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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Macrophage Activation by an Acidic Polysaccharide Isolated from Angelica Sinensis (Oliv.) Diels

  • Yang, Xingbin (Key Laboratory of Ministry of Education for Medicinal Plant Resource and Natural Pharmaceutical Chemistry, College of Life Sciences, Shaanxi Normal University) ;
  • Zhao, Yan (Faculty of Pharmaceutical Sciences, Fourth Military Medical University) ;
  • Wang, Haifang (Faculty of Pharmaceutical Sciences, Fourth Military Medical University) ;
  • Mei, Qibing (Faculty of Pharmaceutical Sciences, Fourth Military Medical University)
  • Published : 2007.09.30
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Abstract

This study was designed to identify and characterize the mechanism of macrophage activation by AAP, an acidic polysaccharide fraction isolated from the roots of Angelica sinensis (Oliv.) Diels. As a result, AAP significantly enhanced nitric oxide (NO) production and cellular lysosomal enzyme activity in murine peritoneal macrophages in vitro and in vivo. Furthermore, L-NAME, a specific inhibitor of inducible nitric oxide synthase (iNOS), effectively suppressed AAP-induced NO generation in macrophages, indicating that AAP stimulated macrophages to produce NO through the induction of iNOS gene expression and the result was further confirmed by the experiment of the increase of AAP-induced iNOS transcription in a dose-dependent manner. To further investigate, AAP was shown to strongly augment toll-like receptor 4 (TLR4) mRNA expression and the pretreatment of macrophages with anti-TLR4 antibody significantly blocked AAP-induced NO release and the increase of iNOS activity, and tumor necrosis factor-$\alpha$ (TNF-$\alpha$) secretion.

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References

  1. Alderton, W. K., Cooper, C. E. and Knowles, R. G. (2001) Nitric oxide synthase: structure function and inhibition. Biochem. J., 357, 593-615. https://doi.org/10.1042/0264-6021:3570593
  2. Ando. I., Tsukumo, Y., Wakabayashi, T., Akashi, S., Miyake, K., Kataoka, T. and Nagai, K. (2002) Safflower polysaccharides activate the transcription factor NF-kappa B via Toll-like receptor 4 and induce cytokine production by macrophages. Int. Immunopharmacol. 2, 1155-1162. https://doi.org/10.1016/S1567-5769(02)00076-0
  3. Beutler, B., Hoebe, K., Du, X. and Ulevitch, R. J. (2003) How we detect microbes and respond to them: the Toll-like receptors and their transducers. J. Leukocyte Biol. 74, 479-485. https://doi.org/10.1189/jlb.0203082
  4. Cho, C. H., Mei, Q. B., Shang, P., Lee, S. S., So, H. L., Guo, X. and Li, Y. (2000) Study of the gastrointestinal protective effects of polysaccharides from Angelica sinensis in rats. Planta Medica 66, 348-351. https://doi.org/10.1055/s-2000-8552
  5. Ferrari, M., Fornasiero, M. C. and Isetta, A. M. (1990) MTT colorimetric assay for testing macrophage cytotoxic activity in vitro. J. Immunol. Methods 131, 165-172. https://doi.org/10.1016/0022-1759(90)90187-Z
  6. Franchini, M., Schweizer, M., Mtzener, P., Magkouras, I., Sauter, K. S., Mirkovitch, J., Peterhans, E. and Jungi, T. W. (2006) Evidence for dissociation of TLR mRNA expression and TLR agonist-mediated functions in bovine macrophages. Vet. Immunol. Immunopathol. 110, 37-49. https://doi.org/10.1016/j.vetimm.2005.09.002
  7. Green, L. C., Wagner, D. A., Glogowski, J., Skipper, P. L., Wishnok, J. S. and Tannenbaum, S. R. (1982) Analysis of nitrate in biological fluids. Anal. Biochem. 126, 131-138. https://doi.org/10.1016/0003-2697(82)90118-X
  8. Han, S. B., Park, S. K., Ahn, H. J., Yoon, Y. D., Kim, Y. H., Lee, J. J., Lee, K. H., Moon, J. S., Kim, H. C. and Kim, H. M. (2003a) Characterization of B cell membrane receptors of polysaccharide isolated from the root of Acanthopanax koreanum. Int. Immunopharmacol. 3, 683-691. https://doi.org/10.1016/S1567-5769(03)00056-0
  9. Han, S. B., Yoon, Y. D., Ahn, H. J., Lee, H. S., Lee, C. W., Yoon, W. K., Park, S. K. and Kim, H. M. (2003b) Toll-like receptormediated activation of B cells and macrophages by polysaccharide isolated from cell culture of Acanthopanax senticosus. Int. Immunopharmacol. 3, 1301-1312. https://doi.org/10.1016/S1567-5769(03)00118-8
  10. Jeon, Y. J., Han, S. B., Ahn, K. S. and Kim, H. M. (1999) Activation of NFkappaB/Rel in angelan-stimulated macrophages. Int. Immunopharmacol. 43, 1-9. https://doi.org/10.1016/S0162-3109(99)00032-6
  11. Jeong, S. C., Jeong, Y. T., Yang, B. K. and Song, C. H. (2006) Chemical characteristics and immuno-stimulating properties of biopolymers extracted from Acanthopanax sessiliflorus. J. Biochem. Mol. Biol. 39, 84-90. https://doi.org/10.5483/BMBRep.2006.39.1.084
  12. Kim, G. Y., Choi, G. S., Lee, S. H. and Park, Y. M. (2004) Acidic polysaccharide isolated from Phellinus linteus enhances through the up-regulation of nitric oxide and tumor necrosis factor-a from peritoneal macrophages. J. Ethnopharmacol. 95, 69-76. https://doi.org/10.1016/j.jep.2004.06.024
  13. Komatsu, W., Yagasaki, K., Miura, Y. and Funabiki, R. (1997) Stimulation of tumor necrosis factor and interleukin-1 productivity by the oral administration of cabbage juice to rats. Biosci. Biotechnol. Biochem. 61, 1937-1938. https://doi.org/10.1271/bbb.61.1937
  14. Lee, K. Y. and Jeon, Y. J. (2003) Polysaccharide isolated from Poria cocos sclerotium induces NF-kappaB/rel activation and iNOS expression in murine macrophages. Int. Immunopharmacol. 3, 1353-1362. https://doi.org/10.1016/S1567-5769(03)00113-9
  15. Lee, K. Y. and Jeon, Y. J. (2005) Macrophage activation by polysaccharide isolated from Astragalus membranaceus. Int. Immunopharmacol. 5, 1225-1233. https://doi.org/10.1016/j.intimp.2005.02.020
  16. MacMicking, J., Xie, Q. W. and Nathan, C. (1997) Nitric oxide and macrophage function. Annu. Rev. Immunol. 15, 323-350. https://doi.org/10.1146/annurev.immunol.15.1.323
  17. Mei, Q. B., Tao, J. Y., Zhang, H. D., Duan, Z. X. and Chen, Y. Z. (1988) Effects of Angelica sinensis polysaccharides on hemopoietic stem cells in irradiated mice. Acta Pharmacol. Sin. 9, 279-282.
  18. Morrison, D. C. and Jacobs, D. M. (1976) Binding of polymyxin B to the lipid A portion of bacterial lipopolysaccharides. Immunochemistry 13, 813-818. https://doi.org/10.1016/0019-2791(76)90181-6
  19. Rojas, A., Padron, J., Caveda, L., Palacios, M. and Moncada, S. (1993) Role of nitric oxide pathway in the protection against lethal endotoxemia by low dose of lipopolysaccharides. Biochem. Biophys. Res. Commun. 191, 441-446. https://doi.org/10.1006/bbrc.1993.1237
  20. Senel, S. and McClure, S. J. (2004) Potential applications of chitosan in veterinary medicine. Adv. Drug Deliv. Rev. 56, 1467-1480. https://doi.org/10.1016/j.addr.2004.02.007
  21. Shang, P., Qian, A. R., Yang, T. H., Jia, M., Mei, Q. B., Cho, C. H., Zhao, W. M. and Chen, Z. N. (2003) Experimental study of anti-tumor effects of polysaccharides from Angelica sinensis. World J. Gastroenterol. 9, 1963-1967. https://doi.org/10.3748/wjg.v9.i9.1963
  22. Suzuki, I., Tanaka, H., Kinoshita, A., Oikawa, S., Osawa, M. and Yadomae, T. (1990) Effect of orally administered beta-glucan on macrophage function in mice. Int. Immunopharmacol. 12, 675-684. https://doi.org/10.1016/0192-0561(90)90105-V
  23. Tzianabos, A. O. (2000) Polysaccharide immunomodulators as therapeutic agents: structural aspects and biologic function. Clin. Microbiol. Rev. 13, 523-533. https://doi.org/10.1128/CMR.13.4.523-533.2000
  24. Werling, D. and Jungi, T. W. (2003) Toll-like receptors linking innate and adaptive immune response. Vet. Immunol. Immunopathol. 91, 1-12. https://doi.org/10.1016/S0165-2427(02)00228-3
  25. Xie, Q. W., Cho, H. J., Calaycay, J., Mumford, R. A., Swiderek, K. M., Lee, T. D., Ding, A., Troso, T. and Nathan, C. (1992) Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256, 225-228. https://doi.org/10.1126/science.1373522
  26. Yang, X. B., Zhao, Y., Wang, Q. W., Wang, H. F. and Mei, Q. B. (2005) Analysis of the monosaccharide components of Angelica polysaccharides by high performance liquid chromatography. Anal. Sci. 21, 1177-1180. https://doi.org/10.2116/analsci.21.1177
  27. Ye, Y. N., Koo, M. W., Li, Y., Matsui, H. and Cho, C. H. (2001b) Angelica sinensis modulates migration and proliferation of gastric epithelial cells. Life Sci. 68, 961-968. https://doi.org/10.1016/S0024-3205(00)00994-2
  28. Ye, Y. N., Liu, E. S., Li, Y., So, H. L., Cho, C. C., Sheng, H. P., Lee, S. S. and Cho, C. H. (2001c) Protective effect of polysaccharides-enriched fraction from Angelica sinensis on hepatic injury. Life Sci. 69, 637-646. https://doi.org/10.1016/S0024-3205(01)01153-5
  29. Ye, Y. N., Liu, E. S., Shin, V. Y., Koo, M. W., Li, Y., Wei, E. Q., Matsui, H. and Cho, C. H. (2001a) A mechanistic study of proliferation induced by Angelica sinensis in a normal gastric epithelial cell line. Biochem. Pharmacol. 61, 1439-1448. https://doi.org/10.1016/S0006-2952(01)00625-6
  30. Ye, Y. N., So, H. L., Liu, E. S., Shin, V. Y. and Cho, C. H. (2003) Effect of polysaccharides from Angelica sinensis on gastric ulcer healing. Life Sci. 72, 925-932. https://doi.org/10.1016/S0024-3205(02)02332-9

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