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Effects of β-Glucan on the Release of Nitric Oxide by Macrophages Stimulated with Lipopolysaccharide

  • Choi, E.Y. (Department of Life Science, Silla University) ;
  • Lee, S.S. (Division of Applied Life Science, Graduate School of Gyeongsang National University, IALS) ;
  • Hyeon, J.Y. (Department of Life Science, Silla University) ;
  • Choe, S.H. (Department of Life Science, Silla University) ;
  • Keum, B.R. (Department of Life Science, Silla University) ;
  • Lim, J.M. (Glucan Corporation) ;
  • Park, D.C. (Glucan Corporation) ;
  • Choi, I.S. (Department of Life Science, Silla University) ;
  • Cho, K.K. (Department of Animal Resources Technology, Gyeongnam National University of Science and Technology)
  • Received : 2016.05.26
  • Accepted : 2016.07.19
  • Published : 2016.11.01

Abstract

This research analyzed the effect of ${\beta}$-glucan that is expected to alleviate the production of the inflammatory mediator in macrophagocytes, which are processed by the lipopolysaccharide (LPS) of Escherichia. The incubated layer was used for a nitric oxide (NO) analysis. The DNA-binding activation of the small unit of nuclear factor-${\kappa}B$ was measured using the enzyme-linked immunosorbent assay-based kit. In the RAW264.7 cells that were vitalized by Escherichia coli (E. coli) LPS, the ${\beta}$-glucan inhibited both the combatant and rendering phases of the inducible NO synthase (iNOS)-derived NO. ${\beta}$-Glucan increased the expression of the heme oxygenase-1 (HO-1) in the cells that were stimulated by E. coli LPS, and the HO-1 activation was inhibited by the tin protoporphyrin IX (SnPP). This shows that the NO production induced by LPS is related to the inhibition effect of ${\beta}$-glucan. The phosphorylation of c-Jun N-terminal kinases (JNK) and the p38 induced by the LPS were not influenced by the ${\beta}$-glucan, and the inhibitory ${\kappa}B-{\alpha}$ ($I{\kappa}B-{\alpha}$) decomposition was not influenced either. Instead, ${\beta}$-glucan remarkably inhibited the phosphorylation of the signal transducer and activator of transcription-1 (STAT1) that was induced by the E. coli LPS. Overall, the ${\beta}$-glucan inhibited the production of NO in macrophagocytes that was vitalized by the E. coli LPS through the HO-1 induction and the STAT1 pathways inhibition in this research. As the host immune response control by ${\beta}$-glucan weakens the progress of the inflammatory disease, ${\beta}$-glucan can be used as an effective immunomodulator.

Keywords

References

  1. Carter, A. B., M. M. Monick, and G. W. Hunninghake. 1999. Both Erk and p38 kinases are necessary for cytokine gene transcription. Am. J. Respir. Cell Mol. Biol. 20:751-758. https://doi.org/10.1165/ajrcmb.20.4.3420
  2. Chae, H. S., O. H. Kang, J. G. Choi, Y. C. Oh, Y. S. Lee, H. J. Jang, J. H. Kim, H. Park, K. Y. Jung, D. H. Sohn, and D. Y. Kwon. 2009. 5-hydroxytryptophan acts on the mitogen-activated protein kinase extracellular-signal regulated protein kinase pathway to modulate cyclooxygenase-2 and inducible nitric oxide synthase expression in RAW 264.7 cells. Biol. Pharm. Bull. 32:553-557. https://doi.org/10.1248/bpb.32.553
  3. Chiou, W. F., C. F. Chen, and J. J. Lin. 2000. Mechanisms of inhibition of inducible nitric oxide synthase (iNOS) expression in RAW 264.7 cells by andrographolide. Br. J. Pharmacol. 129:1553-1560. https://doi.org/10.1038/sj.bjp.0703191
  4. Chung, E. K., E. H. Seo, J. H. Park, H. R. Shim, K. H. Kim, and B. R. Lee. 2011. Anti-inflammatory and anti-allergic effect of extracts from organic soybean. Kor. J. Org. Agric. 19:245-253.
  5. Choi E. Y., Y. M. Hwang, J. Y. Lee, J. I. Choi, I.S. Choi, J. Y. Jin, J. S. Ko, and S. J. Kim. 2007. Lipid A-associated proteins from Porphyromonas gingivalis stimulate release of nitric oxide by inducing expression of inducible nitric oxide synthase. J. Periodontal. Res. 42:350-60. https://doi.org/10.1111/j.1600-0765.2006.00956.x
  6. Choi E. Y., J. Y. Jin, J. Y. Lee, J. Y. Lee, I. S. Choi, and S. J. Kim. 2011. Melatonin inhibits Prevotella intermedia lipopolysaccharide-induced production of nitric oxide and interleukin-6 in murine macrophages by suppressing NF-${\kappa}B$and STAT1 activity. J. Pineal Res. 50:197-206.
  7. Choi, E. Y., J. Y. Jin, J. Y. Lee, J. I. Choi, I. S. Choi, and S. J. Kim. 2012. Anti-inflammatory effects and the underlying mechanisms of action of daidzein in murine macrophages stimulated with Prevotella intermedia lipopolysaccharide. J. Periodontal. Res. 47:204-11. https://doi.org/10.1111/j.1600-0765.2011.01422.x
  8. Compton, R., D. Williams, and W. Browder. 1996. The beneficial effect of enhanced macrophage function on the healing of bowel anastomoses. Am. Surg. 62:14-18.
  9. Covert, M. W., T. H. Leung, J. E. Gaston, and D. Baltimore. 2005. Achieving stability of lipopolysaccharide-induced NF-kappaB activation. Science 309:1854-1857. https://doi.org/10.1126/science.1112304
  10. Di Renzo. L., E. Yefenof, and E. Klein. 1991. The function of human NK cells is enhanced by beta-glucan, a ligand of CR3 (CD11b/CD18). Eur. J. Immunol. 21:1755-1758. https://doi.org/10.1002/eji.1830210726
  11. Gao, J. J., M. B. Filla, M. J. Fultz, S. N. Vogel, S. W. Russell, and W. J. Murphy. 1998. Autocrine/paracrine IFN-${\alpha}{\beta}$ mediates the lipopolysaccharide-induced activation of transcription factor $Stat1{\alpha}$ in mouse macrophages: pivotal role of $Stat1{\alpha}$ in induction of the inducible nitric oxide synthase gene. J. Immunol. 161:4803-4810.
  12. Hamada, N., K. Deguchi, T. Ohmoto, K. Sakai, T. Ohe, and H. Yoshizumi. 2000. Ascorbic acid stimulation of production of a highly branched, beta-1,3-glucan by Aureobasidium pullulans K-1--oxalic acid, a metabolite of ascorbic acid as the stimulating substance. Biosci. Biotechnol. Biochem. 64:1801-1806. https://doi.org/10.1271/bbb.64.1801
  13. Karin, M. and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18:621-663. https://doi.org/10.1146/annurev.immunol.18.1.621
  14. Kim, D. H., B. J. An, S. G. Kim, T. S. Park, G. H. Park, and J. H. Son. 2011. Anti-inflammatory effect of Ligularia fischeri, Solidago virga-aurea and Aruncus dioicus complex extracts in RAW 264.7 cells. J. Life Sci. 21:678-683. https://doi.org/10.5352/JLS.2011.21.5.678
  15. Kimura, Y., M. Sumiyoshi, T. Suzuki, and M. Sakanaka. 2006. Antitumor and antimetastatic activity of a novel water-soluble low molecular weight beta-1,3-D-glucan (branch beta-1,6) isolated from Aureobasidium pullulans 1A1 strain black yeast. Anticancer Res. 26:4131-4141.
  16. Kimura, Y., M. Sumiyoshi, T. Suzuki, T. Suzuki, and M. Sakanaka. 2007. Inhibitory effects of water-soluble low-molecular-weight beta-(1,3-1,6)-D-glucan purified from Aureobasidium pullulans GM-NH-1A1 strain on food allergic reactions in mice. Int. Immunopharmacol. 7:963-972. https://doi.org/10.1016/j.intimp.2007.03.003
  17. McCartney-Francis, N., J. B. Allen, D. E. Mizel, J. E. Albina, Q. W. Xie, C. F. Nathan, and S. M. Wahl. 1993. Suppression of arthritis by an inhibitor of nitric oxide synthase. J. Exp. Med. 178:749-754. https://doi.org/10.1084/jem.178.2.749
  18. Min, H. Y., S. H. Song, B. Lee, S. Kim, and S. K. Lee. 2010. Inhibition of lipopolysaccharide-induced nitric oxide production by antofine and its analogues in RAW 264.7 macrophage cells. Chem. Biodivers. 7:409-414. https://doi.org/10.1002/cbdv.200900040
  19. Morse, D. and A. M. Choi. 2002. Heme oxygenase-1: the "emerging molecule" has arrived. Am. J. Respir. Cell Mol. Biol. 27:8-16. https://doi.org/10.1165/ajrcmb.27.1.4862
  20. Morson, B. C. 1980. Pathology of inflammatory bowel disease. Gastroenterol. Jpn. 15:184-187. https://doi.org/10.1007/BF02774935
  21. Muramatsu, D., K. Kawata, S. Aoki, H. Uchiyama, M. Okabe, T. Miyazaki, H. Kide, and A. Iwai. 2014. Stimulation with the Aureobasidium pullulans-produced beta-glucan effectively induces interferon stimulated genes in macrophage-like cell lines. Sci. Rep. 24:4777.
  22. Nathan, C. F. and J. B. Jr. Hibbs. 1991. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3:65-70. https://doi.org/10.1016/0952-7915(91)90079-G
  23. Ohno, N., N. N. Miura, N. Chiba, Y. Adachi, and T. Yadomae. 1995. Comparison of the immunopharmacological activities of triple and single-helical schizophyllan in mice. Biol. Pharm. Bull. 18:1242-1247. https://doi.org/10.1248/bpb.18.1242
  24. Onderdonk, A. B., R. L. Cisneros, P. Hinkson, and G. Ostroff. 1992. Anti-infective effect of poly-beta 1-6-glucotriosyl-beta 1-3-glucopyranose glucan in vivo. Infect. Immun. 60:1642-1647.
  25. Otterbein, L. E, M. P. Soares, K. Yamashita, and F. H. Bach. 2003. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 24:449-455. https://doi.org/10.1016/S1471-4906(03)00181-9
  26. Ryter, S. W., J. Alam, and A. M. Choi. 2006. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86:583-650. https://doi.org/10.1152/physrev.00011.2005
  27. Samavati, L., R. Rastogi, W. Du, M. Huttemann, A. Fite, and L. Franchi. 2009. STAT3 tyrosine phosphorylation is critical for interleukin1 beta and interleukin-6 production in response to lipopolysaccharide and live bacteria. Mol. Immunol. 46:1867-1877. https://doi.org/10.1016/j.molimm.2009.02.018
  28. Schindler, C., D. E. Levy, and T. Decker. 2007. JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282:20059-20063. https://doi.org/10.1074/jbc.R700016200
  29. Seo, H. P., J. M. Kim, H. D. Shin, T. K. Kim, H. J. Chang, B. R. Park, and J. W. Lee. 2002. Production of beta-1,3/1,6-glucan by Aureobasidium pullulans SM-2001. Korean J. Biotechnol. Bioeng. 17: 376-380.
  30. Shon, D. H., D. W. Choi, and M. H. Kim. 2012. Improvement of anti-inflammation activity of Gardeniae fructus extract by the treatment of beta-Glucosidase. Kor. J. Food Sci. Technol. 44:331-336. https://doi.org/10.9721/KJFST.2012.44.3.331
  31. Thornton, B. P., V. Vetvicka, M. Pitman, R. C. Goldman, and G. D. Ross. 1996. Analysis of the sugar specificity and molecular location of the beta-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18). J. Immunol. 156:1235-1246.
  32. Tsoyi, K., H. J. Kim, J. S. Shin, D. H. Kim, H. J. Cho, S. S. Lee, S. K. Ahn, H. S. Yun-Choi, J. H. Lee, H. G. Seo, and K. C. Chang. 2008. HO-1 and JAK-2/STAT-1 signals are involved in preferential inhibition of iNOS over COX-2 gene expression by newly synthesized tetrahydroisoquinoline alkaloid, CKD712, in cells activated with lipopolysaccharide. Cell. Signal. 20:1839-1847. https://doi.org/10.1016/j.cellsig.2008.06.012
  33. Weisz, A., L. Cicatiello, and H. Esumi. 1996. Regulation of the mouse inducible-type nitric oxide synthase gene promoter by interferon-gamma, bacterial lipopolysaccharide and NG-monomethyl-L-arginine. Biochem. J. 316:209-215. https://doi.org/10.1042/bj3160209
  34. Wu, J., J. Ma, S. T. Fan, H. J. Schlitt, and T. Y. Tsui. 2005. Bilirubin derived from heme degradation suppresses MHC class II expression in endothelial cells. Biochem. Biophys. Res. Commun. 338:890-896. https://doi.org/10.1016/j.bbrc.2005.10.021

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