DOI QR코드

DOI QR Code

Phagocytic Effects of β-Glucans from the Mushroom Coriolus versicolor are Related to Dectin-1, NOS, TNF-α Signaling in Macrophages

  • Jang, Seon-A (Department of Herbal Medicine Resource, Kangwon National University) ;
  • Kang, Se-Chan (Department of Natural Medicine Resources, Semyung University) ;
  • Sohn, Eun-Hwa (Department of Herbal Medicine Resource, Kangwon National University)
  • Received : 2011.06.29
  • Accepted : 2011.08.03
  • Published : 2011.10.30

Abstract

The mushroom Coriolus versicolor contains biologically active polysaccharides, most of which belong to the ${\beta}$-glucan group. Diverse physicochemical properties, due to different sources and isolated types of ${\beta}$-glucans, can induce distinct biological activities. We investigated the effects of ${\beta}$-glucans from C. versicolor on phagocytic activity, nitric oxide (NO), TNF-${\alpha}$ production, and signaling of dectin-1, a well-known ${\beta}$-glucan receptor, in macrophages. ${\beta}$-Glucans increased phagocytic activity and TNF-${\alpha}$ and NO-iNOS/eNOS production. Laminarin, a specific inhibitor of dectin-1, showed strong inhibitory effects on phagocytosis and subsequent TNF-${\alpha}$, iNOS, and eNOS production increased by ${\beta}$-glucans, indicating that ${\beta}$-glucans reacts with dectin-1 receptors. We examined whether the aforementioned cytokines were involved in the signaling pathway from the dectin-1 receptor to phagocytosis, and found that the inhibition of iNOS, eNOS, and TNF-${\alpha}$ receptors significantly decreased ${\beta}$-glucan-induced phagocytosis. In conclusion, our study showed that dectin-1 signaling, triggered by ${\beta}$-glucans, subsequently elicited TNF-${\alpha}$ and NO-iNOS/eNOS production, and that these molecules seem to act as secondary molecules that cause eventual phagocytosis by macrophages. These findings suggest that C. versicolor could be used as a nutritional medicine that may be useful in the treatment of infectious disease.

Keywords

References

  1. Adams, D. O. and Hamilton, T. A. (1984) The cell biology of macrophage activation. Ann. Rev. Immunol. 2, 283-318. https://doi.org/10.1146/annurev.iy.02.040184.001435
  2. Akerman, S., Williamson, D. J., Kaube, H. and Goadsby, P. J. (2002) Nitric oxide synthase inhibitors can antagonize neurogenic and calcitonin gene-related peptide induced dilation of dural meningeal vessels. Br. J. Pharmacol.137, 62-68. https://doi.org/10.1038/sj.bjp.0704842
  3. Akramiene, D., Kondrotas, A., Didziapetriene, J. and Kevelaitis, E. (2007) Effects of beta-glucans on the immune system. Medicina 43, 597-606.
  4. Bredt, D. S. and Snyder, S. H. (1994) Nitric oxide: a physiologic messenger molecule. Annu. Rev. Biochem. 63, 175-195. https://doi.org/10.1146/annurev.bi.63.070194.001135
  5. Brown, G. D., Herre, J., Williams, D. L., Willment, J. A., Marshall, A. S. and Gordon, S. (2003) Dectin-1 mediates the biological effects of $\beta$-glucan. J. Exp. Med. 197, 1119-1124. https://doi.org/10.1084/jem.20021890
  6. Brown, G. D., Taylor, P. R., Reid, D. M., Willment, J. A., Williams, D. L., Martinez-Pomares, L., Wong, S. Y. and Gordon, S. (2002) Dectin-1 is a major beta-glucan receptor on macrophages. J. Exp. Med. 196, 407-412. https://doi.org/10.1084/jem.20020470
  7. Cook, J. A., Holbrook, T. W. and Dougherty, W. J. (1982) Protective effect of glucan against visceral leishmaniasis in hamsters. Infect. Immun. 37, 1261-1269.
  8. Di Luzio, N. R., Williams, D. L., McNamee, R. B., Edwards, B. F. and Kitahama, A. (1979) Comparative tumor-inhibitory and anti-bacterial activity of soluble and particulate glucan. Int. J. Cancer 24, 773-779. https://doi.org/10.1002/ijc.2910240613
  9. Ding, A. H., Nathan, C. F. and Stuehr, D. J. (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141, 2407-2412.
  10. Gantner, B. N., Simmons, R. M., Canavera, S. J., Akira, S. and Underhill, D. M. (2003) Collaborative induction of infl ammatory responses by dectin-1 and Toll-like receptor. J. Exp. Med. 197, 1107-1117. https://doi.org/10.1084/jem.20021787
  11. Gersuk, G. M., Underhill, D. M., Zhu, L. and Marr, K. A. (2006) Dectin-1 and TLRs permit macrophages to distinguish between different Aspergillus fumigatus cellular states. J. Immunol. 176, 3717-3724. https://doi.org/10.4049/jimmunol.176.6.3717
  12. Hahn, H. and Kaufmann, S. H. (1981) The role of cell-mediated immunity in bacterial infections. Rev. Infect. Dis. 3, 1221-1250. https://doi.org/10.1093/clinids/3.6.1221
  13. Ho, C. Y., Kim, C. F., Leung, K. N., Fung, K. P., Tse, T. F., Chan, H. and Lau, C. B. (2005) Differential anti-tumor activity of Coriolus versicolor (Yunzhi) extract through p53- and/or Bcl-2-dependent apoptotic pathway in human breast cancer cells. Cancer. Biol. Ther. 4, 638-644. https://doi.org/10.4161/cbt.4.6.1721
  14. Imura, H., Ohno, N., Suzuki, I. and Yadomae, T. (1985) Purifi cation, antitumor activity, and structural characterization of $\beta$-1,3-glucan from Peziza vesiculosa. Chem. Pharm. Bull. 33, 5096-5099. https://doi.org/10.1248/cpb.33.5096
  15. Itoh, W., Sugawara, I., Kimura, S., Tabata, K., Hirata, A., Kojima, T., Mori, S. and Shuimada, K. (1990) Immunopharmacological study of sulfated schizophyllan (SPG) I. Its action as a mitogen and anti- HIV agent. Int. J. Immunopharmacol. 12, 225-233. https://doi.org/10.1016/0192-0561(90)90057-T
  16. Janeway, C. A. and Medzhitov, R. (2002) Innate immune recognition. Annu. Rev. Immunol. 20, 197-216. https://doi.org/10.1146/annurev.immunol.20.083001.084359
  17. Jang, S. A., Park, S, Lim, J. D., Kang, C. H., Yang, K. H., Pyo, S. and Sohn, E. H. (2009) The comparative Immunomodulatory effects of β-glucans from yeast, bacteria, and mushroom on the function of macrophages. J. Food. Sci. Nutr. 14, 102-108. https://doi.org/10.3746/jfn.2009.14.2.102
  18. Kidd, P. M. (2000) The use of mushroom glucans and proteoglycans in cancer treatment. Altern. Med. Rev. 5, 4-27.
  19. Keller, R. and Keist, R. (1989) Abilities of activated macrophages to manifest tumoricidal activity and to generate reactive nitrogen intermediates: a comparative study in vitro and ex vivo. Biochem. Biophys. Res. Commun. 164, 968-973. https://doi.org/10.1016/0006-291X(89)91764-6
  20. Kokoshis, P. L., Williams, D. L., Cook, J. A. and Di Luzio, N. R. (1978) Increased resistance to Staphylococcus aureus infection and enhancement in serum lysozyme activity by glucan. Science 199, 1340-1342. https://doi.org/10.1126/science.628841
  21. Kroncke, K. D., Fehsel, K. and Kolb-Bachofen, V. (1997) Nitric oxide: cytotoxicity versus cytoprotection: how, why, when and where? Nitric Oxide 1, 107-120. https://doi.org/10.1006/niox.1997.0118
  22. Muller, A., Rice, P. J., Ensley, H. E., Coogan, P. S., Kalbfl eisch, J. H., Kelley, J. L., Love, E. J., Portera, C. A., Ha, T., Browder, I. W. and Williams, D. L. (1996) Receptor binding and internalization of water-soluble (1$\rightarrow$3)-beta-D-glucan biologic response modifi er in two monocyte/macrophage cell lines. J. Immunol. 156, 3418-3425.
  23. Murray, R. Z., Kay, J. G., Sangermani, D. G. and Stow, J. L. (2005) A role for the phagosome in cytokine secretion. Science 310, 1492-1495. https://doi.org/10.1126/science.1120225
  24. Nathan, C. F. (1987) Secretory products of macrophage. J. Clin. Invest. 79, 319-326. https://doi.org/10.1172/JCI112815
  25. Okimura, T., Ogawa, M. and Yamauchi, T. (1986) Stress and immune responses. III. Effect of resistant stress on delayed type hypersensitivity (DTH) response, natural killer (NK) activity and phagocytosis in mice. Jpn. J. Pharmacol. 41, 229-235. https://doi.org/10.1254/jjp.41.229
  26. Rickard, N. S., Gibbs, M. E. and Ng, K. T. (1999) Inhibition of the endothelial isoform of nitric oxide synthase impairs long-term memory formation in the chick. Learn Mem. 6, 458-466. https://doi.org/10.1101/lm.6.5.458
  27. Ross, G. D. (2000) Regulation of the adhesion versus cytotoxic functions of the Mac-1/CR3/alphaMbeta2-integrin glycoprotein. Crit. Rev. Immunol. 20, 197-222.
  28. Rogers, N. C., Slack, E. C., Edwards, A. D., Nolte, M. A., Schulz, O., Schweighoffer, E., Williams, D. L., Gordon, S., Tybulewicz, V. L. and Brown, G. D. (2005) Syk-dependent cytokine induction by dectin- 1 reveals a novel pattern recognition pathway for C-type lectins. Immunity 22, 507-517. https://doi.org/10.1016/j.immuni.2005.03.004
  29. Saijo, S., Fujikado, N., Furuta, T., Chung, S. H., Kotaki, H., Seki, K., Sudo, K., Akira, S., Adachi, Y., Ohno, N., Kinjo, T., Nakamura, K., Kawakami, K. and lwakura, Y. (2007) Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat. Immunol. 8, 39-46. https://doi.org/10.1038/ni1425
  30. Steele, C., Marrero, L., Swain, S., Harmsen, A. G., Zheng, M., Brown, G. D., Gordon, S., Shellito, J. E. and Kolls, J. K. (2003) Alveolar macrophage-mediated killing of Pneumocystis carinii f. sp. muris involves molecular recognition by the dectin-1$\beta$-glucan receptor. J. Exp. Med. 198, 1677-1688. https://doi.org/10.1084/jem.20030932
  31. Taylor, P. R., Brown, G. D., Reid, D. M., Willment, J. A., Martinez-Pomares, L., Gordon, S. and Wong, S. Y. (2002) The $\beta$-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J. Immunol. 169, 3876-3882. https://doi.org/10.4049/jimmunol.169.7.3876
  32. Taylor, P. R., Tsoni, S. V., Willment, J. A., Dennehy, K. M., Rosas, M., Findon, H., Haynes, K., Steele, C., Botto, M., Gordon, S. and Brown, G. D. (2007) Dectin-1 is required for $\beta$-glucan recognition and control of fungal infection. Nat. Immunol. 8, 31-38. https://doi.org/10.1038/ni1408
  33. Tipoe, G. L., Leung, T. M., Liong, E., So, H., Leung, K. M., Lau, T. Y., Tom, W. M., Fung, M. L., Fan, S.T. and Nanji, A. A. (2006) Inhibitors of inducible nitric oxide (NO) synthase are more effective than an NO donor in reducing carbon-tetrachloride induced acute liver injury. Histol. Histopathol. 21, 1157-1165.
  34. Uthaisangsook, S., Day, N. K., Bahna, S. L., Good, R. A. and Haraguchi, S. (2002) Innate immunity and its role against infections. Ann. Allergy. Asthma Immunol. 88, 253-264. https://doi.org/10.1016/S1081-1206(10)62005-4
  35. Van der Graaf, C. A. A., Netea, M. G., Verschueren, I., van der Meer, J. W. and Kullberg, B. J. (2005) Differential cytokine production and Toll-like receptor signaling pathways by Candida albicans blastoconidia and hyphae. Infect. Immun. 73, 7458-7464. https://doi.org/10.1128/IAI.73.11.7458-7464.2005
  36. Verstovsek, S., Maccubbin, D. and Mihich, E. (1992) Tumoricidal activation of murine resident peritoneal macrohages by interleukin 2 and tumor necrosis factor. Cancer Res. 52, 3880-3885.
  37. Williams, D. L., Cook, J. A., Hoffmann, E. O. and Di Luzio, N. R. (1978) Protective effect of glucan in experimentally induced candidiasis. J. Reticulocndothelial. Soc. 23, 479-490.
  38. Williams, D. L., Pretus, H. A. and Browder, I. W. (1992) Application of aqueous gel permeation chromatography with in-line multi-angle laser light scattering and differential viscometry detectors for the characterization of natural product carbohydrate pharmaceuticals. J. Liq. Chromatogr. 15, 2297-2309. https://doi.org/10.1080/10826079208016179
  39. Willment, J. A., Marshall, A. S. J., Reid, D. M., Williams, D. L., Wong, S. Y., Gordon, S. and Brown. G. D. (2005) The human $\beta$-glucan receptor is widely expressed and functionally equivalent to murine dectin-1 on primary cells. Eur. J. Immunol. 35, 1539-1547. https://doi.org/10.1002/eji.200425725
  40. Yadomae, T. (2000) Structure and biological activities of fungal $\beta$-1,3- glucans. Yakugaku. Zasshi. 120, 413-431.

Cited by

  1. Purification, characterization, and antitumor activity of a novel glucan from the fruiting bodies of Coriolus Versicolor vol.12, pp.2, 2017, https://doi.org/10.1371/journal.pone.0171270
  2. Effects of β-glucans from Coriolus versicolor on macrophage phagocytosis are related to the Akt and CK2/Ikaros vol.57, 2013, https://doi.org/10.1016/j.ijbiomac.2013.03.017
  3. 8-(Tosylamino)quinoline inhibits macrophage-mediated inflammation by suppressing NF-κB signaling vol.33, pp.8, 2012, https://doi.org/10.1038/aps.2012.52
  4. β-glucans from Coriolus versicolor protect mice against S. typhimurium challenge by activation of macrophages vol.86, 2016, https://doi.org/10.1016/j.ijbiomac.2016.01.058
  5. Immunomodulatory Properties of Filamentous Fungi Cultivated through Solid-State Fermentation on Rapeseed Meal vol.182, pp.3, 2017, https://doi.org/10.1007/s12010-016-2370-7
  6. HangAmDan-B, an Ethnomedicinal Herbal Mixture, Suppresses Inflammatory Responses by Inhibiting Syk/NF-κB and JNK/ATF-2 Pathways vol.16, pp.1, 2013, https://doi.org/10.1089/jmf.2012.2374
  7. 20S-dihydroprotopanaxatriol modulates functional activation of monocytes and macrophages vol.37, pp.3, 2013, https://doi.org/10.5142/jgr.2013.37.300
  8. Yarrowia lipolytica N6-glucan protects goat leukocytes against Escherichia coli by enhancing phagocytosis and immune signaling pathway genes vol.150, pp.None, 2011, https://doi.org/10.1016/j.micpath.2021.104735
  9. Botryosphaeran, [(1 → 3)(1 → 6)-β-D-glucan], induces apoptosis-like death in promastigotes of Leishmania amazonensis, and exerts a leishmanicidal effect on infected macrophages by activating NF vol.351, pp.None, 2011, https://doi.org/10.1016/j.cbi.2021.109713