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Luteolin 5-O-glucoside from Korean Milk Thistle, Cirsium maackii, Exhibits Anti-Inflammatory Activity via Activation of the Nrf2/HO-1 Pathway

  • Jung, Hyun Ah (Department of Food Science and Human Nutrition, Chonbuk National University) ;
  • Roy, Anupom (Department of Food and Life Science, Pukyong National University) ;
  • Abdul, Qudeer Ahmed (Department of Food and Life Science, Pukyong National University) ;
  • Kim, Hyeung Rak (Department of Food and Life Science, Pukyong National University) ;
  • Park, Hee Juhn (Department of Pharmaceutical Engineering, Sangji University) ;
  • Choi, Jae Sue (Department of Food and Life Science, Pukyong National University)
  • Received : 2017.05.09
  • Accepted : 2017.05.26
  • Published : 2017.09.29

Abstract

Luteolin 5-O-glucoside is the major flavonoid from Korean thistle, Cirsium maackii. We previously reported the anti-inflammatory activities of luteolin 5-O-glucoside in lipopolysaccharide (LPS)-stimulated RAW 264.7 cells. In this study, we determined the anti-inflammatory mechanisms of luteolin 5-O-glucoside through the inhibition of nitric oxide (NO) production in vitro and in vivo. Results revealed that luteolin 5-O-glucoside dose-dependently inhibited NO production and expression of iNOS and COX-2 in LPS-induced RAW 264.7 cells. Luteolin 5-O-glucoside also significantly inhibited the translocation of $NF-{\kappa}B$, the activation of MAPKs, and ROS generation in LPS-induced RAW 264.7 cells. In addition, protein expressions of Nrf-2 and HO-1 were also upregulated by luteolin 5-O-glucoside treatment. Moreover, luteolin 5-O-glucoside inhibited ${\lambda}-carrageenan-induced$ mouse paw edema by 65.34% and 48.31% at doses of 50 and 100 mg/kg body weight, respectively. These findings indicate potential anti-inflammatory effect of luteolin 5-O-glucoside particularly by downregulating $NF-{\kappa}B$ and upregulating HO-1/Nrf-2 pathway.

Keywords

References

  1. Choudhari, A. S.; Raina, P.; Deshpande, M. M.; Wali, A. G.; Zanwar, A.; Bodhankar, S. L.; Kaul-Ghanekar, R. J. Ethnopharmacol. 2013, 150, 215-222. https://doi.org/10.1016/j.jep.2013.08.025
  2. Joung, E. J.; Lee, B.; Gwon, W. G.; Shin, T.; Jung, B. M.; Yoon, N. Y.; Choi, J. S.; Oh, C. W.; Kim, H. R. Int. Immunopharmacol. 2015, 29, 693-700. https://doi.org/10.1016/j.intimp.2015.09.007
  3. Giuliani, C.; Napolitano, G.; Bucci, I.; Montani, V.; Monaco, F. Clin. Ter. 2001, 152, 249-253.
  4. May, M. J.; Ghosh, S. Immunol. Today 1998, 19, 80-88. https://doi.org/10.1016/S0167-5699(97)01197-3
  5. Tak, P. P.; Firestein, G. S. J. Clin. Invest. 2001, 107, 7-11. https://doi.org/10.1172/JCI11830
  6. Kim, A. R.; Lee, M. S.; Shin, T. S.; Hua, H.; Jang, B. C.; Choi, J. S.; Byun, D. S.; Utsuki, T.; Ingram, D.; Kim, H. R. Toxicol. In Vitro 2011, 25, 1789-1795. https://doi.org/10.1016/j.tiv.2011.09.012
  7. Pae, H. O.; Chung, H. T. Immune. Netw. 2009, 9, 12-19. https://doi.org/10.4110/in.2009.9.1.12
  8. Chen, T. Y.; Sun, H. L.; Yao, H. T.; Lii, C. K.; Chen, H. W.; Chen, P. Y.; Li, C. C.; Liu, K. L. Food Chem. Toxicol. 2013, 55, 257-264. https://doi.org/10.1016/j.fct.2012.12.056
  9. Taha, R.; Blaise, G. Funct. Food Health Dis. 2014, 4, 510-523.
  10. Kim, J. G., Illustrated Natural Drugs Encyclopedia. Namsandang, Korea, pp. 37 (1984).
  11. Iwashina, T.; Ito, T.; Ootani, S. Ann. Tsukuba. Bot. Gard. 1989, 8, 15-19.
  12. Jung, H. A.; Kim, Y. S.; Choi, J. S. Food Chem. Toxicol. 2009, 47, 2790-2797. https://doi.org/10.1016/j.fct.2009.08.014
  13. Jung, H. A.; Jin, S. E.; Min, B. S.; Kim, B. W.; Choi, J. S. Food Chem. Toxicol. 2012, 50, 2171-2179. https://doi.org/10.1016/j.fct.2012.04.011
  14. Morris, C. J. Methods Mol. Biol. 2003, 225, 115-21.
  15. Sharif, O.; Bolshakov, V. N.; Raines, S.; Newham, P.; Perkins, N. D. BMC Immunol. 2007, 8, 1-17. https://doi.org/10.1186/1471-2172-8-1
  16. Lee, C. B., Flora of Korea. Hyangmoonsa, Korea, pp. 274 (1979).
  17. Lee, S. J., Korean Folk Medicine. Seoul National University, Korea, pp. 145-146 (1966).
  18. Keiser, K., Johnson, C. C.; Tipton, D. A. J. Endod. 2000, 26, 288-291. https://doi.org/10.1097/00004770-200005000-00010
  19. Meda, L.; Cassatella, M. A.; Szendrei, G. I.; Otvos, L. Jr.; Baron, P.; Villalba, M.; Ferrari, D.; Rossi, F. Nature 1995, 374, 647-650. https://doi.org/10.1038/374647a0
  20. Dandona, P.; Chaudhuri, A.; Dhindsa, S. Diabetes Care 2010, 33, 1686-1687. https://doi.org/10.2337/dc10-0503
  21. Marks-Konczalik, J.; Chu, S. C.; Moss, J. J. Biol. Chem. 1998, 273, 22201-22208. https://doi.org/10.1074/jbc.273.35.22201
  22. Islam, M. N.; Choi, R. J.; Jin, S. E.; Kim, Y. S.; Ahn, B. R.; Zhao, D.; Jung, H. A.; Choi, J. S. J. Ethnopharmacol. 2012, 144, 175-181. https://doi.org/10.1016/j.jep.2012.08.048
  23. Chen, J. J.; Huang, W. C.; Chen, C. C. Mol. Biol. Cell 2005, 16, 5579-5591. https://doi.org/10.1091/mbc.e05-08-0778
  24. Rajapakse, N.; Kim, M. M.; Mendis, E.; Kim, S. K. Immunology 2008, 123, 348-357. https://doi.org/10.1111/j.1365-2567.2007.02683.x
  25. Kaminska, B. Biochim. Biophys. Acta 2005, 1754, 253-262. https://doi.org/10.1016/j.bbapap.2005.08.017
  26. Hancock, J. T.; Desikan, R.; Neill, S. J. Biochem. Soc. Trans. 2001, 29, 345-350. https://doi.org/10.1042/bst0290345
  27. Choi, S. Y.; Hwang, J. H.; Ko, H. C.; Park, J. G.; Kim, S. J. J. Ethnopharmacol. 2007, 113, 149-155. https://doi.org/10.1016/j.jep.2007.05.021
  28. Siomek, A. Acta Biochim. Pol. 2012, 59, 323-331.
  29. Ryan, K. A.; Smith, M. F. Jr.; Sanders, M. K.; Ernst, P. B. Infect Immun. 2004, 72, 2123-2130. https://doi.org/10.1128/IAI.72.4.2123-2130.2004
  30. Kim, J. H.; Choo, Y. Y.; Tae, N.; Min, B. S.; Lee, J. H. Int. Immunopharmacol. 2014, 22, 420-426. https://doi.org/10.1016/j.intimp.2014.07.025
  31. Lee, I. S.; Lim, J.; Gal, J.; Kang, J. C.; Kim, H. J.; Kang, B. Y.; Choi, H. J. Neurochem. Int. 2011, 58, 153-160. https://doi.org/10.1016/j.neuint.2010.11.008
  32. Paine, A.; Eiz-Vesper, B.; Blasczyk, R.; Immenschuh, S. Biochem. Pharmacol. 2010, 80, 1895-1903. https://doi.org/10.1016/j.bcp.2010.07.014
  33. Lee, M. Y.; Lee, J. A.; Seo, C. S.; Ha, H.; Lee, H.; Son, J. K.; Shin, H. K. Food Chem. Toxicol. 2011, 49, 1047-1055. https://doi.org/10.1016/j.fct.2011.01.010
  34. Tsoyi, K.; Lee, T. Y.; Lee, Y. S.; Kim, H. J.; Seo, H. G.; Lee, J. H.; Chang, K. C. Mol. Pharmacol. 2009, 76, 173-182. https://doi.org/10.1124/mol.109.055137
  35. Salvemini, D.; Wang, Z. Q.; Bourdon, D. M.; Stern, M. K.; Currie, M. G.; Manning, P. T. Eur. J. Pharmacol. 1996, 303, 217-220. https://doi.org/10.1016/0014-2999(96)00140-9
  36. Rocha, A. C.; Fernandes, E. S.; Quintão, N. L.; Campos, M. M.; Calixto, J. B. Br. J. Pharmacol. 2006, 148, 688-695. https://doi.org/10.1038/sj.bjp.0706775
  37. Yuan, G.; Wahlqvist, M. L.; He, G.; Yang, M.; Li, D. Asia. Pac. J. Clin. Nutr. 2006, 15, 143-152.
  38. Camuesco, D.; Comalada, M.; Rodriguez-Cabezas, M. E.; Nieto, A.; Lorente, M. D.; Concha, A.; Zarzuelo, A.; Galvez, J. Br. J. Pharmacol. 2004, 143, 908-918. https://doi.org/10.1038/sj.bjp.0705941
  39. Halliwell, B.; Zhao, K.; Whiteman, M. Free Radic. Res. 2000, 33, 819-830. https://doi.org/10.1080/10715760000301341
  40. Comalada, M.; Ballester, I.; Bailon, E.; Sierra, S.; Xaus, J.; Galvez, J.; de Medina, F. S.; Zarzuelo, A. Biochem. Pharmacol. 2006, 72, 1010-1021. https://doi.org/10.1016/j.bcp.2006.07.016

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