoshida I, Kiho T, Usui S, Sakushima M, Ukai S (1996) Polysaccharides in fungi. XXXVII. Immunomodulating activities of carboxymethylated derivatives of linear (1– > 3)-α-d-glucans extracted from the fruiting bodies of Agrocybe cylindracea and Amanita muscaria. Biol Pharm Bull 19:114–121
Yoshioka Y, Tabeta R, Saito H, Uehara N, Fukuoka F (1985) Antitumor polysaccharides from (Fr.) Quel.: isolation and structure of a β-glucan. Carbohydr Res 140:93–100
Zaidman BZ, Yassin M, Mahajna J, Wasser SP (2005) Medicinal mushroom modulators of molecular targets as cancer therapeutics. Appl Microbiol Biotechnol 67:453–468
Zhang M, Cheung PC, Zhang L (2001) Evaluation of mushroom dietary fiber (nonstarch polysaccharides) from sclerotia of Pleurotus tuber-regium (Fries) singer as a potential antitumor agent. J Agric Food Chem 49:5059–5062
Zhou X, Lin J, Yin Y, Zhao J, Sun X, Tang K (2007) Ganodermataceae: natural products and their related pharmacological functions. Am J Chin Med 35:559–574
Zusman I, Reifen R, Livni O, Smirnoff P, Gurevich P, Sandler B, Nyska A, Gal R, Tendler Y, Madar Z (1997) Role of apoptosis, proliferating cell nuclear antigen and p53 protein in chemically induced colon cancer in rats fed corncob fiber treated with the fungus Pleurotus ostreatus. Anticancer Res 17:2105–2113
Author information
Authors and Affiliations
Corresponding author
Additional information
This study was partially supported by a Grant from the “Yissum Research Development Company of the Hebrew University of Jerusalem.”
Rights and permissions
About this article
Cite this article
Lavi, I., Levinson, D., Peri, I. et al. Chemical characterization, antiproliferative and antiadhesive properties of polysaccharides extracted from Pleurotus pulmonarius mycelium and fruiting bodies. Appl Microbiol Biotechnol 85, 1977–1990 (2010). https://doi.org/10.1007/s00253-009-2296-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-009-2296-x