Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
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Whitening and inhibiting NF-κB-mediated inflammation properties of the biotransformed green ginseng berry of new cultivar K1, ginsenoside Rg2 enriched, on B16 and LPS-stimulated RAW 264.7 cells

  • Xu, Xing Yue (Graduate School of Biotechnology, and College of Life Science, Kyung Hee University) ;
  • Yi, Eun Seob (Graduate School of Biotechnology, and College of Life Science, Kyung Hee University) ;
  • Kang, Chang Ho (Division of Applied Life Science and PMBBRC, Gyeongsang National University) ;
  • Liu, Ying (Graduate School of Biotechnology, and College of Life Science, Kyung Hee University) ;
  • Lee, Yeong-Geun (Graduate School of Biotechnology, and College of Life Science, Kyung Hee University) ;
  • Choi, Han Sol (Graduate School of Biotechnology, and College of Life Science, Kyung Hee University) ;
  • Jang, Hyun Bin (Graduate School of Biotechnology, and College of Life Science, Kyung Hee University) ;
  • Huo, Yue (Graduate School of Biotechnology, and College of Life Science, Kyung Hee University) ;
  • Baek, Nam-In (Graduate School of Biotechnology, and College of Life Science, Kyung Hee University) ;
  • Yang, Deok Chun (Graduate School of Biotechnology, and College of Life Science, Kyung Hee University) ;
  • Kim, Yeon-Ju (Graduate School of Biotechnology, and College of Life Science, Kyung Hee University)
  • Received : 2020.07.08
  • Accepted : 2021.02.19
  • Published : 2021.11.15
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Abstract

Background: Main bioactive constituents and pharmacological functions of ripened red ginseng berry (Panax ginseng Meyer) have been frequently reported. Yet, the research gap targeting the beneficial activities of transformed green ginseng berries has not reported elsewhere. Methods: Ginsenosides of new green berry cultivar K-1 (GK-1) were identified by HPLC-QTOF/MS. Ginsenosides bioconversion in GK-1 by bgp1 enzyme was confirmed with HPLC and TLC. Then, mechanisms of GK-1 and β-glucosidase (bgp1) biotransformed GK-1 (BGK-1) were determined by Quantitative Reverse Transcription-Polymerase Chain Reaction and Western blot. Results: GK-1 possesses highest ginsenosides especially ginsenoside-Re amongst seven ginseng cultivars including (Chunpoong, Huangsuk, Kumpoong, K-1, Honkaejong, Gopoong, and Yunpoong). Ginseng root's biomass is not affected with the harvest of GK-1 at 3 weeks after flowering period. Then, Re is bioconverted into a promising pharmaceutical effect of Rg2 via bgp1. According to the results of cell assays, BGK-1 shows decrease of tyrosinase and melanin content in α-melanocyte-stimulating hormone challenged-murine melanoma B16 cells. BGK-1 which is comparatively more effective than GK-1 extract shows significant suppression of the nuclear factor (NF)-κB activation and inflammatory target genes, in LPS-stimulated RAW 264.7 cells. Conclusion: These results reported effective whitening and anti-inflammatory of BGK-1 as compared to GK-1.

Keywords

Acknowledgement

This work was supported by the Rural Development Administration grant "Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ013173))", and grant from Basic Science Research Program through National Research Foundation of Korea by Ministry of Education (2019R1A2C1010428), Republic of Korea.

References

  1. Jang HJ, Han IH, Kim YJ, Yamabe N, Lee D, Hwang GS, et al. Anticarcinogenic effects of products of heat-processed ginsenoside Re, a major constituent of ginseng berry, on human gastric cancer cells. J Agric Food Chem 2014;62:2830-6. https://doi.org/10.1021/jf5000776.
  2. Jimenez Z, Kim Y-J, Mathiyalagan R, Seo K-H, Mohanan P, Ahn J-C, et al. Assessment of radical scavenging, whitening and moisture retention activities of Panax ginseng berry mediated gold nanoparticles as safe and efficient novel cosmetic material. Artif Cells, Nanomedicine, Biotechnol 2018;46:333-40. https://doi.org/10.1080/21691401.2017.1307216.
  3. Kim J, Cho SY, Kim SH, Cho D, Kim S, Park CW, et al. Effects of Korean ginseng berry on skin antipigmentation and antiaging via FoxO3a activation. J Ginseng Res 2017;41:277-83. https://doi.org/10.1016/j.jgr.2016.05.005.
  4. Li Z, Kim HJ, Park MS, Ji GE. Effects of fermented ginseng root and ginseng berry on obesity and lipid metabolism in mice fed a high-fat diet. J Ginseng Res 2018;42:312-9. https://doi.org/10.1016/j.jgr.2017.04.001.
  5. Chung IM, Lim JJ, Ahn MS, Jeong HN, An TJ, Kim SH. Comparative phenolic compound profiles and antioxidative activity of the fruit, leaves, and roots of Korean ginseng (Panax ginseng Meyer) according to cultivation years. J Ginseng Res 2016;40:68-75. https://doi.org/10.1016/j.jgr.2015.05.006.
  6. Wang CZ, Hou L, Wan JY, Yao H, Yuan J, Zeng J, et al. Ginseng berry polysaccharides on inflammation-associated colon cancer: inhibiting T-cell differentiation, promoting apoptosis, and enhancing the effects of 5-fluorouracil. J Ginseng Res 2020;44:282-90. https://doi.org/10.1016/j.jgr.2018.12.010.
  7. Parikh M, Raj P, Yu L, Stebbing JA, Prashar S, Petkau JC, et al. Ginseng berry extract rich in phenolic compounds attenuates oxidative stress but not cardiac remodeling post myocardial infarction. Int J Mol Sci 2019;20. https://doi.org/10.3390/ijms20040983.
  8. Kim SW, Gupta R, Lee SH, Min CW, Agrawal GK, Rakwal R, et al. An integrated biochemical, proteomics, and metabolomics approach for supporting medicinal value of panax ginseng fruits. Front Plant Sci 2016;7:994. https://doi.org/10.3389/fpls.2016.00994.
  9. Yoon D, Choi B-R, Kim Y-C, Oh SM, Kim H-G, Kim J-U, et al. Comparative analysis of panax ginseng berries from seven cultivars using UPLC-QTOF/MS and NMR-based metabolic profiling. Biomolecules 2019;9. https://doi.org/10.3390/biom9090424.
  10. Wang H, Xu F, Wang X, Kwon WS, Yang DC. Molecular discrimination of Panax ginseng cultivar K-1 using pathogenesis-related protein 5 gene. J Ginseng Res 2019;43:482-7. https://doi.org/10.1016/j.jgr.2018.07.001.
  11. Bae HM, Cho OS, Kim SJ, Im BO, Cho SH, Lee S, et al. Inhibitory effects of ginsenoside re isolated from ginseng berry on histamine and cytokine release in human mast cells and human alveolar epithelial cells. J Ginseng Res 2012;36:369-74. https://doi.org/10.5142/jgr.2012.36.4.369.
  12. Nam Y, Bae J, Jeong JH, Ko SK, Sohn UD. Protective effect of ultrasonication-processed ginseng berry extract on the D-galactosamine/lipopolysaccharide-induced liver injury model in rats. J Ginseng Res 2018;42:540-8. https://doi.org/10.1016/j.jgr.2017.07.007.
  13. Park EY, Kim HJ, Kim YK, Park SU, Choi JE, Cha JY, et al. Increase in insulin secretion induced by panax ginseng berry extracts contributes to the amelioration of hyperglycemia in streptozotocininduced diabetic mice. J Ginseng Res 2012;36:153-60. https://doi.org/10.5142/jgr.2012.36.2.153.
  14. Kim SJ, Kim JD, Ko SK. Changes in ginsenoside composition of ginseng berry extracts after a microwave and vinegar process. J Ginseng Res 2013;37:269-72. https://doi.org/10.5142/jgr.2013.37.269.
  15. Jung H, Bae J, Ko SK, Sohn UD. Ultrasonication processed Panax ginseng berry extract induces apoptosis through an intrinsic apoptosis pathway in HepG2 cells. Arch Pharm Res 2016;39:855-62. https://doi.org/10.1007/s12272-016-0760-6.
  16. Huq MA, Siraj FM, Kim YJ, Yang DC. Enzymatic transformation of ginseng leaf saponin by recombinant beta-glucosidase (bgp1) and its efficacy in an adipocyte cell line. Biotechnol Appl Biochem 2016;63:532-8. https://doi.org/10.1002/bab.1400.
  17. Quan L-H, Min J-W, Yang D-U, Kim Y-J, Yang D-C. Enzymatic biotransformation of ginsenoside Rb1 to 20(S)-Rg3 by recombinant b-glucosidase from Microbacterium esteraromaticum. Appl Microbiol Biotechnol 2012;94:377-84. https://doi.org/10.1007/s00253-011-3861-7.
  18. Quan LH, Min JW, Sathiyamoorthy S, Yang DU, Kim YJ, Yang DC. Biotransformation of ginsenosides Re and Rg1 into ginsenosides Rg2 and Rh1 by recombinant beta-glucosidase. Biotechnol Lett 2012;34:913-7. https://doi.org/10.1007/s10529-012-0849-z.
  19. Mack Correa MC, Mao G, Saad P, Flach CR, Mendelsohn R, Walters RM. Molecular interactions of plant oil components with stratum corneum lipids correlate with clinical measures of skin barrier function. Exp Dermatol 2014;23:39-44. https://doi.org/10.1111/exd.12296.
  20. van Smeden J, Bouwstra JA. Stratum corneum lipids: their role for the skin barrier function in healthy subjects and atopic dermatitis patients. Curr Probl Dermatol 2016;49:8-26. https://doi.org/10.1159/000441540.
  21. Ando H, Niki Y, Ito M, Akiyama K, Matsui MS, Yarosh DB, et al. Melanosomes are transferred from melanocytes to keratinocytes through the processes of packaging, release, uptake, and dispersion. J Invest Dermatol 2012;132:1222-9. https://doi.org/10.1038/jid.2011.413.
  22. Pereira AFC, Igarashi MH, Mercuri M, Pereira AF, Pinheiro A, da Silva MS, et al. Whitening effects of cosmetic formulation in the vascular component of skin pigmentation. J Cosmet Dermatol 2019. https://doi.org/10.1111/jocd.12979.
  23. Thong HY, Jee SH, Sun CC, Boissy RE. The patterns of melanosome distribution in keratinocytes of human skin as one determining factor of skin colour. Br J Dermatol 2003;149:498-505. https://doi.org/10.1046/j.1365-2133.2003.05473.x
  24. Nomura J, Busso N, Ives A, Tsujimoto S, Tamura M, So A, et al. Febuxostat, an inhibitor of xanthine oxidase, suppresses lipopolysaccharide-induced MCP-1 production via MAPK phosphatase-1-mediated inactivation of JNK. PLoS One 2013;8:e75527. https://doi.org/10.1371/journal.pone.0075527.
  25. Quinonez-Flores CM, Gonzalez-Chavez SA, Del Rio Najera D, Pacheco-Tena C. Oxidative stress relevance in the pathogenesis of the rheumatoid arthritis: a systematic review. Biomed Res Int 2016;2016:6097417. https://doi.org/10.1155/2016/6097417.
  26. Yu HS, Lee NK, Choi AJ, Choe JS, Bae CH, Paik HD. Anti-inflammatory potential of probiotic strain weissella cibaria JW15 isolated from kimchi through regulation of NF-kappaB and MAPKs pathways in LPS-induced RAW 264.7 cells. J Microbiol Biotechnol 2019;29:1022-32. https://doi.org/10.4014/jmb.1903.03014.
  27. Zhao Z, Dai XS, Wang ZY, Bao ZQ, Guan JZ. MicroRNA-26a reduces synovial inflammation and cartilage injury in osteoarthritis of knee joints through impairing the NF-kappaB signaling pathway. Biosci Rep 2019;39. https://doi.org/10.1042/BSR20182025.
  28. Lee JW, Ji SH, Lee YS, Choi DJ, Choi BR, Kim GS, et al. Mass spectrometry based profiling and imaging of various ginsenosides from panax ginseng roots at different ages. Int J Mol Sci 2017;18. https://doi.org/10.3390/ijms18061114.
  29. Jin Y, Kim YJ, Jeon JN, Wang C, Min JW, Noh HY, et al. Effect of white, red and black ginseng on physicochemical properties and ginsenosides. Plant Foods Hum Nutr 2015;70:141-5. https://doi.org/10.1007/s11130-015-0470-0.
  30. Kim M, Yi Y-S, Kim J, Han SY, Kim SH, Seo DB, et al. Effect of polysaccharides from a Korean ginseng berry on the immunosenescence of aged mice. J Ginseng Res 2018;42:447-54. https://doi.org/10.1016/j.jgr.2017.04.014.
  31. Park JS, Park EM, Kim DH, Jung K, Jung JS, Lee EJ, et al. Anti-inflammatory mechanism of ginseng saponins in activated microglia. J Neuroimmunol 2009;209:40-9. https://doi.org/10.1016/j.jneuroim.2009.01.020.
  32. Wang DD, Jin Y, Wang C, Kim YJ, Perez ZEJ, Baek NI, et al. Rare ginsenoside Ia synthesized from F1 by cloning and overexpression of the UDP-glycosyltransferase gene from Bacillus subtilis: synthesis, characterization, and in vitro melanogenesis inhibition activity in BL6B16 cells. J Ginseng Res 2018;42:42-9. https://doi.org/10.1016/j.jgr.2016.12.009.
  33. Wang PF, Li YP, Ding LQ, Cao SJ, Wang LN, Qiu F. Six new methyl apiofuranosides from the bark of phellodendron chinense schneid and their inhibitory effects on nitric oxide production. Molecules 2019;24. https://doi.org/10.3390/molecules24101851.
  34. Sreekanth TVM, Nagajyothi PC, Muthuraman P, Enkhtaivan G, Vattikuti SVP, Tettey CO, et al. Ultra-sonication-assisted silver nanoparticles using Panax ginseng root extract and their anti-cancer and antiviral activities. J Photochem Photobiol B 2018;188:6-11. https://doi.org/10.1016/j.jphotobiol.2018.08.013.
  35. Chen J, Li M, Qu D, Sun Y. Neuroprotective effects of red ginseng saponins in scopolamine-treated rats and activity screening based on pharmacokinetics. Molecules 2019;24. https://doi.org/10.3390/molecules24112136.
  36. Kim ST, Kim HB, Lee KH, Choi YR, Kim HJ, Shin IS, et al. Steam-dried ginseng berry fermented with Lactobacillus plantarum controls the increase of blood glucose and body weight in type 2 obese diabetic db/db mice. J Agric Food Chem 2012;60:5438-45. https://doi.org/10.1021/jf300460g.
  37. Li Z, Ahn HJ, Kim NY, Lee YN, Ji GE. Korean ginseng berry fermented by mycotoxin non-producing Aspergillus Niger and Aspergillus oryzae: ginsengoside analyses and anti-proliferative activities. Biol Pharm Bull 2016;39:1461-7. https://doi.org/10.1248/bpb.b16-00239.
  38. Solano F, Briganti S, Picardo M, Ghanem G. Hypopigmenting agents: an updated review on biological, chemical and clinical aspects. Pigment Cell Res 2006;19:550-71. https://doi.org/10.1111/j.1600-0749.2006.00334.x.
  39. Hearing VJ. Determination of melanin synthetic pathways. J Invest Dermatol 2011;131:E8-11. https://doi.org/10.1038/skinbio.2011.4.
  40. Zhai XT, Zhang ZY, Jiang CH, Chen JQ, Ye JQ, Jia XB, et al. Nauclea officinalis inhibits inflammation in LPS-mediated RAW 264.7 macrophages by suppressing the NF-kappaB signaling pathway. J Ethnopharmacol 2016;183:159-65. https://doi.org/10.1016/j.jep.2016.01.018.
  41. Wang R, Dong Z, Lan X, Liao Z, Chen M. Sweroside alleviated LPS-induced inflammation via SIRT1 mediating NF-kappaB and FOXO1 signaling pathways in RAW264.7 cells. Molecules 2019;24. https://doi.org/10.3390/molecules24050872.
  42. Hsu HY, Wen MH. Lipopolysaccharide-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J Biol Chem 2002;277:22131-9. https://doi.org/10.1074/jbc.M111883200.
  43. Kraaij MD, van der Kooij SW, Reinders ME, Koekkoek K, Rabelink TJ, van Kooten C, et al. Dexamethasone increases ROS production and T cell suppressive capacity by anti-inflammatory macrophages. Mol Immunol 2011;49:549-57. https://doi.org/10.1016/j.molimm.2011.10.002.
  44. Liu W, Zhao Z, Na Y, Meng C, Wang J, Bai R. Dexamethasone-induced production of reactive oxygen species promotes apoptosis via endoplasmic reticulum stress and autophagy in MC3T3-E1 cells. Int J Mol Med 2018;41:2028-36. https://doi.org/10.3892/ijmm.2018.3412.
  45. Deng S, Dai G, Chen S, Nie Z, Zhou J, Fang H, et al. Dexamethasone induces osteoblast apoptosis through ROS-PI3K/AKT/GSK3beta signaling pathway. Biomed Pharmacother 2019;110:602-8. https://doi.org/10.1016/j.biopha.2018.11.103.
  46. Yao YD, Shen XY, Machado J, Luo JF, Dai Y, Lio CK, et al. Nardochinoid B inhibited the activation of RAW264.7 macrophages stimulated by lipopolysaccharide through activating the Nrf2/HO-1 pathway. Molecules 2019;24. https://doi.org/10.3390/molecules24132482.