Abstract
β-Glucan isolated from cell wall of fungi not only has low purity and yield, but also causes adverse effects. Consequently, extracellular β-glucan produced by microorganisms is the focus of this study. β-Glucan-rich exopolysaccharides (G-EPSs) with different molecular weights from Paenibacillus polymyxa JB115 were prepared by ultrafiltration and spray-drying. The weight-average molecular masses of the G-EPSs, P-SD-1 (spray-dried G-EPSs powder prepared below 100 kDa) and P-SD-2 (spray-dried G-EPSs powder prepared above 100 kDa), were 7.084×104 and 9.235×105 g/mol, respectively. β-Glucan content was 47.38% in P-SD-1 and 73.12% in P-SD-2. The hydroxyl radical- and superoxide radicalscavenging activities of P-SD-2 at 1 mg/mL (39.45 and 87.34%, respectively) were higher than those of P-SD-1 (30.32 and 53.06%, respectively). Maximal nitric oxide (22.24±1.34 μM) was generated in the presence of P-SD-2 (1 mg/mL) and the antitumor activity of P-SD-2 was higher than P-SD-1 in four tumor cell lines (HeLa, Sarcoma 180, A549, and Hep3B cells). Thus, antioxidant and antitumor activities could be enhanced by regulating the molecular weight of G-EPSs. We anticipate that the food and medicinal use of G-EPSs will follow further characterization of this class of exopolysaccharides.
Similar content being viewed by others
References
Adachi Y, Ohno N, Ohsawa M, Oikawa S, and Yadomae T (1990) Change of biological activities of (1–3)-β-d-glucan from Grifola frondosa upon molecular weight reduction by heat treatment. Chem Pharm Bull 38, 477–481.
Ahn SG, Suh HH, Lee CH, Moon SH, Kim SH, Ahn KH et al. (1998) Isolation and characterization of a novel polysaccharide producing Bacillus polymyxa A49 KCTC 4648P. J Microbiol Biotechnol 8, 171–177.
Chao D, Zhun H, Haitian F, Minghua H, **n X, and **ghua C (2012) Chemical analysis and antioxidant activity in vitro of a β-d-glucan isolated from Dictyophora indusiata. Int J Biol Macromol 51, 70–75.
Chen J, Da W, Zhang D, Liu Q, and Kang J (2005). Water-soluble antioxidants improve the antioxidant and anticancer activity of low concentrations of curcumin in human leukemia cells. Pharmazie 60, 57–61.
Cleary JA, Kelly G, and Husband AJ (1999) The effect of molecular weight and β-1,6-linkages on priming of macrophage function in mice by (1,3)-β-d-glucan. Immunol Cell Biol 77, 395–403.
Cohen G and Heikkila RE (1974) The generation of hydrogen peroxide, superoxide radical, and hydroxyl radical by 6-hydroxydopamine, dialuric acid, and related cytotoxic agents. J Biol Chem 25, 2447–2452.
Cui S, Reichner JS, Mateo RB, and Albina JE (1994). Activated murine macrophages induce apoptosis in tumor cells through nitric oxidedependent or-independent mechanisms. Cancer Res 54, 2462–2467.
Dore GC, Azevedo TG, Souza MR, Rego LA, Dantas JCM, Silva FRF et al. (2007) Antiinflammatory, antioxidant and cytotoxic actions of β-glucanrich extract from Geastrum saccatum mushroom. Int Immunopharmacol 7, 1160–1169.
Gummadi SN and Kumar K (2005) Production of extracellular water insoluble β-1,3-glucan(curdlan) from Bacillus sp. SNC07. Biotechnol Bioprocess Eng 10, 546–551.
Hong JH and Choi YH (2007) Physicochemical properties of protein bound polysaccharide from Agaricus blazei Murill prepared by ultrafiltration and spray drying process. Int J Food Sci Tech 42, 1–8.
Hong JH, Kim SJ, Pogaku R, and Youn KS (2007) Antitumor activities of spray-dried powders with different molecular masses fractionated from the crude protein-bound polysaccharide extract of Agaricus blazei Murill. Food Sci Biotechnol 16, 600–604.
Huang Q, Zhang L, Cheung PCK, and Tan X (2006) Evaluation of sulfated α-glucans from Poria cocos mycelia as potential antitumor agent. Carbohydr Polym 64, 337–344.
Hwang HJ, Kim SW, Choi JW, and Yun JW (2003) Production and characterization of exopolysaccharides from submerged culture of Phellinus linteus KCTC 6190. Enzyme Microb Technol 33, 309–319.
Im SA, Kim KJ, and Lee CK (2006) Immunomodulatory activity of polysaccharide isolated form Salicornia herbacea. Int Immunopharmacol 6, 1451–1458.
Ishibashi KI, Miura NN, Adachi Y, Ohno N, and Yadomae T (2001) Relationship between solubility of grifolan, a fungal 1, 3-β-d-glucan, and production of tumor necrosis factor by macrophages in vitro. Biosci biotechnol biochem 65, 1993–2000.
Jung HK, Hong JH, Park SC, Park BK, Nam DH, and Kim SD (2007) Production and physicochemical characterization of β-glucan produced by Paenibacillus polymyxa JB115. Biotechnol Bioprocess Eng 12, 713–719.
Jung HK, Park SC, Park BK, and Hong JH (2008) Physiological activities of a β-glucan produced by Paenibacillus polymyxa. Biotechnol Lett 30, 1545–1551.
Kim MK, Lee IY, Ko JH, Rhee YH, and Park YH (1999) Higher intracellular levels of uridinemonophosphate under nitrogen-limited conditions enhance metabolic flux of curdlan synthesis in Agrobacterium species. Biotechnol Bioeng 62, 317–323.
Kimura Y, Sumiyoshi M, Suzuki T, and Sakanaka M (2006) Antitumor and antimetastatic activity of a novel water-soluble low molecular weight β-1,3-d-glucan (branch β-1,6) isolated from Aureobasidium pullulans 1A1 strain black yeast. Anticancer res, 26, 4131–4141.
Kofuji K, Aoki A, Tsubaki K, Konishi M, Isobe T, and Murata Y (2012) Antioxidant activity of β-glucan. ISRN Phamaceutics. doi: 10.5402/2012/125864.
Krakowski L, Krzyzanowski J, Wrona Z, and Siwicki AK (1999) The effect of nonspecific immunostimulation of pregnant mares with 1,3/1,6 glucan and levamisole on the immunoglobulin levels in colostrums, selected indices of nonspecific cellular and humoral immunity in foals in neonatal and postnatal period. Vet Immunol Immnopathol 68, 1–11.
Kulicke WM, Lettau AI, and Thielking H (1997) Correlation between immunological activity, molar mass, and molecular structure of different (1→3)-β-d-glucans. Carbohyd Res 297, 135–143.
Kupfahl C, Geginat G, and Hof H (2006) Lentinan has a stimulatory effect on innate and adaptive immunity against murin Listeria monocytihenes infection. Int Immunopharmacol 6, 686–696.
Lee KY, Lee MH, Chang IY, Yoon SP, Lim DY, and Jeon YJ (2006) Macrophage activation by polysaccharide fraction isolated from Salicornia herbacea. J Ethnopharmacol 103, 372–378.
Lee SJ, Lee YB, Hong JH, Chung JH, Kim SS, Lee WJ et al. (2005) Optimization of pine flavor microencapsulation by spray drying. Food Sci Biotechnol 14, 747–751.
Leung MYK, Fung KP, and Choy YM (1997) The isolation and characterization of an immunomodulatory and antitumor polysaccharide preparation from Flammulina velutipes. Immunopharmacology 35, 255–263.
Leung MYK, Liu C, Koon JCM, and Fung KP (2006) Polysaccharide biological response modifiers. Immunol Lett 105, 101–114.
Li XM, Li XL, and Zhou AG (2007) Evaluation of antioxidant activity of the polysaccharides extracted form Lycium barbarum fruits in vitro. Eur Polym J 43, 488–497.
Lin X, C YJ, Li ZX, Chen O, Liu ZL, and Wang R (2003) Structure determination, apoptosis induction, and telomerase inhibition of CFP-2, a novel lichenin from Cladonia furcata. Biochimica et Biophysica Acta. 1622, 99–108.
Lin Y, Zhang L, Chen L, ** Y, Zeng F, ** J et al. (2004) Molecular mass and antitumor activities of sulfated derivatives of α-glucan from Poria cocos mycelia. Int J Biol Macromol 34, 231–236.
Liu J, Luo J, Ye H, Sun Y, Lu Z, and Zen X (2009) Production, characterization and antioxidant activities in vitro of exopolysaccharides from endophytic bacterium Paenibacillus polymyxa EJS-3. Carbohydr Polym 78, 275–281.
Liu** F, **wei L, Kequan D, and Lianzhong A (2012) Effects of drying methods on the antioxidant activities of polysaccharides extracted from Ganoderma lucidum. Carbohydr Polym 87, 1849–1854.
Ljungma AG, Leanderson P, and Tagesson C (1998) β(1→2)(1→3)-d-glucan stimulated nitric oxide generation and cytokine mRNA expression in macrophages. Environ Toxicol Phar 5, 273–281.
Lowry OH, Rosebrough NJ, Farr AL, and Randall RJ (1951). Protein measurement with the Folin-phenol reagents. J Biol Chem 193, 265–275.
Madden JK, Dea ICM, and Steer DC (1986) Structural and rheological properties of the extracellular polysaccharides from Bacillus polymyxa. Carbohydr Polym 6, 51–73.
Marian R, Anusuya N, Siddhyraju P, and Manian S (2008) The antioxidant activity and free radical of Camellia sinensis (L.) O. Kuntz, Ficus bengalensis L. and Ficus racemosa L. Food Chem 107, 1000–1007.
Mau JL, Lin HC, and Song SF (2002) Antioxidant properties of several specialty mushrooms. Food Res Int 35, 519–526.
McCleary BV and Holmes MG (1985) Enzymatic quantification of (1–3),(1–4) β-glucan in barley and malt. J Inst Brew 91, 285–295.
Mizuno T, Hagiwara T, Nakamura T, Ito H, Shimura K, Sumiya T et al. (1990) Antitumor activity and some properties of water-soluble polysaccharides from “Himematsutake”, the fruiting body of Agaricus blazei Murill. Agric Biol Chem 54, 2889–2896.
Mulder M (1991) In Basic principle of membrane technology: Membrane processes (2nd ed). Kluwer Academic Publishers, USA.
Nair R, Melinick S, Ramachandra R, Escalon E, and Ramachandran C (2006) Mechanism of macrophage activation by (1,4)-α-d-glucan isolated from Tonospora cordifolia. Int Immunopharmacol 6, 1815–1824.
Ohno N, Miura NN, Chiba N, Adachi Y, and Yadomae T (1995) Comparison of the immunopharmacological activities of triple and single-helical Schizophyllan in mice. Biol Pharm Bull 18, 1242–1247.
Patel S and Goyal A (2012) Recent developments in mushrooms as anticancer therapeutics: a review. 3 Biotech 2, 1–15.
Pelicano H, Carney D, and Huang P (2004) ROS stress in cancer cells and therapeutic implications. Drug Resist Updates 7, 97–110.
Qi HM, Zhang QB, Zhao TT, Chen R, Zhang H, and Niu XZ (2005) Antioxidant activity of different sulfate content derivatives of polysaccharide extracted from Ulva pertusa (Chlorophyra) in vitro. Int J Biol Macromol 37, 195–199.
Ratti C (2001) Hot air and freeze-drying of high value foods: a review. J Food Eng 49, 311–319.
Saha SK and Brewer CF (1994) Determination of the concentrations of oligosaccharides, complex type carbohydrates, and glyco-proteins using the phenol-sulfuric acid method. Carbohydr Res 254, 157–167.
Schepetkin IA and Quinn MT (2006). Botanical polysaccharides: macrophage immunomodulation and therapeutic potential. Int Immunopharmacol, 6, 317–333.
Tsiapali E, Whaley S, Kalbfleisch J, Ensley HE, Browder IW, and Williams DL (2001) Glucans exhibit weak antioxidant activity, but stimulate macrophage free radical activity. Free Radical Bio Med 30, 393–402.
Wang Y, Zhang L, Li Y, Hou X, and Zeng F (2004) Correlation of structure to antitumor activities of five derivatives of a β-glucan from Poria cocos sclerotium. Carbohydr Res 339, 2567–2574.
Wilson TA, Nicolosi RJ, Delaney B, Chadwell K, Moolchandani V, Kotyla T et al. (2004) Reduced and high molecular weight barley β-glucans decrease plasma total and non-HDL-cholesterol in hypercholesterolemic Syrian golden hamsters. J Nutr 134, 2617–2622.
**e G, Schepetkin IA, Siemsen DW, Kirpotina LN, Wiley JA, and Quinn MT (2008). Fractionation and characterization of biologically-active polysaccharides from Artemisia tripartita. Phytochemistry, 69, 1359–1371
Zhang M, Cui SW, Cheung PCK and Wang Q (2007) Antitumor polysaccharides from mushrooms: a review on their isolation process, structural characteristics and antitumor activity. Trends Food Sci Tech 18, 4–19.
Zhang L, Li X, Xu X, and Zeng F (2005) Correlation between antitumor activity, molecular weight, and conformation of lentinan. Carbohyd Res 340, 1515–1521.
Zhang P, Zhang L, and Cheng S (1999) Chemical structure and molecular weight of (1→3)-α-d-glucan from Lentinus edodes. Biosci Biotechnol Biochem 63, 1197–1202.
Zhang Z, Wang F, Wang X, Liu X, Hou Y, and Zhang Q (2010) Extraction of the polysaccharides from five algae and their potential antioxidant activity in vitro. Carbohydr Polym 82, 118–121.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hong, JH., Jung, H.K. Antioxidant and antitumor activities of β-glucan-rich exopolysaccharides with different molecular weight from Paenibacillus polymyxa JB115. J Korean Soc Appl Biol Chem 57, 105–112 (2014). https://doi.org/10.1007/s13765-013-4252-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13765-013-4252-9