DOI QR코드

DOI QR Code

Agrocybe chaxingu polysaccharide prevent inflammation through the inhibition of COX-2 and NO production

  • Lee, Byung-Ryong (Departments of Biomedical Science and Research Institute for Bioscience and Biotechnology, College of Medicine, Hallym University) ;
  • Kim, So-Young (Departments of Biomedical Science and Research Institute for Bioscience and Biotechnology, College of Medicine, Hallym University) ;
  • Kim, Dae-Won (Departments of Biomedical Science and Research Institute for Bioscience and Biotechnology, College of Medicine, Hallym University) ;
  • An, Jae-Jin (Departments of Biomedical Science and Research Institute for Bioscience and Biotechnology, College of Medicine, Hallym University) ;
  • Song, Ha-Yong (Departments of Biomedical Science and Research Institute for Bioscience and Biotechnology, College of Medicine, Hallym University) ;
  • Yoo, Ki-Yeon (Departments of Anatomy and Neurobiology, College of Medicine, Hallym University) ;
  • Kang, Tae-Cheon (Departments of Anatomy and Neurobiology, College of Medicine, Hallym University) ;
  • Won, Moo-Ho (Departments of Anatomy and Neurobiology, College of Medicine, Hallym University) ;
  • Lee, Kwang-Jae (Gangwon Agricultural Research & Extention Services) ;
  • Kim, Kyung-Hee (Gangwon Agricultural Research & Extention Services) ;
  • Joo, Jin-Ho (Department of Biological Environment, Kangwon National University) ;
  • Ham, Hun-Ju (Department of Biological Environment, Kangwon National University) ;
  • Hur, Jang-Hyun (Department of Biological Environment, Kangwon National University) ;
  • Cho, Sung-Woo (Department of Biochemistry and Molecular Biology, University of Ulsan College of Medicine) ;
  • Han, Kyu-Hyung (Departments of Biomedical Science and Research Institute for Bioscience and Biotechnology, College of Medicine, Hallym University) ;
  • Lee, Kil-Soo (Departments of Biomedical Science and Research Institute for Bioscience and Biotechnology, College of Medicine, Hallym University) ;
  • Park, Jin-Seu (Departments of Biomedical Science and Research Institute for Bioscience and Biotechnology, College of Medicine, Hallym University) ;
  • Choi, Soo-Young (Departments of Biomedical Science and Research Institute for Bioscience and Biotechnology, College of Medicine, Hallym University) ;
  • Eum, Won-Sik (Departments of Biomedical Science and Research Institute for Bioscience and Biotechnology, College of Medicine, Hallym University)
  • Published : 2009.12.31

Abstract

The inhibition of nitric oxide (NO) and cyclooxygenase-2 (COX-2) production is considered to be a promising approach to the treatment of various diseases, including inflammation and cancer. In this study, we examined the effects of the Agrocybe chaxingu $\beta$-glucan (polysaccharide) on lipopolysaccaride (LPS)-induced nitric oxide (NO) and cyclooxygenase-2 (COX-2) expression in murine macrophage Raw 264.7 cells as well as 12-O-tetradecanoylphorbol 13-acetate (TPA)-induced ear edema in mice. The polysaccharide significantly inhibited (P < 0.01) LPS-induced iNOS and COX-2 expression levels in the cells. Furthermore, topical application of polysaccharide resulted in markedly inhibited (P < 0.01) TPA-induced ear edema in mice. These results suggest that this polysaccharide may be used for NO- and COX-2-related disorders such as inflammation and cancer.

Keywords

References

  1. Yu, H. H., Wu, F. L., Lin, S. E. and Shen, L. J. (2008) Recombinant arginine deiminase reduces inducible nitric oxide synthase iNOS-mediated neurotoxicity in a coculture of neurons and microglia. J. Neurosci. Res. 86, 2963-2972 https://doi.org/10.1002/jnr.21740
  2. Colton, C. A., Vitek, M. P., Wink, D. A., Xu, Q., Cantillana, V., Previti, M. L., van Nostrand, W. E., Weinberg, J. B. and Dawson, H. (2006) NO synthase 2 (NOS2) deletion promotes multiple pathologies in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 103, 12867-12872 https://doi.org/10.1073/pnas.0601075103
  3. Dawson, V. L., Kizushi, V. M., Huang, P. L., Snyder, S. H. and Dawson, T. M. (1996) Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient deficient mice. J. Neurosci. 16, 2479-2487
  4. Good, P. F., Hsu, A., Werner, P., Perl, D. P. and Olanow, C. W. (1998) Protein nitration in Parkinson’s disease. J. Neuropathol. Exp. Neurol. 57, 338-342 https://doi.org/10.1097/00005072-199804000-00006
  5. Huang, Z., Huang, P. L., Panahian, N., Dalkara, T., Fishman M. C. and Moskowitz, M. A. (1994) Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265, 1883-1885 https://doi.org/10.1126/science.7522345
  6. Iadecola, C., Zhang, F., Casey, R., Nagayama, M. and Ross, M. E. (1997) Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J. Neurosci. 17, 9157-9164
  7. Martin, L. J., Liu, Z., Chen, K., Price, A. C., Pan, Y., Swaby, J. A. and Golden, W. C. (2007) Motor neuron degeneration in amyotrophic lateral sclerosis mutant superoxide dismutase-1 transgenic mice: mechanism of mitochondriopathy and cell death. J. Comp. Neurol. 500, 20-46 https://doi.org/10.1002/cne.21160
  8. Amin, A. R., Attur, M. and Abramson, S. B. (1999) Nitric oxide synthase and cyclooxygenases: distribution, regulation, and intervention in arthritis. Curr. Opin. Rheumatol. 11, 202-209 https://doi.org/10.1097/00002281-199905000-00009
  9. Tilley, S. L., Coffman, T. M. and Koller, B. A. (2001) Mixed message: gene: modulation of inflammation and immune responses by prostaglandins and thromboxanes. J. Clin. Invest. 107, 191-195 https://doi.org/10.1172/JCI9862
  10. Smith, W. L. and Dewit, D. L. (1990) Prostaglandin endoperoxide H synthase-1 and -2. Adv. Immunol. 62, 167-215 https://doi.org/10.1016/S0065-2776(08)60430-7
  11. Carey, M. A., Germolec, D. R., Langenbach, R. and Zeldin, D. C. (2003) Cyclooxygenase enzymes in allergic inflammation and asthma. Prostaglandins Leukot. Essent. Fatty Acids 69, 157-162 https://doi.org/10.1016/S0952-3278(03)00076-0
  12. Vancheri, C., Mastruzzo, C., Sortino, M. A. and Crimi, N. (2004) The lung as a privileged site for the beneficial actions of PEG2. Trends Immunol. 25, 40-46 https://doi.org/10.1016/j.it.2003.11.001
  13. Rietschel, E. T., Kirikae, T., Schade, F. U., Mamat, U., Schmidt, G., Loppnow, H., Ulmer, A. J., Zahringer, U., Seydel, U. and Di Padova, F. (1994) Bacterial endotoxin: molecular relationships and structure to activity and function. FASEB J. 8, 217-225 https://doi.org/10.1096/fasebj.8.2.8119492
  14. Adams, D. O. and Hamilton, T. A. (1984) The cell biology of macrophage activation. Annu. Rev. Immunol. 2, 283-318 https://doi.org/10.1146/annurev.iy.02.040184.001435
  15. Morrison, D. C. and Ryan, J. L. (1987) Endotoxins and disease mechanisms. Annu. Rev. Med. 38, 417-432 https://doi.org/10.1146/annurev.me.38.020187.002221
  16. DiGiovanni, J. (1992) Multistage carcinogenesis in mouse skin. Pharmacol. Ther. 54, 63-128 https://doi.org/10.1016/0163-7258(92)90051-Z
  17. Slaga, T. J., Fischer, S. M., Weeks, C. E., Klein-Szanto, A. J. and Reiners, J. (1982) Studies on the mechanisms involved in multistage carcinogenesis in mouse skin. J. Cell Biochem. 18, 99-119 https://doi.org/10.1002/jcb.1982.240180109
  18. Furstenberger, G., Berry, D. L., Sorg, B. and Marks, F. (1981) Skin tumor promotion by phorbol esters is a two-stage process. Proc. Natl. Acad. Sci. U.S.A. 78, 7722-7726 https://doi.org/10.1073/pnas.78.12.7722
  19. Furstenberger, G., Sorg, B. and Marks, F. (1983) Tumor promotion by phorbol esters in skin: evidence for a memory effect. Science 220, 89-91 https://doi.org/10.1126/science.6828884
  20. Song, H. Y., Lee, J. A., Ju, S. M., Yoo, K. Y., Won, M. H., Kwon, H. J., Eum, W. S., Jang, S. H., Choi, S. Y. and Park, J. (2008) Topical transduction of superoxide dismutase mediated by HIV-1 Tat protein transduction domain ameliorates 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced inflammation in mice. Biochem. Pharmacol. 75,1348-1357 https://doi.org/10.1016/j.bcp.2007.11.015
  21. Chung, W. Y., Park, J. H., Kim, M. J., Kim, H. O., Hwang, J. K., Lee, S. K. and Park, K. K. (2007) Xanthorrhizol inhibits 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced acute inflammation and two-stage mouse skin carcinogenesis by blocking the expression of ornithine decarboxylase, cyclooxygenase-2 and inducible nitric oxide synthase through mitogen-activated protein kinases and/or the nuclear factor-kB. Carcinogenesis 28, 1224-1231 https://doi.org/10.1093/carcin/bgm005
  22. Ho, Y. S., Lai, C. S., Liu, H. I., Ho, S. Y., Tai, C., Pan, M. H. and Wang, Y. J. (2007) Dihydrolipoic acid inhibits skin tomor promotion through anti-inflammation and anti-oxidation. Biochem. Pharmacol. 73, 1786-1795 https://doi.org/10.1016/j.bcp.2006.12.006
  23. Surh, Y. J., Chun, K. S., Cha, H. H., Han, S. S., Keum, Y. S., Park, K. K. and Lee, S. S. (2001) Molecular mechanisms underlying chemoprventive activities of anti-inflammatory phytochemicals: down-regulation of COX-2 and iNOS through suppression of NF-kappa B activation. Mutat. Res. 480-481, 243-268 https://doi.org/10.1016/S0027-5107(01)00183-X
  24. Yoon, S. Y., Eo, S. K., Kim, Y. S., Lee, S. K. and Han, S. S. (1994) Antimicrobial activity of Garnoderma lucidum extracts alone and in combination with some antibiotics. Arch. Pharm. Res. 17, 438-442 https://doi.org/10.1007/BF02979122
  25. Wang, S. Y., Hsu, M. L., Hsu, H. C., Tzeng, C. H., Lee, S. S., Shiao, M. S. and Ho, C. K. (1997) The anti-tumor effect of Garnoderma lucidum is mediated by cytokines released from activated macrophages and T lymphocytes. Int. J. Cancer 70, 699-705 https://doi.org/10.1002/(SICI)1097-0215(19970317)70:6<699::AID-IJC12>3.0.CO;2-5
  26. Eo, S. K., Kim, Y. S., Lee, C. K. and Han, S. S. (2000) Possible mode of antiviral activity of acidic protein bound polysaccharides isolated from Ganoderma lucidum on herpes simplex viruses. J. Ethnopharmacol. 72, 475-481 https://doi.org/10.1016/S0378-8741(00)00266-X
  27. Lin, J. M., Lin, C. C., Chen, M. F., Ujiie, T. and Takada, A. (1995) Radical scavenger and antihepatotoxic activity of Garnoderma formosanum, Garnoderma lucidum and Garnoderma neo-japonicum. J. Ethnopharmacol. 47, 33-41 https://doi.org/10.1016/0378-8741(95)01251-8
  28. Lin, J. M., Lin, C. C., Chiu, H. F., Yang, J. J. and Lee, S. C. (1993) Evaluation of the anti-inflammatory and liver-protective effects of anoectohilus formosanus, garnoderma lucidum and gynostemma pentaphyllum in rats. Am. J. Chin. Med. 21, 59-69 https://doi.org/10.1142/S0192415X9300008X
  29. Prescott, S. M. and Fitzpatrick, F. A. (2000) Cyclooxygenase-2 and carcinogenesis. Biochim. Biophys. Acta 1470, M69-78
  30. Chun, K. S., Cha, H. H., Shin, J. W., Na, H. K., Park, K. K., Chung, W. Y. and Surh, Y. J. (2004) Nitric oxide induces expression of cyclooxygenase-2 in mouse skin through activation of NF-kappa B. Carcinogenesis 25, 445-454 https://doi.org/10.1093/carcin/bgh021
  31. Chun, K. S., Keum, Y. S., Han, S. S., Song, Y. S., Kim, S. H. and Surh, Y. J. (2003) Curcumin inhibits phorbol ester-induced expression of cyclooxgenase-2 in mouse skin through suppression of extracellular signal-regulated kinase activity and NF-kappa B activation. Carcinogenesis 24, 1515-1524 https://doi.org/10.1093/carcin/bgg107
  32. Choi, M. A., Kim, S. H., Chung, W. Y., Hwang, J. K. and Park, K. K. (2005) Xanthorrhizol, a natural sesquiterpenoid from Curcuma xanthorrhiza, has an anti-metastatic potential in experimental mouse lung metastasis model. Biochem. Biophys. Res. Commun. 326, 210-217 https://doi.org/10.1016/j.bbrc.2004.11.020
  33. Stanely, P. L., Steiner, S., Havens, M. and Tramposch, K. M. (1991) Mouse skin inflammation induced by multiple topical applications of 12-O-tetradecanoylphorbol-13-acetate. Skin Pharmacol. 4, 262-271 https://doi.org/10.1159/000210960
  34. Pastore, S., Mascia, F., Mariotti, F., Dattilo, C., Mariani, V. and Girolomoni, G. (2005) ERK1/2 regulates epidermal chemokine expression and skin inflammation. J. Immunol. 174, 5047-5056 https://doi.org/10.4049/jimmunol.174.8.5047
  35. Steeber, D. A., Tang, M. L., Green, N. E., Zhang, X. Q., Sloane, J. E. and Tedder, T. F. (1999) Leukocyte entry into sites of inflammation requires overlapping interactions between the L-selectin and ICAM-1 pathways. J. Immunol. 163, 2176-2186
  36. Kim, D. W., Kim, S. Y., Lee, S. H., Lee, Y. P., Lee, M. J., Jeong, M. S., Jang, S. H., Park, J., Lee, K. S., Kang, T. C., Won, M. H., Cho, S. W., Kwon, O. S., Eum, W. S. and Choi, S. Y. (2008) Protein transduction of an antioxidant enzyme: subcellular localization of superoxide dismutase fusion protein in cells. BMB Reports 4, 170-175
  37. Misko, T. P., Schilling, R. J., Salvemini, D., Moore, W. M. and Currie, M. G. (1993) A fluorometric assay for the measurement of nitrite in biological samples. Anal. Biochem. 214, 11-16 https://doi.org/10.1006/abio.1993.1449
  38. Shin, J., Gu, C., Kim, J. and Park, S. (2008) Transient activation of the MAP kinase signaling pathway by the forward signaling of EphA4 in PC12 cells. BMB Reports 41, 479-484 https://doi.org/10.5483/BMBRep.2008.41.6.479
  39. Zhang, S. Y., Park, K. W., Oh, S., Cho, H. J., Cho, H. J., Park, J. S., Cho, Y. S., Koo, B. K., Chae, I. H., Choi, D. J., Kim, H. S. and Lee, M. M. (2005) NF-kappaB decoy potentiates the effects of radiation on vascular smooth muscle cell by enhancing apoptosis. Exp. Mol. Med. 37, 18-26 https://doi.org/10.1038/emm.2005.3

Cited by

  1. Lotus (Nelumbo nucifera Gaertn) plumule polysaccharide protects the spleen and liver from spontaneous inflammation in non-obese diabetic mice by modulating pro-/anti-inflammatory cytokine gene expression vol.129, pp.2, 2011, https://doi.org/10.1016/j.foodchem.2011.03.103
  2. Phylogenetic analysis of the Agrocybe aegerita multispecies complex in Southwest China inferred from ITS and mtSSU rDNA sequences and mating tests vol.62, pp.4, 2012, https://doi.org/10.1007/s13213-012-0437-4
  3. An insight into anti-inflammatory effects of fungal beta-glucans vol.41, pp.1, 2015, https://doi.org/10.1016/j.tifs.2014.09.002
  4. Inflammatory Modulation Effect of Glycopeptide fromGanoderma capense(Lloyd) Teng vol.2014, 2014, https://doi.org/10.1155/2014/691285
  5. Characterization and Anti-Inflammatory Potential of an Exopolysaccharide from Submerged Mycelial Culture of Schizophyllum commune vol.8, 2017, https://doi.org/10.3389/fphar.2017.00252
  6. Anti-inflammatory potential of mushroom extracts and isolated metabolites vol.50, 2016, https://doi.org/10.1016/j.tifs.2016.02.005
  7. Amelioration of streptozotocin-induced diabetes by Agrocybe chaxingu polysaccharide vol.29, pp.4, 2010, https://doi.org/10.1007/s10059-010-0044-9
  8. Antitumor Activity of the Protein and Small Molecule Component Fractions fromAgrocybe aegeritaThrough Enhancement of Cytokine Production vol.17, pp.4, 2014, https://doi.org/10.1089/jmf.2013.2846
  9. Herbs vol.14, pp.11, 2017, https://doi.org/10.1002/cbdv.201700280