Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Study on Immunostimulating Activity of Macrophage Treated with Purified Polysaccharides from Liquid Culture and Fruiting Body of Lentinus edodes

  • Lee, Hee-Hwan (Department of Bioengineering and Technology, Kangwon National University) ;
  • Lee, Jong-Seok (Department of Bioengineering and Technology, Kangwon National University) ;
  • Cho, Jae-Youl (School of Bioscience and Biotechnology, and Institute of Bioscience and Biotechnology, Kangwon National University) ;
  • Kim, Young-Eon (Korea Food Research Institute) ;
  • Hong, Eock-Kee (Department of Bioengineering and Technology, Kangwon National University)
  • Published : 2009.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Lentinus edodes is a well-known edible and medicinal mushroom used in Oriental cultures. Recently, L. edodes has attracted a lot of attention owing to its antifungal activity, antibacterial activity, antiviral activity, hepatoprotective effect, antitumor activities, and immunomodulatory and cytotoxic effects. In this study, the water-soluble crude polysaccharides, CPF and CPB, which were obtained from the fruiting body and culture cell-free broth of L. edodes by hot-water extraction and ethanol precipitation, were fractionated by DEAE cellulose and Sepharose CL-6B column chromatography, resulting in six polysaccharide fractions, CPFN-G-I, CPFN-G-II, CPFN-G-III, CPFA-G, CPBN-G, and CPBA-G Among these fractions, CPFN-G-I, CPBN-G, and CPBA-G were shown to stimulate the functional activation of macrophages including NO production, cytokine expression, and phagocytosis.

Keywords

References

  1. Baloch, Z., S. Cohen, and F. D. Coffman. Synergistic interactions between tumor necrosis factor and inhibitors of DNA topoisomerase I and II. J. Immunol. 145: 2908-2913
  2. Borchers, A. T., J. S. Stern, R. M. Hackman, C. L. Keen, and M. E. Gershwin. 1999. Mushrooms, tumors, and immunity. Proc. Soc. Exp. Biol. Med. 221: 281-293 https://doi.org/10.1046/j.1525-1373.1999.d01-86.x
  3. Bradford, M. M. 1976. A rapid and sensitive method for 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
  4. Bruneteau, M., I. Fabre, J. Perret, G. Michel, P. Ricci, J. P. Joseleau, et al. 1988. Antitumor active ${beta}$-D-glucans from Phytophthora parasitica. Carbohydr. Res. 175: 137-143 https://doi.org/10.1016/0008-6215(88)80164-2
  5. Carmichael, J., W. G. DeGraff, A. F. Gazdar, J. D. Minna, and J. B. Mitchell. 1987. Evaluation of a tetrazolium-based semiautomated colorimetric assay: Assessment of chemosensitivity testing. Cancer Res. 47: 936-942
  6. Chaplin, M. F. and J. F. Kennedy. 1986. Carbohydrate Chemistry. Oxford IRL Press
  7. Chihara, G., J. Hamuro, Y. Maeda, Y. Arai, and F. Fukuoka. 1970. Fractionation and purification of the polysaccharides with marked antitumor activity, especially lentinan, from Lentinus edodes (Berk.) Sing. (an edible mushroom). Cancer Res. 30:2776-2781
  8. Chihara, G., Y. Maeda, J. Hamuro, T. Sasaki, and F. Fumiko. 1969. Inhibition of mouse sarcoma 180 by polysaccharides from Lentinus edodes. Nature 222: 687-688 https://doi.org/10.1038/222687a0
  9. Cho, J. Y., K. U. Baik, J. H. Jung, and M. H. Park. 2000. In vitro anti-inflammatory effects of cynaropicrin, a sesquiterpene lactone, from Saussurea lappa. Eur. J. Pharmacol. 398: 399-407 https://doi.org/10.1016/S0014-2999(00)00337-X
  10. Collins, L., T. Zhu, J. Guo, Z. J. Xiao, and C. Y. Chen. 2006. Phellinus linteus sensitizes apoptosis induced by doxorubicin in prostate cancer. Br. J. Cancer 95: 282-288 https://doi.org/10.1038/sj.bjc.6603277
  11. Cui, S., J. S. Reichner, R. B. Mateo, and J. E. Albina. 1994. Activated murine macrophages induce apoptosis in tumor cells through nitric oxide-dependent or -independent mechanisms. Cancer Res. 54: 2462-2467
  12. Duperrier, K., A. Eljaafari, C. Dezutter-Dambuyant, C. Bardin, C. Jacquet, K. Yoneda, D. Schmitt, L. Gebuhrer, and D. Rigal. 2000. Distinct subsets of dendritic cells resembling dermal DCs can be generated in vitro from monocytes, in the presence of different serum supplements. J. Immunol. Methods 238: 119-131 https://doi.org/10.1016/S0022-1759(00)00147-2
  13. Farias Eisner, R., M. P. Sherman, E. Aeberhard, and G. Chaudhuri. 1994. Nitric oxide is an important mediator for tumoricidal activity in vivo. Proc. Natl. Acad. Sci. U.S.A. 91:9407-9411 https://doi.org/10.1073/pnas.91.20.9407
  14. Goossens, V., J. Grooten, K. De Vos, and W. Fiers. 1995. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc. Natl. Acad. Sci. U.S.A. 92: 8115-8119 https://doi.org/10.1073/pnas.92.18.8115
  15. Gregory, F. J., E. M. Healy, H. P. Agersborg Jr., and G. H. Warren. 1966. Studies on antitumor substances produced by Basidiomycetes. Mycologia 58: 80-90 https://doi.org/10.2307/3756990
  16. Griffith, T. S., S. R. Wiley, M. Z. Kubin, L. M. Sedger, C. R. Maliszewski, and N. A. Fanger. 1999. Monocyte-mediated tumoricidal activity via the tumor necrosis factor-related cytokine. J. Exp. Med. 189: 1343-1354 https://doi.org/10.1084/jem.189.8.1343
  17. Han, M. D., E. S. Lee, Y. K. Kim, J. W. Lee, H. Jeong, and K. H. Yoon. 1998. Production of nitric oxide in RAW264.7 macrophages treated with ganoderan, the ${\beta}$-glucan of Ganoderma lucidum. Kor. J. Mycol. 26: 246-255
  18. Hibbs Jr., J. B. 1976. The macrophage as a tumoricidal effector cell: A review of in vivo and in vitro studies on the mechanism of the activator macrophage nonspecific cytotoxic reactions. In:The Macrophage in Neoplasia. Academic Press, New York, pp.83-91
  19. Jung, Y. S., B. K. Yang, Y. T. Jeong, R. Islam, S. M. Kim, and C. H. Song. 2008. Immunomodulating activities of watersoluble exopolysaccharides obtained from submerged culture of Lentinus lepideus. J. Microbiol. Biotechnol. 18: 1431-1438
  20. Keller, R., M. Geiges, and R. Keist. 1990. L-Arginine-dependent reactive nitrogen intermediates as mediators of tumor cell killing by activated macrophages. Cancer Res. 50: 1421-1425
  21. Kiener, P. A., P. M. Davis, B. M. Rankin, S. J. Klebanoff, J. A. Ledbetter, G. C. Starling, and W. C. Liles. 1997. Human monocytic cells contain high levels of intracellular Fas ligand:Rapid release following cellular activation. J. Immunol. 159:1594-1598
  22. Kim, J. Y., S. E. Byeon, Y. G. Lee, Y. J. Lee, J. S. Park, E. K. Hong, and J. Y. Cho. 2008. Immunostimulatory activities of polysaccharides from liquid culture of pine-mushroom Tricholoma matsutake. J. Microbiol. Biotechnol. 18: 95-103
  23. Komatsu, N., S. Okubo, S. Kikumoto, K. Kimura, and G. Saito. 1969. Host-mediated antitumor action of schizophyllan, a glucan produced by Schizophyllum commune. Gann 60: 137-144
  24. Kroncke, K. D., K. Fehsel, and V. Kolb-Bachofen. 1995. Inducible nitric oxide synthase and its product nitric oxide, a small molecule with complex biological activities. Biol. Chem. Hoppe Seyler 376: 327-343
  25. Lee, B. W., G. H. Im, D. W. Kim, K. M. Park, S. H. Son, and T. H. Shon. 1993. Cultural characteristics and pilot scale fermentation for the submerged mycelial culture of Lentinus edodes. Kor. J. Appl. Microbiol. Biotechnol. 21: 609-614
  26. Lee, H. H., J. Y. Cho, and E. K. Hong. 2007. Exopolysaccharide production from liquid culture of Lentinus edodes. Kor. J. Biotechnol. Bioeng. 22:1-6
  27. Lorenzen, K. and T. Anke. 1998. Biologically active metabolites from basidiomycetes. Curr. Org. Chem. 2: 329-364
  28. Mackay, R. J. and S. W. Pussell. 1986. Protein changes associated with stages of activation of mouse macrophages for tumor cell killing. J. Immunol. 137: 1392-1398
  29. MacMicking, J., Q. W. Xie, and C. Nathan. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15: 323-350 https://doi.org/10.1146/annurev.immunol.15.1.323
  30. Monastra, G., A. Cabrelle, A. Zambon, A. Rosato, B. Macino, D. Collavo, and P. Zanovello. 1996. Membrane form of TNF alpha induces both cell lysis and apoptosis in susceptible target cells. Cell Immunol. 171: 102-110 https://doi.org/10.1006/cimm.1996.0179
  31. Nathan, C. F., S. C. Silrerstein, L. D. Bruker, and Z. A. Lohn. 1979. Extracellular cytolysis by activated macrophages and granulocytes. J. Exp. Med. 149: 100-113 https://doi.org/10.1084/jem.149.1.100
  32. Ng, T. B. and H. X. Wang. 2005. Pharmacological actions of Cordyceps, a prized folk medicine. J. Pharm. Pharmacol. 57:1509-1520 https://doi.org/10.1211/jpp.57.12.0001
  33. Ogura, T., M. Tatemichi, and H. Esumi. 1997. TNF-alpha mediates inducible nitric oxide synthase expression in human neuroblastoma cell line by cisplatin. Biochem. Biophys. Res. Commun. 233: 788-791 https://doi.org/10.1006/bbrc.1997.6558
  34. Ohno, N., Y. Adachi, I. Suzuki, K. Sato, S. Oikawa, and T. Yadomae. 1986. Characterization of the antitumor glucan obtained from liquid-cultured Grifola frondosa. Chem. Pharm. Bull. 34: 1709-1715
  35. Park, K. S. and B. N. Lee. 1997. Extraction and separation of protein-bound polysaccharide by Lentinus edodes. Kor. J. Food Nutr. 10: 503-508
  36. Roland, J. F., Z. F. Chmiolewicz, B. A. Weiner, A. M. Gross, O. P. Boening, J. V. Luck, et al. 1960. Calvacin: A new antitumor agent. Science 132: 1987
  37. Sasaki, T., N. Takasuka, G. Chihara, and Y. Y. Maeda. 1976. Antitumor activity of degraded products of lentinan: Its correlation with molecular weight. Gann 67: 191-195
  38. Shu, C. H., B. J. Wen, and K. J. Lin. 2003. Monitoring the polysaccharide quality of Agaricus blazei in submerged culture by examining molecular weight distribution and TNF-$\alpha$ release capability of macrophage cell line RAW264.7. Biotechnol. Lett. 25: 2061-2064 https://doi.org/10.1023/B:BILE.0000007066.00221.b9
  39. Smith, C. A., T. Davis, D. Anderson, L. Solam, M. P. Beckmann, R. Jerzy, S. K. Dower, D. Cosman, and R. G. Goodwin. 1990. A receptor for tumor necrosis factor defines an unusual family of cellular and viral proteins. Science 248:1019-1023 https://doi.org/10.1126/science.2160731
  40. Suffys, P., R. Beyaert, F. Van Roy, and W. Fiers. 1988. Involvement of a serine protease in tumour-necrosis-factormediated cytotoxicity. Eur. J. Biochem. 178: 257-265 https://doi.org/10.1111/j.1432-1033.1988.tb14451.x
  41. Takahashi, K., M. Yamazaki, and S. Abe. 1988. Local induction of a tumor necrosis factor (TNF)-like cytotoxic factor in murine tissues with tumorous and nontumorous inflammation after systemic administration of antitumor polysaccharides. J. Pharmacobiodynam. 11: 472-478 https://doi.org/10.1248/bpb1978.11.472
  42. Tsukagoshi, S. and F. Ophashi. 1974. Protein-bound polysaccharide preparation, PS-K, effective against mouse sarcoma-180 and rat ascites hepatoma AH-13 by oral use. Gann 65: 557-578
  43. Ukai, S., T. Kiho, C. Hara, M. Morita, A. Goto, N. Imazumi, and Y. Hasegawa. 1983. Polysaccharides in fungi. XIII. Antitumor activity of various polysaccharides isolated from Dictyophora indusiata, Ganoderma japonicum, Cordyceps cicadae, Auricularia auricular-judae, and Auricularia species. Chem. Pharm. Bull. 31: 741-744 https://doi.org/10.1248/cpb.31.741
  44. Ukawa, Y., H. Ito, and M. Hisamatsu. 2000. Antitumor effects of (1$\rightarrow$3)-$\beta$-D-glucan and (1$\rightarrow$6)-$\beta$-D-glucan purified from newly cultivated mushroom, Hatakeshimeji (Lyophyllum decastes Sing.). J. Biosci. Bioeng. 90: 98-104 https://doi.org/10.1016/S1389-1723(00)80041-9
  45. Wasser, P. D. 2002. Medicinal mushroom as a source of antitumor and immunomodulating polysaccharides. Appl. Microbiol. Biotech. 60: 258-274 https://doi.org/10.1007/s00253-002-1076-7
  46. Zheng, R., S. Jie, D. Hanchuan, and W. Moucheng. 2005. Characterization and immunomodulating activities of polysaccharide from Lentinus edodes. Int. Immunopharmacol. 5: 811-820 https://doi.org/10.1016/j.intimp.2004.11.011

Cited by

  1. Activation and stabilization of enzymes in ionic liquids vol.8, pp.13, 2009, https://doi.org/10.1039/b926130c
  2. 항보체 활성을 갖는 Phellinus linteus 균사체 생산의 최적화 vol.53, pp.3, 2009, https://doi.org/10.3839/jabc.2010.032
  3. Study of Macrophage Activation and Structural Characteristics of Purified Polysaccharide from the Fruiting Body of Cordyceps militaris vol.20, pp.7, 2009, https://doi.org/10.4014/jmb.0910.10022
  4. Automatic flow methodology for kinetic and inhibition studies of reactions with poorly water-soluble substrates in ionic liquid systems vol.690, pp.1, 2009, https://doi.org/10.1016/j.aca.2011.01.053
  5. Monolithic Phases for Ion Chromatography vol.4, pp.None, 2009, https://doi.org/10.1146/annurev-anchem-061010-113929
  6. Improvement of Thermostability and Activity of Firefly Luciferase Through [TMG][Ac] Ionic Liquid Mediator vol.168, pp.3, 2009, https://doi.org/10.1007/s12010-012-9803-8
  7. Glycosynthases as tools for the production of glycan analogs of natural products vol.29, pp.6, 2009, https://doi.org/10.1039/c2np20032e
  8. Antiproliferative Protein from the Culture Supernatant of Lentinula Edodes C91-3 Mycelia vol.62, pp.23, 2014, https://doi.org/10.1021/jf500316f
  9. UV-guided isolation of polyynes and polyenes from the roots of Codonopsis pilosula vol.5, pp.52, 2009, https://doi.org/10.1039/c5ra02765a
  10. In vivo anticancer and immunomodulating activities of mannogalactoglucan-type polysaccharides from Lentinus edodes (Berkeley) Singer vol.41, pp.1, 2009, https://doi.org/10.5114/ceji.2015.56962
  11. Detoxification of azo dyes by bacterial oxidoreductase enzymes vol.36, pp.4, 2016, https://doi.org/10.3109/07388551.2015.1004518
  12. A novel thermostable β-1,3-1,4-glucanase from Thermoascus aurantiacus and its application in oligosaccharide production from oat bran vol.469, pp.None, 2009, https://doi.org/10.1016/j.carres.2018.08.017
  13. Multi-omics analysis provides insights into lignocellulosic biomass degradation by Laetiporus sulphureus ATCC 52600 vol.14, pp.1, 2009, https://doi.org/10.1186/s13068-021-01945-7