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References

  1. Bae HM, Kim SS, Cho CW, Yang DC, Ko SK, Kim KT. 2012. Antioxidant activities of ginseng seeds treated by autoclaving. J. Ginseng Res. 36: 411-417.
    Pubmed PMC CrossRef
  2. Bogdan C. 2015. Nitric oxide synthase in innate and adaptive immunity: an update. Trends Immunol. 36: 161-178.
    Pubmed CrossRef
  3. Chen H, Dorrigan A, Saad S, Hare DJ, Cortie MB, Valenzuela SM. 2013. In vivo study of spherical gold nanoparticles:inflammatory effects and distribution in mice. PLoS One 8: e58208.
    Pubmed PMC CrossRef
  4. Cheon J, Lee J, Kim J. 2012. Inkjet printing using copper nanoparticles synthesized by electrolysis. Thin Solid Films 520: 2639-2643.
    CrossRef
  5. Cho IH. 2012. Effects of Panax ginseng in neurodegenerative diseases. J. Ginseng Res. 36: 342-353.
    Pubmed PMC CrossRef
  6. Christensen LP. 2009. Ginsenosides chemistry, biosynthesis, analysis, and potential health effects. Adv. Food Nutr. Res. 55: 1-99.
    CrossRef
  7. Chueh PJ, Liang RY, Lee YH, Zeng ZM, Chuang SM. 2014. Differential cytotoxic effects of gold nanoparticles in different mammalian cell lines. J. Hazard. Mat. 264: 303-312.
    Pubmed CrossRef
  8. Da Silva LC, Oliva MA, Azevedo AA, De Araújo JM. 2006. Responses of restinga plant species to pollution from an iron pelletization factory. Water Air Soil Pollut. 175: 241-256.
    CrossRef
  9. de La Rosa G, Lopez-Moreno ML, de Haro-Del Rio D, Botez CE, Peralta-Videa JR, Gardea-Torresdey JL. 2013. Effects of ZnO nanoparticles in alfalfa, tomato, and cucumber at the germination stage: root development and X-ray absorption spectroscopy studies. Pure Appl. Chem. 85: 2161-2174.
    CrossRef
  10. Gao F, Hong F, Liu C, Zheng L, Su M, Wu X, et al. 2006. Mechanism of nano-anatase TiO2 on promoting photosynthetic carbon reaction of spinach: inducing complex of RubiscoRubisco activase. Biol. Trace Elem. Res. 111: 239-253.
    CrossRef
  11. Hong FH, Zhou J, Liu C, Yang F, Wu C, Zheng L, Yang P. 2005. Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach. Biol. Trace Elem. Res. 105: 269-279.
    CrossRef
  12. Jo MR, Bae SH, Go MR, K im HJ, Hwang YG, Choi SJ. 2015. Toxicity and biokinetics of colloidal gold nanoparticles. Nanomaterials 5: 835-850.
    CrossRef
  13. Jung HJ, Choi H, Lim HW, Shin D, Kim H, Kwon B, et al. 2012. Enhancement of anti-inflammatory and antinociceptive actions of red ginseng extract by fermentation. J. Pharm. Pharmacol. 64: 756-762.
    Pubmed CrossRef
  14. Kang S, Min H. 2012. Ginseng, the ‘immunity boost': the effects of Panax ginseng on immune system. J. Ginseng Res. 36: 354-368.
    Pubmed PMC CrossRef
  15. Kim K, Duramad O, Qin XF, Su B. 2007. MEKK3 is essential for lipopolysaccharide-induced interleukin-6 and granulocytemacrophage colony-stimulating factor production in macrophages. Immunology 120: 242-250.
    Pubmed PMC CrossRef
  16. K ole C, K ole P, R andunu K M, C houdhary P , Podila R , K e PC, et al. 2013. Nanobiotechnology can boost crop production and quality: first evidence from increased plant biomass, fruit yield and phytomedicine content in bitter melon (Momordica charantia). BMC Biotechnol. 13: 37.
  17. Lee SM, Bae BS, Park HW, Ahn NG, Cho BG, Cho YL, Kwak YS. 2015. Characterization of Korean red ginseng (Panax ginseng Meyer): history, preparation method, and chemical composition. J. Ginseng Res. 39: 384-391.
    Pubmed PMC CrossRef
  18. Mosser DM, Edwards JP. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8: 958-969.
    Pubmed PMC CrossRef
  19. Nair R, Varghese SH, Nair BG, Maekawa T, Yoshida Y, K umar D S. 2 010. N anoparticulate m aterial delivery t o plants. Plant Sci. 179: 154-163.
    CrossRef
  20. Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, et al. 2008. Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17: 372-386.
    Pubmed CrossRef
  21. Shin YM, Jung HJ, Choi WY, Lim CJ. 2013. Antioxidative, anti-inflammatory, and matrix metalloproteinase inhibitory activities of 20(S)-ginsenoside Rg3 in cultured mammalian cell lines. Mol. Biol. Rep. 40: 269-279.
    Pubmed CrossRef
  22. Wong AS, Che CM, Leung KW. 2015. Recent advances in ginseng as cancer therapeutics: a functional and mechanistic overview. Nat. Prod. Rep. 32: 256-272.
    Pubmed CrossRef
  23. Wu H, Hoiby N, Yang L, Givskov M, Song Z. 2014. Effects of radix ginseng on microbial infections: a narrative review. J. Tradit. Chin. Med. 34: 227-233.
    CrossRef
  24. Yoon SJ, Park JY, Choi S, Lee JB, Jung H, Kim TD, et al. 2015. Ginsenoside Rg3 regulates S-nitrosylation of the NLRP3 inflammasome via suppression of iNOS. Biochem. Biophys. Res. Commun. 463: 1184-1189.
    Pubmed CrossRef
  25. Yoon SR, L ee GD, Park J H, L ee I S, K won JH. 2010. Ginsenoside composition and antiproliferative activities of explosively puffed ginseng (Panax ginseng C.A. Meyer). J. Food Sci. 75: C378-C382.
    Pubmed CrossRef
  26. Zhang XD, Wu HY, Wu D, Wang YY, Chang JH, Zhai ZB, et al. 2010. Toxicologic effects of gold nanoparticles in vivo by different administration routes. Int. J. Nanomed. 5: 771-781.
    Pubmed PMC CrossRef
  27. Zheng L, Hong FS, Lu SP, Liu C. 2005. Effect of nano-TiO2 on strength of naturally and growth aged seeds of spinach. Biol. Trace Elem. Res. 104: 83-91.
    CrossRef
  28. Zheng SD, Wu HJ, Wu DL. 2012. Roles and mechanisms of ginseng in protecting heart. Chin. J. Integr. Med. 18: 548-555.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(10): 1668-1674

Published online October 28, 2016 https://doi.org/10.4014/jmb.1604.04034

Copyright © The Korean Society for Microbiology and Biotechnology.

Use of Gold Nanoparticle Fertilizer Enhances the Ginsenoside Contents and Anti-Inflammatory Effects of Red Ginseng

Hee Kang 1, Yun-Gu Hwang 2, Taek-Guen Lee 3, Cheng-Ri Jin 3, Chi Heung Cho 3, Hee-Yeong Jeong 1 and Dae-Ok Kim 3*

1Graduate School of East-West Medical Science, Kyung Hee University, Yongin 17104, Republic of Korea, 2SMNANOBIO Co., Ltd., Daejeon 34028, Republic of Korea, 3Department of Food Science and Biotechnology, Kyung Hee University, Yongin 17104, Republic of Korea

Received: April 12, 2016; Accepted: July 7, 2016

Abstract

Red ginseng, a steamed and sun-dried ginseng, is a popular health-promoting food in Korea
and other Asian countries. We introduced nanofertilizer technology using gold nanoparticles
in an effort to develop red ginseng with an elevated level of ginsenosides, the main active
compounds of ginseng. Shoots of 6-year-old ginseng plants were fertilized three times with
colloidal gold nanoparticle sprays. Red ginseng extract was prepared from the main roots. The
concentrations of gold and ginsenosides were measured following gold nanoparticle
treatment. To evaluate the anti-inflammatory effects, mouse peritoneal macrophages of male
BALB/c mouse were stimulated with lipopolysaccharide plus interferon-γ in the presence of
extracts from red ginseng with or without gold nanoparticle treatment. The content of
ginsenosides, such as Rg1, Re, Rf, and Rb1, increased in ginseng treated with gold nanofertilizer
whereas the steaming process increased only the levels of Rd and Rg3. The levels of nitric
oxide, inducible nitric oxide synthase, and interleukin-6, but not tumor necrosis factor-α, were
more suppressed in macrophages treated with extract from gold nanoparticle-treated red
ginseng. Our results show that the use of a colloidal gold nanoparticle fertilizer improved the
synthesis of ginsenosides in ginseng and enhanced the anti-inflammatory effects of red
ginseng. Further research is required to elucidate the causal factors for the gold-induced
change in ginsenoside synthesis and to determine the in vivo effect of gold nanoparticletreated
ginseng.

Keywords: gold nanoparticles, inflammation, macrophages, red ginseng, ginsenoside

References

  1. Bae HM, Kim SS, Cho CW, Yang DC, Ko SK, Kim KT. 2012. Antioxidant activities of ginseng seeds treated by autoclaving. J. Ginseng Res. 36: 411-417.
    Pubmed KoreaMed CrossRef
  2. Bogdan C. 2015. Nitric oxide synthase in innate and adaptive immunity: an update. Trends Immunol. 36: 161-178.
    Pubmed CrossRef
  3. Chen H, Dorrigan A, Saad S, Hare DJ, Cortie MB, Valenzuela SM. 2013. In vivo study of spherical gold nanoparticles:inflammatory effects and distribution in mice. PLoS One 8: e58208.
    Pubmed KoreaMed CrossRef
  4. Cheon J, Lee J, Kim J. 2012. Inkjet printing using copper nanoparticles synthesized by electrolysis. Thin Solid Films 520: 2639-2643.
    CrossRef
  5. Cho IH. 2012. Effects of Panax ginseng in neurodegenerative diseases. J. Ginseng Res. 36: 342-353.
    Pubmed KoreaMed CrossRef
  6. Christensen LP. 2009. Ginsenosides chemistry, biosynthesis, analysis, and potential health effects. Adv. Food Nutr. Res. 55: 1-99.
    CrossRef
  7. Chueh PJ, Liang RY, Lee YH, Zeng ZM, Chuang SM. 2014. Differential cytotoxic effects of gold nanoparticles in different mammalian cell lines. J. Hazard. Mat. 264: 303-312.
    Pubmed CrossRef
  8. Da Silva LC, Oliva MA, Azevedo AA, De Araújo JM. 2006. Responses of restinga plant species to pollution from an iron pelletization factory. Water Air Soil Pollut. 175: 241-256.
    CrossRef
  9. de La Rosa G, Lopez-Moreno ML, de Haro-Del Rio D, Botez CE, Peralta-Videa JR, Gardea-Torresdey JL. 2013. Effects of ZnO nanoparticles in alfalfa, tomato, and cucumber at the germination stage: root development and X-ray absorption spectroscopy studies. Pure Appl. Chem. 85: 2161-2174.
    CrossRef
  10. Gao F, Hong F, Liu C, Zheng L, Su M, Wu X, et al. 2006. Mechanism of nano-anatase TiO2 on promoting photosynthetic carbon reaction of spinach: inducing complex of RubiscoRubisco activase. Biol. Trace Elem. Res. 111: 239-253.
    CrossRef
  11. Hong FH, Zhou J, Liu C, Yang F, Wu C, Zheng L, Yang P. 2005. Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach. Biol. Trace Elem. Res. 105: 269-279.
    CrossRef
  12. Jo MR, Bae SH, Go MR, K im HJ, Hwang YG, Choi SJ. 2015. Toxicity and biokinetics of colloidal gold nanoparticles. Nanomaterials 5: 835-850.
    CrossRef
  13. Jung HJ, Choi H, Lim HW, Shin D, Kim H, Kwon B, et al. 2012. Enhancement of anti-inflammatory and antinociceptive actions of red ginseng extract by fermentation. J. Pharm. Pharmacol. 64: 756-762.
    Pubmed CrossRef
  14. Kang S, Min H. 2012. Ginseng, the ‘immunity boost': the effects of Panax ginseng on immune system. J. Ginseng Res. 36: 354-368.
    Pubmed KoreaMed CrossRef
  15. Kim K, Duramad O, Qin XF, Su B. 2007. MEKK3 is essential for lipopolysaccharide-induced interleukin-6 and granulocytemacrophage colony-stimulating factor production in macrophages. Immunology 120: 242-250.
    Pubmed KoreaMed CrossRef
  16. K ole C, K ole P, R andunu K M, C houdhary P , Podila R , K e PC, et al. 2013. Nanobiotechnology can boost crop production and quality: first evidence from increased plant biomass, fruit yield and phytomedicine content in bitter melon (Momordica charantia). BMC Biotechnol. 13: 37.
  17. Lee SM, Bae BS, Park HW, Ahn NG, Cho BG, Cho YL, Kwak YS. 2015. Characterization of Korean red ginseng (Panax ginseng Meyer): history, preparation method, and chemical composition. J. Ginseng Res. 39: 384-391.
    Pubmed KoreaMed CrossRef
  18. Mosser DM, Edwards JP. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8: 958-969.
    Pubmed KoreaMed CrossRef
  19. Nair R, Varghese SH, Nair BG, Maekawa T, Yoshida Y, K umar D S. 2 010. N anoparticulate m aterial delivery t o plants. Plant Sci. 179: 154-163.
    CrossRef
  20. Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, et al. 2008. Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17: 372-386.
    Pubmed CrossRef
  21. Shin YM, Jung HJ, Choi WY, Lim CJ. 2013. Antioxidative, anti-inflammatory, and matrix metalloproteinase inhibitory activities of 20(S)-ginsenoside Rg3 in cultured mammalian cell lines. Mol. Biol. Rep. 40: 269-279.
    Pubmed CrossRef
  22. Wong AS, Che CM, Leung KW. 2015. Recent advances in ginseng as cancer therapeutics: a functional and mechanistic overview. Nat. Prod. Rep. 32: 256-272.
    Pubmed CrossRef
  23. Wu H, Hoiby N, Yang L, Givskov M, Song Z. 2014. Effects of radix ginseng on microbial infections: a narrative review. J. Tradit. Chin. Med. 34: 227-233.
    CrossRef
  24. Yoon SJ, Park JY, Choi S, Lee JB, Jung H, Kim TD, et al. 2015. Ginsenoside Rg3 regulates S-nitrosylation of the NLRP3 inflammasome via suppression of iNOS. Biochem. Biophys. Res. Commun. 463: 1184-1189.
    Pubmed CrossRef
  25. Yoon SR, L ee GD, Park J H, L ee I S, K won JH. 2010. Ginsenoside composition and antiproliferative activities of explosively puffed ginseng (Panax ginseng C.A. Meyer). J. Food Sci. 75: C378-C382.
    Pubmed CrossRef
  26. Zhang XD, Wu HY, Wu D, Wang YY, Chang JH, Zhai ZB, et al. 2010. Toxicologic effects of gold nanoparticles in vivo by different administration routes. Int. J. Nanomed. 5: 771-781.
    Pubmed KoreaMed CrossRef
  27. Zheng L, Hong FS, Lu SP, Liu C. 2005. Effect of nano-TiO2 on strength of naturally and growth aged seeds of spinach. Biol. Trace Elem. Res. 104: 83-91.
    CrossRef
  28. Zheng SD, Wu HJ, Wu DL. 2012. Roles and mechanisms of ginseng in protecting heart. Chin. J. Integr. Med. 18: 548-555.
    Pubmed CrossRef