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Antioxidant, Anticancer and Immune Activation of Anthocyanin Fraction from Rubus coreanus Miquel fruits (Bokbunja)

복분자 안토시아닌 분획의 항산화, 항암 및 면역증진 효과

  • Choung, Myoung-Gun (Department of Herbal Medicine Resource, Kangwon National University) ;
  • Lim, Jung-Dae (Department of Herbal Medicine Resource, Kangwon National University)
  • 정명근 (강원대학교 생약자원개발학과) ;
  • 임정대 (강원대학교 생약자원개발학과)
  • Received : 2012.08.05
  • Accepted : 2012.08.10
  • Published : 2012.08.30

Abstract

This study was performed to determined the antioxidant activities, anticancer and immuno-activities of anthocyanin fraction from Rubus coreanus Miquel fruits (Bokbunja). Anthocyanin fraction extracted from Bokbunja revealed the presence of three anthocyanin components, which were tentatively identified as cyanidin 3-O-sambubioside, cyanidin 3-O-xylosylrutinoside and cyanidin 3-O-rutinoside using RP-HPLC/DAD/MS. The anthocyanin fraction from Bokbunja always showed reducing power and high scavenging activities against DPPH, hydroxy radical (OH) and superoxide anion radical ($O_2{^-}$) similar to general synthetic antioxidant and polyphenol compounds from plant origin. Anthocyanin fraction from Bokbunja showed high inhibition on proliferation of LNCaP and A549 cells and did not inhibit the proliferation of other cancer cells. Immuno-activities of Anthocyanin fraction from Bokbunja were investigated, it showed high promotion of human B and T cells growth about 50% and secretion of IL-6 and TNF-${\alpha}$ by treatment after 6 days. Over all, the result of the study suggest that anthocyanin fraction from Bokbunja displays antioxidant activity comparable to that general synthetic antioxidant, also, anthocyanin fraction from Bokbunja are expected to be good candidate for development into source of anticaner and immuno-activator agent in food industry.

Keywords

References

  1. Acquaviva R, Russo A and Galvano F. (2003). Cyanidin and cyanidin 3-O-beta-D-glucoside as DNA cleavage protectors and antioxidants. Cell Biology and Toxicology. 19:243-252. https://doi.org/10.1023/B:CBTO.0000003974.27349.4e
  2. Ames BN, Shigenaga MK and Hagen TM. (1993). Oxidants, antioxidants, and the degenerative diseases of aging. Proceedings of the National Academy of Sciences of the United states of America. 90:7915-7922. https://doi.org/10.1073/pnas.90.17.7915
  3. Baeuerle PA and Baichwal VR. (1997). NF-kappa B as a frequent target for immunosuppressive and anti-inflammatory molecules. Advances in Immunology. 65:111-137. https://doi.org/10.1016/S0065-2776(08)60742-7
  4. Byamukama R, Kiremire BT, Andersen OM and Steigen A. (2005). Anthocyanins from fruits of Rubus pinnatus and Rubus rigidus. Journal of Food Composition and Analysis. 18:599- 605. https://doi.org/10.1016/j.jfca.2004.04.007
  5. Calfee-Mason KG, Spear BT and Glauert HP. (2002). Vitamin E inhibits hepatic NF-${\kappa}B$ activation in rats administered the hepatic tumor promoter, phenobarbital. Journal of Nutrition. 132:3178-3185.
  6. Cha HS, Youn AR, Park PJ, Choi HR and Kim BS. (2007). Physiological characteristics of Rubus coreanus Miquel during maturation. Korean Journal of Food Science and Technology. 39:476-479.
  7. Chen F, Sun Y, Zhao G, Liao X, Hu X, Wu J and Wang Z. (2007). Optimization of ultrasound-assisted extraction of anthocyanins in red raspberries and identification of anthocyanins in extract using high performance liquid chromatography mass spectrometry. Ultrasonics Sonochemistry. 14:767-778. https://doi.org/10.1016/j.ultsonch.2006.12.011
  8. Choung MG. (2004). Analysis of anthocyanins. Korean Journal of Crop Science. 49(S):55-67.
  9. Chung HY, Baek BS, Song SH, Kim MS, Huh JI, Shim KH, Kim KW and Lee KH. (1997). Xanthine dehydrogenase/ xanthine oxidase and oxidative stress. Age. 20:127-140. https://doi.org/10.1007/s11357-997-0012-2
  10. Felgines C, Texier O, Besson C, Fraisse D, Lamaison JL and Rémésy C. (2002). Blackberry anthocyanins are slightly bioavailable in rats. Journal of Nutrition. 132:1249-1253. https://doi.org/10.1093/jn/132.6.1249
  11. Halliwell B, Gutteridge JM and Aruoma OI. (1987). The deoxyribose method: a simple "test-tube" assay for determination of rate constants for reactions of hydroxy radicals. Analytical Biochemisry. 165:215-219 https://doi.org/10.1016/0003-2697(87)90222-3
  12. Hollman PC. (2001). Evidence for health benefits of plant phenol: local or systemic effects? Journal of the Science of Food and Agriculture. 81:842-852. https://doi.org/10.1002/jsfa.900
  13. Jeong HS, Han JG, Ha JH, Kim Y, OH SH, KIm SS, Jeong MH, Choi GP, Park UY and Lee HY. (2009). Antioxidant activities and skin-whitening effects of nano-encapsuled water extract from Rubus coreanus Miquel. Korean Journal of Medicinal Crop Science. 17:83-89.
  14. Joo NM, Lee SM and Jeong HS. (2009). Optimization of jelly made with Rubus coreanus (Bokbunja) using response surface methodology. Journal of Food Science and Nutrition. 14:148- 155. https://doi.org/10.3746/jfn.2009.14.2.148
  15. Jung GT, Ju IO, Choi JS and Hong JS. (2000). The antioxidative, antimicrobial and nitrite scavenging effects of Schizandra chinensis RUPRECHT (Omija) seed. Korean Journal of Food Science and Technology. 32:928-935.
  16. Kim EJ, Lee YJ, Shin HK and Park JH. (2005). Induction of apoptosis by the aqueous extract of Rubus coreanum in HT-29 human colon cancer cells. Nutrition. 21(11-12):1141-1148. https://doi.org/10.1016/j.nut.2005.02.012
  17. Kim MK, Jin YS, Heo SI, Shim TH, Sa JH and Wang MH. (2006). Studies for component analysis and antioxidant effect, antimicrobial activity in Acanthopanax senticosus HARMS. Korean Journal of Pharmacognosy. 37:151-156.
  18. Kim SH, Chung HG, Jang YS, Park YK, Park HS and Kim SC. (2005). Characteristics and screening of antioxidative activity for the fruits by Rubus coreanus Miq. clones. Journal of Korean Forest Society. 94:11-15.
  19. Kim TG, Park MS, Han HM, Kang SY, Jung KK, Rheu HM and Kim SH. (1999). Inhibitory effects of Terminalia chebula, Sanguisorba officinalis, Rubus coreanus and Rheum palmatum on Hepatitis B virus replication in HepG2 2.2.15 cells. Yakhak Hoeji. 43:458-463.
  20. Kim YC and Chung SK. (2002). Reactive oxygen radical species scavenging effects of Korean medicinal plant leaves. Food Science and Biotechnology. 11:407-411.
  21. Korycka-Dahl M, Richardson T and Hicks CL. (1979). Superoxide dismutase activity in bovine milk serum and its relevance for oxidative stability of milk. Journal of Food Protection. 42: 867-871. https://doi.org/10.4315/0362-028X-42.11.867
  22. Ku CS and Mun SP. (2008a) Optimization of the extraction of anthocyanin from Bokbunja (Rubus coreanus Miq.) marc produced during traditional wine processing and characterization of the extracts. Bioresource Technology. 99:8325-8330. https://doi.org/10.1016/j.biortech.2008.03.013
  23. Ku CS and Mun SP. (2008b) Antioxidant activities of ethanol extracts from seeds in fresh Bokbunjda (Rubus coreanus Miq.) and wine processing waste. Bioresource Technology. 99:4503- 4509. https://doi.org/10.1016/j.biortech.2007.08.063
  24. Kwon JW, Lee HK, Park HJ, Kwon TO, Choi HR and Song JY. (2011). Screening of biological activities to different ehtanol extracts of Rubus coreanus Miq. Korean Journal of Medicinal Crop Science. 19:325-333. https://doi.org/10.7783/KJMCS.2011.19.5.325
  25. Lazze M, Pizzala R, Savio M, Stivala L, Prosperi E and Bianchi L. (2003). Anthocyanins protect against DNA damage induced by tert-butyl-hydroperoxide in rat smooth muscle and hepatoma cells. Mutation Research. 53:103-115.
  26. Lee MK, Lee HS, Choi GP, Oh DH, Kim JD, Yu CH and Lee HY. (2003). Screening of biological activities of the extracts from Rubus coreanus Miq. Korean Journal of Medicinal Crop Science. 11:5-12.
  27. Lee SO, Lee HJ, Yu MH, Im HG and Lee IS. (2005). Total polyphenol contents and antioxidant activities of methanol extracts from vegetables produced in Ullung island. Korean Journal of Food Science and Technology. 37:233-240.
  28. Lefevre M, Howard L, Most M, Ju Z and Delany J. (2004). Microarray analysis of the effects of grape anthocyanins on hepatic gene expression in mice. The FASEB Journal. 18:A851. https://doi.org/10.1096/fj.03-0637fje
  29. Li N and Karin M. (1999). Is NF-${\kappa}B$ the sensor of oxidative stress? The FASEB Journal. 13:1137-1143. https://doi.org/10.1096/fasebj.13.10.1137
  30. Nagai T, Nagashima T, Suzuki N and Inoue R. (2005). Antioxidant activity and angiotensin I-converting enzyme inhibition by enzymatic hydrolysates from bee bread. Zeitschrift fur Naturforschung. 60:133-138.
  31. Oyaizu M. (1986). Studies on product of browning reaction prepared from glucosamine. Japanese Journal of Nutrition. 44:307-315. https://doi.org/10.5264/eiyogakuzashi.44.307
  32. Park JH, Lee HS, Mun HC, Kim DH, Seong NS, Jung JK, Bang JK and Lee HY. (2004). Effect of ultrasonification process on enhancement of immuno-stimulatory activity of Ephedera sinica Stapf and Rubus coreanus Miq. Korean Journal of Biotechnology and Bioengineering. 19:113-117.
  33. Park JH, Oh SM, Lim SS, Lee YS, Shin HK, Oh YS, Choe NH, Park HY and Kim JK. (2006). Induction of heme oxygenase-1 mediates the anti-inflammatory effects of the ethanol extract of Rubus coreanus in murine macrophages. Biochemical and Biophysical Research Communications. 351:146-152 https://doi.org/10.1016/j.bbrc.2006.10.008
  34. Park YE, Jeong JC, Cho HM, Hwang YS, Lee HJ, Choi SS, Lee SJ, Park ES, Ko EA, Kim NS, Lim JD and Choung MG. (2008). Amntimutagenic effect and cytotoxicity to human cancer cell lines of colored potato extracts. Korean Journal of Crop Science. 53:75-84.
  35. Park YS, Kim BW, Kim TC, Jang HG, Chon SU, Cho JY, Jiang SH and Heo BG. (2008). Physiological activity of methanol extracts from Korean kiwifruits. Korean Journal of Horticultural Science and Technology. 26:495-500.
  36. Ramirez-Tortosa C, Andersen O and Gardner P. (2001). Anthocyanin-rich extract decreases indices of lipid peroxidation and DNA damage in vitamin E depleted rats. Free Radical Biology and Medicine. 31:1033-1037. https://doi.org/10.1016/S0891-5849(01)00618-9
  37. Rice-Evans CA, Miller N and Paganga G. (1996). Structure antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biology and Medicine. 20:933-956. https://doi.org/10.1016/0891-5849(95)02227-9
  38. Rossi A, Serraino I and Dugo P. (2003). Protective effects of anthocyanins from blackberry in a rat model of acute lung inflammation. Free Radical Research. 37:891-900. https://doi.org/10.1080/1071576031000112690
  39. Shin TY, Kim SH, Lee ES, Eom DO and Kim HM. (2002). Action of Rubus coreanus extract on systemic and local anaphylaxis. Phytotherapy Research. 16:508-513. https://doi.org/10.1002/ptr.925
  40. Song HS, Lee YJ, Kim SK, Moon WK, Kim DW, Kim YS and Moon KY. (2004). Downregulatory effect of AGI-1120 ($\alpha$- glucosidase inhibitor) and chaga mushroom (Inonotus obliquus) on cellular NF-${\kappa}B$ activation and their antioxidant activity. Korean Journal of Pharmacognosy. 35:92-97.
  41. Tian Q, Giusti MM, Stoner GD and Schwartz SJ. (2006). Characterization of a new anthocyanin in black raspberries (Rubus occidentalis) by liquid chromatography electrospray ionization tandem mass spectrometry. Food Chemistry. 94:465- 468. https://doi.org/10.1016/j.foodchem.2005.01.020
  42. Triantis T, Stelakis A, Dimotikali D and Papadopoulos K. (2005). Investigations on the antioxidant activity of fruit and vegetable aqueous extracts on superoxide radical anion using chemiluminescence techniques. Analytica Chimica Acta. 536:101-105. https://doi.org/10.1016/j.aca.2004.11.048
  43. Wu X, Cao G and Prior RL. (2002). Absorption and metabolism of anthocyanins in elderly women after consumption of elderberry or blueberry. Journal of Nutrition. 132:1865-1871. https://doi.org/10.1093/jn/132.7.1865
  44. Yoo KM, Kim DO and Lee CY. (2007). Evaluation of different methods of antioxidant measurement. Food Science and Biotechnology. 16:177-182.
  45. Yoon I, Cho JY, Kuk JH, Wee JH, Jang MY, Ahn TH and Park KH. (2002). Identification and activity of antioxidative compounds from Rubus coreanum fruit. Korean Journal of Food Science and Technology. 34:898-904.
  46. Yoon I, Wee JH, Moon JH, Ahn TH and Park KH. (2003). Isolation and identification of quercetin with antioxidative activity from the fruits of Rubus coreanus Miquel. Korean Journal of Food Science and Technology. 35:499-502.

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