Journal of Physiology & Pathology in Korean Medicine (동의생리병리학회지)

The Physiological Society of Korean Medicine and The Society of Pathology in Korean Medicine (대한동의생리학회·한의병리학회)
권호 표지

Suppressive Effect of FARFARE FLOS Extracts on Oxidative Stress and Inflammatory Response through the Antioxidative Mechanism

FARFARE FLOS의 항산화 기전을 통한 산화적 스트레스 및 염증 반응 억제효과

  • Shin, Seung-An (Department of Diagnostics, College of Oriental Medicine, Dongguk University) ;
  • Lee, Min-Ja (Institute of Oriental Medicine, College of Oriental Medicine, Dongguk University) ;
  • Lee, Hye-Sook (Department of Diagnostics, College of Oriental Medicine, Dongguk University) ;
  • Park, Won-Hwan (Department of Diagnostics, College of Oriental Medicine, Dongguk University)
  • 신승안 (동국대학교 한의과대학 진단학교실) ;
  • 이민자 (동국대학교 한의과대학 한의학연구소) ;
  • 이혜숙 (동국대학교 한의과대학 진단학교실) ;
  • 박원환 (동국대학교 한의과대학 진단학교실)
  • Received : 2011.02.07
  • Accepted : 2011.04.11
  • Published : 2011.04.25
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Abstract

There is currently increased interest in the identification of antioxidant compounds that are pharmacologically potent and have low or no side effects. Plants produce significant amounts of antioxidants to prevent the oxidative stress caused by photons and oxygen, therefore they represent a potential source of new compounds with antioxidant activity. FARFARE FLOS has been frequently used on the respiratory system including bronchitis, phthisis. In this study, the antioxidant activity of extract from FF was studied in vitro methods by measuring the antioxidant activity by TEAC, measuring the scavenging effects on reactive oxygen species (ROS) [superoxide anion, hydroxyl radical] and on reactive nitrogen species (RNS) [nitric oxide and peroxynitrite] as well as measuring the inhibitory effect on Cu2+-induced human LDL oxidation. The FF extracts were found to have a potent scavenging activity, as well as an inhibitory effect on LDL oxidation. And this study was designed to evaluate whether FFEA may ameliorate oxidative stress and inflammatory status through the antioxidative mechanism in LPS-stimulated RAW 264.7 murine macrophage cell line. Treatment of RAW 264.7 cells with FFEA significantly reduced LPS-stimulated inflammatory response in a dose-dependent manner. In conclusion, the FF extracts have anti-oxidative and anti-inflammatory effects in vitro system, which can be used for developing pharmaceutical drug against oxidative stress and atherosclerosis.

Keywords

References

  1. 2009년 사망원인 통계 결과, 통계청, 2010.
  2. Aruoma, O.I., Free, radicals, oxidative stress and antioxidants in human health and disease. J Am Oil Chem Soc. 75: 199-212, 1998. https://doi.org/10.1007/s11746-998-0032-9
  3. Finkel, T., Holbrook, N.J. Oxidants, oxidative stress and the biology of ageing. Nature 408(6809):239-247, 2000. https://doi.org/10.1038/35041687
  4. Libby, P. Inflammation in atherosclerosis. Nature, 420:868-874, 2002. https://doi.org/10.1038/nature01323
  5. Ross, R. Atherosclerosis-An Inflammatory Disease. N Engl J Med. 340(2):115-126, 1999. https://doi.org/10.1056/NEJM199901143400207
  6. Blokhina, O., Virolainen, E., Fagerstedt, K.V. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot. 91: 179-194, 2003. https://doi.org/10.1093/aob/mcf118
  7. Delledonne, M., Polverari, A., Murgia, I. The functions of nitric oxide mediated signalling and changes in gene expression during the hypersensitive response. Antioxid. Redox Signal. 5: 33-41, 2003. https://doi.org/10.1089/152308603321223522
  8. Ali, K.A., Abdelhak, M., George, B., Panagiotis, K. Tea and herbal infusions: Their antioxidant activity and phenolic propolis. Food Chem. 89: 27-36, 2005. https://doi.org/10.1016/j.foodchem.2004.01.075
  9. Barene, A.L. Toxicological and biochemistry of butylated hydroxyanisole and butylated hydroxytoluene. J Am Oil Chem Soc. 52: 59-63, 1975. https://doi.org/10.1007/BF02901825
  10. Nakayama, M., Suzuki, K., Toda, M., Okubo, S., Hara, Y., Shimamura, T. Inhibition of the infectivity of influenza virus by tea polyphenols. Antiviral Res. 21: 289-299, 1993. https://doi.org/10.1016/0166-3542(93)90008-7
  11. Hsieh, T.C., Wu, J.M. Differential effects on growth, cell cycle arrest, and induction of apoptosis by resveratrol in human prostate cancer cell lines. Experimental Cell Res., 25: 109-115, 1999.
  12. Pal, S., Choudhuri, T., Chattopadhyay, S., Bhattacharya, A., Datta, G.K., Das, T., Sa, G. Mechanisms of curcumin-induced apoptosis of Ehrlich's ascites carcinoma cells. Biochem Biophys Res Commun, 288: 658-665, 2001. https://doi.org/10.1006/bbrc.2001.5823
  13. 전국한의과대학본초학교수 공편저, 본초학. 서울, 영림사, p 194, 2000.
  14. 한방약리학 교재편찬위원회 저, 한방약리학. 서울, 신일상사, pp 145-148, 2006.
  15. Song, G.S., Ahn, B.Y., Lee, K.S., Maeng, I.K., Choi, D.S. Effect of Hot Water Extracts from Medicinal Plants on the Mutagenicity of Indirect Mutagens. KOREAN J. FOOD SCI. TECHNOL. 29(6):1288-1294, 1997.
  16. Lee, K.T., Kim, B.J., Kim, J.H., Heo, M.Y., Kim, H.P. Biological screening of 100 plant extracts for cosmetic use (I): inhibitory activities of tyrosinase and DOPA auto-oxidation. Int J Cosmet Sci. 19(6):291-298, 1997. https://doi.org/10.1111/j.1467-2494.1997.tb00193.x
  17. Lim, H.J., Lee, H.S., Ryu, J.H. Suppression of inducible nitric oxide synthase and cyclooxygenase-2 expression by tussilagone from Farfarae flos in BV-2 microglial cells. Arch Pharm Res. 31(5):645-652, 2008. https://doi.org/10.1007/s12272-001-1207-4
  18. Turker, A.U., Usta, C. Biological screening of some Turkish medicinal plant extracts for antimicrobial and toxicity activities. Nat Prod Res. 22(2):136-146, 2008. https://doi.org/10.1080/14786410701591663
  19. Cho, J., Kim, H.M., Ryu, J.H., Jeong, Y.S., Lee, Y.S., Jin, C. Neuroprotective and antioxidant effects of the ethyl acetate fraction prepared from Tussilago farfara L. Biol Pharm Bull. 28(3):455-460, 2005. https://doi.org/10.1248/bpb.28.455
  20. Kujala, T.S., Loponen, J.M., Klika, K.D., Pihlaja, K. Phenolic and betacyanins in red beetroot (Beta vulgaris) root: distribution and effects of cold storage on the content of total phenolics and three individual compounds. J Agri Food Chem. 48: 5338-5342, 2000. https://doi.org/10.1021/jf000523q
  21. Roberta, R.E., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med, 26: 1231-1237, 1999. https://doi.org/10.1016/S0891-5849(98)00315-3
  22. Miller, N.J., Rice-Evans, C., Davies, M.J., Gopinathan, V., Milner, A.A. A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci. 84: 407-412, 1993. https://doi.org/10.1042/cs0840407
  23. Blois, M.S. Antioxidant determination by the use of stable free radical. Nature 26: 1199-1200, 1958.
  24. Gotoh, N., Niki, E. Rates of interactions of superoxide with vitamin E, vitamin C and related compounds as measured by chemiluminescence. Biochem Biophys Acta 1115: 201-207, 1992. https://doi.org/10.1016/0304-4165(92)90054-X
  25. Halliwell, B., Gutteridge, J.M. Role of free radicals and catalytic metalions in human disease: an overview. Method Enzymol. 186: 1-85, 1990.
  26. Nagata, N., Momose, K., Ishida, Y. Inhibitory effects of catecholamines and anti-oxidants on the fluorescence reactionof 4,5-diaminofluorescein, DAF-2, a novel indicator of nitric oxide. J Biochem. (Tokyo) 125: 658-661, 1999. https://doi.org/10.1093/oxfordjournals.jbchem.a022333
  27. Crow, J.P. Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide 1: 145-157, 1997. https://doi.org/10.1006/niox.1996.0113
  28. Yoon, M.A., Jeong, T.S., Park, D.S., Xu, M.Z., Oh, H.W., Song, K.B., Lee, W.S., Park, H.Y. Antioxidant effect of quinoline alkaloid and 2,4-di-tert-butylphenol isolated from Scolopendra subspinipes. Biol Pharm Bull. 29: 735-739, 2006. https://doi.org/10.1248/bpb.29.735
  29. Yagi, K.A. Simple fluometric assay for lipoperoxide in blood plasma. Biochem Med. 15: 212-216, 1976. https://doi.org/10.1016/0006-2944(76)90049-1
  30. Kahkonen, M.P., Hopia, A.I., Vuorela, H.J., Rauha, J.P., Pihlaja, K., Kujala, T.S., et al. Antioxidant activity of plant extracts containing phenolic compounds. J Agri Food Chem. 47: 3954-3962, 1999. https://doi.org/10.1021/jf990146l
  31. Kaur, C., Kapoor, H.C. Anti-oxidant activity and total phenolic content of some Asian vegetables. Int J Food Sci Tech. 37: 153-161, 2002. https://doi.org/10.1046/j.1365-2621.2002.00552.x
  32. Maisuthisakul, P., Suttajit, M., Pongsawatmanit, R. Assessment of phenolic content and free radical-scavenging capacity of some Thai indigenous plants. Food Chem. 100(4):1409-1418, 2007. https://doi.org/10.1016/j.foodchem.2005.11.032
  33. Yao, P., Nussler, A., Liu, L., Hao, L., Song, F., Schirmeier, A., et al. Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways. J Hepatol. 47(2):253-261, 2007. https://doi.org/10.1016/j.jhep.2007.02.008
  34. Rice-Evans, C., Miller, N., Paganga, G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med. 20: 933-956, 1996. https://doi.org/10.1016/0891-5849(95)02227-9
  35. Fogliano, V., Verde, V., Randazzo, G., Ritieni, A. Method for measuring antioxidant activity and its application to monitoring the antioxidant capacity of wines. J Agric Food Chem. 47: 1035-1040, 1999. https://doi.org/10.1021/jf980496s
  36. Molyneux, P. The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. J Sci Tech. 26: 211-219, 2004.
  37. 남석현, 강미영. 한약재 열수추출물의 항산화효과 검정. 한국농화학회지 43: 141-147, 2000.
  38. Sanchez, C.S., Gonzalez, A.M.T., Garcia-Parrilla, M.C., Granados, J.J.Q., Serrana, H.L.G., Martinez, M.C.L. Different radical scavenging tests in virgin olive oil and their relation to the total phenol content. Anal Chim Acta 593: 103-107, 2007. https://doi.org/10.1016/j.aca.2007.04.037
  39. Magalhaes, L.M., Segundo, M.A., Reis, S. Automatic method for determination of total antioxidant capacity using 2,2-diphenyl-1- picrylhydrazyl assay. Anal Chin Acta 558: 310-318, 2006. https://doi.org/10.1016/j.aca.2005.11.013
  40. Okawa, M., Kinjo, J., Nohara, T., Ono, M. DPPH (1,1-diphenyl- 2-picrylhydrazyl) radical scavenging activity of flavonoids obtained from some medicinal plants. Biol Pharm Bull. 24(10):1202-1205, 2001. https://doi.org/10.1248/bpb.24.1202
  41. Halliwell, B., Chirico, S. Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr, 57: 715-725, 1993. https://doi.org/10.1093/ajcn/57.5.715S
  42. Fang, Y.Z., Yang, S., Wu, G. Free radicals, antioxidants, and nutrition. Nutrition. 18: 872-879, 2002. https://doi.org/10.1016/S0899-9007(02)00916-4
  43. Frankel, E.N., Huang, S.W., Aeschbach, R. Antioxidant activity of green teas in different lipid systems. J Am Oil Chem Soc. 74: 1309-1315, 1997. https://doi.org/10.1007/s11746-997-0062-8
  44. Wrona, M., Patel, K., Wardman, P. Reactivity of 2′,7′ -dichloro dihydro fluorescein and dihydrorhodamine 123 and their oxidized forms toward carbonate, nitrogen dioxide, and hydroxyl radicals. Free Radic Biol Med. 38(2):262-270, 2005. https://doi.org/10.1016/j.freeradbiomed.2004.10.022
  45. Patel, R.P., McAndrew, J., Sellak, H., White, C.R., Jo, H., Freeman, B.A., Darley-Usmar, V.M. Biological aspects of reactive nitrogen species. Biochem Biophys Acta 1411: 385-400, 1999. https://doi.org/10.1016/S0005-2728(99)00028-6
  46. Pfeilschifter, J., Eberhardt, W., Hummel, R., Kunz, D., Muhl, H., Nitsch, D., Pluss, C., Walker, G. Therapeutic strategies for the inhibition of inducible nitric oxide synthase-potential for a novel class of anti-inflammatory agents. Cell Biol Int. 20: 51-58, 1996. https://doi.org/10.1006/cbir.1996.0008
  47. Salvemini, D., Misko, T.P., Masferrer, J.L., Seibert, K., Currie, M.G., Needleman, P. Nitric oxide activates cyclooxygenase enzymes. Proc Natl Acad Sci USA 90: 7240-7244, 1993. https://doi.org/10.1073/pnas.90.15.7240
  48. McCartney-Francis, N., Allen, J.B., Mizel, D.E., Albina, J.E., Xie, Q.W., Nathan, C.F., Wahl, S.M. Suppression of arthritis by an inhibitor of nitric oxide synthase. J Exp Med. 178: 749-754, 1993. https://doi.org/10.1084/jem.178.2.749
  49. Wolfe, T.A., Dasta, J.F. Use of nitric oxide synthase inhibitors as a novel treatment for septic shock. Ann Pharmacother. 29: 36-46, 1995. https://doi.org/10.1177/106002809502900108
  50. Virag, L., Szabo, E., Gergely, P., Szabo, C. Peroxynitrite induced cytotoxicity: metabolism and opportunities for intervention. Toxocol Lett. 140-141: 113-124, 2003. https://doi.org/10.1016/S0378-4274(02)00508-8
  51. Rubbo, H., O'Donnell, V. Nitric oxide, peroxynitrite and lipoxygenase in atherogenesis: mechanistic insights. Toxicology, 208: 273-288, 2005. https://doi.org/10.1016/j.tox.2004.11.023
  52. Fredrikson, G., Bjorkbacka, H., Ljungcrantz, I., Soderberg, I., Chyu, K.Y., Shah, P., Nilsson, J. Inhibition of atherosclerosis by apo B peptide vaccins in LDL receptor deficient mice expressing human apo B-100. Atherosclerosis Supplements, 9(1):38-39, 2008.
  53. Chen, C.Y., Milbury, P.E., Chung, S.K., and Blumberg, J. Effect of almond skin polyphenolics and quercetin on human LDL and apolipoprotein B-100 oxidation and conformation. J Nutr Biochem. 18(12):785-794, 2007. https://doi.org/10.1016/j.jnutbio.2006.12.015
  54. Witzum, J.L. The role of monocytes and oxidized LDL in atherosclerosis. In: Atherosclerosis Reviews. Leaf A. Weber PC. (eds). Ravan Press, New York, USA. 21: 59-69, 1990.
  55. Rotheneder, M., Puhl, H., Waeg, G., Striegl, G., Esterbauer, H. Effect of oral supplementation with $D-{\alpha}-tocopherol$ on the vitamin E content of human low density lipoprotein and resistance to oxidation. J Lipid Res. 32: 1325-1332, 1991.
  56. Meng, Q., Lewis, P., Wahala, K., Adlercreutz, H., Tikkanen. Incorporation of esterified soybean isoflavone with antioxidant activity into low density lipoprotein. Biochim. Biophys. Acta. 1438: 369-376, 1996.
  57. Chen, T.Y., Pan, B.S. Ex vivo inhibitory effect on tilapia LDL oxidation and hypolipidemia properties of Glycine tomentella root extract. Comp Biochem Physiol Part A 148: 189-195, 2007. https://doi.org/10.1016/j.cbpa.2007.04.004
  58. Djordjevic, V.B. Free Radicals in Cell Biology. Int Rev Cytol, 237: 57-89, 2004.
  59. Liu, Y.H., Lin, S.Y., Lee, C.C., Hou W.C. Antioxidant and nitric oxide production inhibitory activities of galacturonyl hydroxamic acid. Food Chem. 109(1):159-166, 2008. https://doi.org/10.1016/j.foodchem.2007.12.055
  60. Yoshitake, J., Kato, K., Yoshioka, D., Sueishi, Y., Sawa, T., Akaike, T., Yoshimura, T. Suppression of NO production and 8-nitroguanosine formation by phenol-containing endocrine-disrupting chemicals in LPS-stimulated macrophages: Involvement of estrogen receptor-dependent or -independent pathways. Nitric Oxide, 18(3):223-228, 2008. https://doi.org/10.1016/j.niox.2008.01.003
  61. Shin, E.M., Zhou, H.Y., Guo, L.Y., Kim, J.A., Lee, S.H., Merfort, I., Kang, S.S., Kim, H.S., Kim, S.H., Kim, Y.S. Anti-inflammatory effects of glycyrol isolated from Glycyrrhiza uralensis in LPS-stimulated RAW264.7 macrophages. Int Immunopharm. 8(11):1524-1532, 2008. https://doi.org/10.1016/j.intimp.2008.06.008
  62. Wang, H., Gao, J., Koua, J., Zhua, D., Yu, B. Anti-inflammatory activities of triterpenoid saponins from Polygala japonica. Phytomedicine 15: 321-326, 2008. https://doi.org/10.1016/j.phymed.2007.09.014
  63. Hsieh, Y.H., Kuo, P.M., Chien, S.C., Shyur, L.F., Wang, S.Y. Effects of Chamaecyparis formosensis Matasumura extractives on lipopolysaccharide-induced release of nitric oxide. Phytomedicine 14(10):675-680, 2007. https://doi.org/10.1016/j.phymed.2006.11.029
  64. Suh, S.J., Chung, T.W., Son, M.J., Kim, S.H., Moon, T.C., Son, K.H., Kim, H.P., Chang, H.W., Kim, C.H. The naturally occurring biflavonoid, ochnaflavone, inhibits LPS-induced iNOS expression, which is mediated by ERK1/2 via $NF-{\kappa}B$ regulation, in RAW264.7 cells. Arch Biochem Biophys. 447(2):136-146, 2006. https://doi.org/10.1016/j.abb.2006.01.016
  65. Vasquez-Vivar, J., Whitsett, J., Ionova, I., Konorev, E., Zielonka, J., Kalyanaraman, B., Shi, Y., Pieper, G.M. Cytokines and lipopolysaccharides induce inducible nitric oxide synthase but not enzyme activity in adult rat cardiomyocytes. Free Radic Biol Med. 45(7):994-1001, 2008. https://doi.org/10.1016/j.freeradbiomed.2008.06.017
  66. Simon, L.S. Role of regulation of cyclooxygenase-2 during inflammation. Am J Med. 106: 37S-42S, 1999. https://doi.org/10.1016/S0002-9343(99)00115-1
  67. Wendehenne, D., Dussably, A., Jeannin, E.F., Pugin, A. Nitric oxide: Chemistry and bioactivity in animal and plant cells. Studies in Natural Products Chem. 26(7):909-963, 2002.
  68. Ziolo, M.T., Kohr, M.J., Wang, H. Nitric oxide signaling and the regulation of myocardial function. J Mol Cell Cardiol. 45(5):625-632, 2008. https://doi.org/10.1016/j.yjmcc.2008.07.015
  69. Rees, M.D., Kennett, E.C., Whitelock, J.M., Davies, M.J. Oxidative damage to extracellular matrix and its role in human pathologies. Free Radic Biol Med. 44(12):1973-2001, 2008. https://doi.org/10.1016/j.freeradbiomed.2008.03.016
  70. Kolodziej, H., Burmeister, A., Trun, W., Radtke, O.A., Kiderlen, A.F., Ito, H., Hatano, T., Yoshida, T., Foo, L.Y. Tannins and related compounds induce nitric oxide ynthase and cytokines gene expressions in Leishmania major-infected macrophage-like RAW 264.7 cells. Bioorg Med Chem, 13(23):6470-6476, 2005. https://doi.org/10.1016/j.bmc.2005.07.012
  71. Tsatsanis, C., Androulidaki, A., Venihaki, M., Margioris, A.N. Signalling networks regulating cyclooxygenase-2. Int J Biochem Cell Biol. 38(10):1654-1661, 2006. https://doi.org/10.1016/j.biocel.2006.03.021
  72. Rios, J.L., Recio, M.C. Natural products as modulators of apoptosis and their role in inflammation. Studies in Natural Products Chem. 33(13):141-192, 2006.
  73. Gorczynski, R.M. Understanding classical conditioning of immune responses. Neuro Immune Biology 1: 237-254, 2005.