Journal of Applied Biological Chemistry

  • Volume 66
  • /
  • Pages.492-502
  • /
  • 2023
  • /
  • 1976-0442(pISSN)
  • /
  • 2234-7941(eISSN)
The Korean Society for Applied Biological Chemistry (한국응용생명화학회)
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Anti-oxidant and immune enhancement effects of Artemisia argyi H. fermented with lactic acid bacteria

  • Ji Yun Lee (Department of Food Science and Nutrition, Pusan National University) ;
  • Ji Hyun Kim (Department of Food Science and Nutrition, Gyeongsang National University) ;
  • Ji Myung Choi (Department of Food and Nutrition, Kyungsung University) ;
  • Hyemee Kim (Department of Food Science and Nutrition, Pusan National University) ;
  • Weon Taek Seo (Department of Food Science and Technology, Gyeongsang National University) ;
  • Eun Ju Cho (Department of Food Science and Nutrition, Pusan National University) ;
  • Hyun Young Kim (Department of Food Science and Nutrition, Gyeongsang National University)
  • Received : 2023.11.22
  • Accepted : 2023.12.08
  • Published : 2023.12.31
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Abstract

This study investigated the antioxidant and immune enhancement activities of Artemisia argyi H. fermented by Lactobacillus plantarum. The fermented A. argyi H. ethanol extract increased scavenging activities of 1,1-diphenyl-2-picrylhydrazyl (DPPH), 2,2'-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS+), hydroxyl (·OH), and superoxide (O2-) radicals. Particularly, the ethanol extract of fermented A. argyi H. exhibited higher ·OH and O2- radical scavenging activities, compared with DPPH and ABTS+ radical scavenging activities. To evaluate the immune enhancement effects of the fermented A. argyi H., mice were fed a normal diet supplemented the fermented A. argyi H. at concentrations of 1%, 2%, and 5%, respectively. The supplementation of fermented A. argyi H. dose-dependently increased splenocyte proliferation. In addition, mice fed with 5% fermented A. argyi H. showed enhanced proliferation of T-cells and B-cells, along with increased levels of interferon-γ, interleukin-10, and tumor necrosis factor-α, compared to the normal group. Furthermore, mice fed with fermented A. argyi H. exhibited an increase in prominent probiotics such as Akkermansia muciniphila and Lactobacillus in gut microbiota, compared to the normal group. This study suggests that fermented A. argyi H. with Lactobacillus plantarum could be used as a dietary antioxidant and immune enhancement agent.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea(NRF) grant funded by the Korea government(MSIT) (No. 2021R1F1A1061542).

References

  1. McNeela EA, Mills KH (2001) Manipulating the immune system: humoral versus cell-mediated immunity. Adv Drug Deliv 51: 43-54. doi: 10.1016/s0169-409x(01)00169-7 
  2. Leung HY, Ko KM (2023) Differential effects of yin- and yang-chinese tonifying herbs on innate and adaptive immunity. Chin Med 14: 68-78. doi: 10.4236/cm.2023.142004 
  3. Lanier LL (2013) Shades of grey--the blurring view of innate and adaptive immunity. Nat Rev Immunol 13: 73-74. doi: 10.1038/nri3389 
  4. Turvey SE, Broide DH (2010) Innate immunity. J Allergy Clin Immunol 125: 24-32. doi: 10.1016/j.jaci.2009.07.016 
  5. Bonilla FA, Oettgen HC (2010) Adaptive immunity. J Allergy Clin Immunol 125: 33-40. doi: 10.1016/j.jaci.2009.09.017 
  6. Lee SH, Shin JH, Lee HJ, Tak HM, Kang MJ, Sung NJ (2013) Antioxidant and anti-inflammatory activities of functional plant materials. J Acric Life Sci 23: 869-878. doi:10.5352/JLS.2013.23.7.869 
  7. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39: 44-84. doi: 10.1016/j.biocel.2006.07.001 
  8. Finley JW, Kong AN, Hintze KJ, Jeffery EH, Ji LL, Lei XG (2011) Antioxidants in foods: state of the science important to the food industry. J Agric Food Chem 59: 6837-6846. doi: 10.1021/jf2013875 
  9. Belikov AV, Burkhart S, Luca S (2015) T cells and reactive oxygen species. J Biomed Sci 22: 85. doi: 10.1186/s12929-015-0194-3 
  10. Yang Y, Bazhin AV, Werner J, Karakhanova S (2013) Reactive oxygen species in the immune system. Int Rev Immunol 32: 249-270. doi: 10.3109/08830185.2012.755176 
  11. Victor VM, Rocha M, De la Fuente M (2004) Immune cells: free radicals and antioxidants in sepsis. Int Immunopharmacol 4: 327-347. doi: 10.1016/j.intimp.2004.01.020 
  12. Zhao YS, Eweys AS, Zhang JY, Zhu Y, Bai J, Darwesh OM, Zhang HB, Xiao X (2021) Fermentation affects the antioxidant activity of plant-based food material through the release and production of bioactive components. Antioxidants (Basel) 10: 2004. doi: 10.3390/antiox10122004 
  13. Abedi E, Hashemi SMB (2020) Lactic acid production - producing microorganisms and substrates sources-state of art. Heliyon 6: e04974. doi: 10.1016/j.heliyon.2020.e04974 
  14. Park KY, Jeong JK, Lee YE, Daily JW 3rd (2014) Health benefits of kimchi (Korean fermented vegetables) as a probiotic food. J Med Food 17: 6-20. doi: 10.1089/jmf.2013.3083 
  15. De Montijo-Prieto S, Razola-Diaz MDC, Barbieri F, Tabanelli G, Gardini F, Jimenez-Valera M, Ruiz-Bravo A, Verardo V, Gomez-Caravaca AM (2023) Impact of lactic acid bacteria fermentation on phenolic compounds and antioxidant activity of avocado leaf extracts. Antioxidants (Basel) 12: 298. doi: 10.3390/antiox12020298 
  16. Kang JR, Kang MJ, Choi MH, Byun HU, Shin JH (2017) Physicochemical characteristics of ethanol extract from Artemisia argyi H. using different preparation methods. J Life Sci 27: 23-31. doi: 10.5352/JLS.2017.27.1.23 
  17. Hwang CR, Seo WT, Bae WY, Kang MJ, Shin JH (2014) Physicochemical characteristics and biological activities of Artemisia argyi H. J Life Sci 24: 377-385. doi: 10.5352/JLS.2014.24.4.377 
  18. Kim MJ, Han JM, Jin YY, Baek NI, Bang MH, Chung HG, Choi MS, Lee KT, Sok DE, Jeong TS (2008) In vitro antioxidant and anti-inflammatory activities of Jaceosidin from Artemisia princeps Pampanini cv. Sajabal. Arch Pharm Res 31: 429-437. doi: 10.1007/s12272-001-1175-8 
  19. Yin Y, Sun Y, Gu L, Zheng W, Gong F, Wu X, Shen Y, Xu Q (2011) Jaceosidin inhibits contact hypersensitivity in mice via down-regulating IFN-γ/STAT1/T-bet signaling in T cells. Eur J Pharmacol 651: 205-211. doi: 10.1016/j.ejphar.2010.10.068 
  20. Ha HJ, Lee DS, Seung TW, Park CH, Park SK, Jin DE, Kim NK, Shin HY, Heo HJ (2015) Anti-amnesic and neuroprotective effects of Artemisia argyi H. (Seomae mugwort) extracts. Korean J Food Sci Technol 47: 380-387. doi:10.9721/kjfst.2015.47.3.380 
  21. Kang JY, Lee DS, Park SK, Ha JS, Kim JM, Ha GJ, Seo WT, Heo HJ (2017) Cognitive function of Artemisia argyi H. fermented by Monascus purpureus under TMT-induced learning and memory deficits in ICR mice. Evid Based Complement Alternat Med 2017: 5809370. doi: 10.1155/2017/5809370 
  22. Kim JH, Kim NK, Lee AY, Seo WT, Kim HY (2022) Antioxidant activity study of Artemisia argyi H. extract fermented with lactic acid bacteria. J Korean Med Obes Res 22: 115-124. doi: 10.15429/jkomor.2022.22.2.115 
  23. Hatano T, Edamatsu R, Hiramatsu M, Mori A, Fujita Y, Yasuhara T, Yoshida T, Okuda T (1989) Effects of the interaction of tannins with coexisting substances: Effects of tannins and VI related poly phenols on superoxide anion radical, and on 1,1-diphenyl-2-picrylhydrazyl radical. Chem Pharm Bull 37: 2016-2021. doi: 10.1248/cpb.37.2016 
  24. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26: 1231-1237. doi: 10.1016/s0891-5849(98)00315-3 
  25. SK Chung (1997) Hydroxyl radical- scavenging effects of spices and scavengers from brown mustard (Brassica nigra). Biosci Biotechnol Biochem 61: 118-123  https://doi.org/10.1271/bbb.61.118
  26. Kaur C, Kapoor HC (2002) Anti-oxidant activity and total phenolic content of some Asian vegetables. Int J Food Sci Techol 37: 153-161. doi: 10.1046/j.1365-2621.2002.00552.x 
  27. Choi MJ, Lee JH, Lee YJ, Pail HD, Park EJ (2022) Egg yolk protein water extracts modulate the immune response in BALB/c mice with immune dysfunction caused by forced swimming. Foods 11: 121. doi: 10.3390/foods11010121. 
  28. Noratto GD, Garcia-Mazcorro JF, Markel M, Martino HS, Minamoto Y, Steiner JM, Byrne D, Suchodolski JS, Mertens-Talcott SU (2014) Carbohydrate-free peach (Prunus persica) and plum (Prunus domestica) juice affects fecal microbial ecology in an obese animal model. Plos One 9(7): e101723. doi: 10.1371/journal.pone.0101723 
  29. Nathan T, Myra S (1970) Studies on some physicochemical properties of a thymus humoral factor conferring immunocompetence on lymphoid cells. J Exp Med 132(5): 885-897. doi: 10.1084/jem.132.5.885 
  30. Schaich KM, Tian X, Xie J (2015) Hurdles and pitfalls in measuring antioxidant efficacy: A critical evaluation of ABTS, DPPH, and ORAC assays. J Funct Foods 14: 111-125. doi: 10.1016/j.jff.2015.01.043 
  31. Molyneux P (2004) The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin J Sci Technol 26(2): 211-219 
  32. Jasprica I, Bojic M, Mornar A, Besic E, Bucan K, Medic-Saric M (2007) Evaluation of antioxidative activity of Croatian propolis samples using DPPH** and ABTS*+ stable free radical assays. Molecules 12(5): 1006-1021. doi: 10.3390/12051006 
  33. Hui Z, Wenfeng X, Xiangxiang Z, Linlin T, Fen Z, Hua W, Xueying T (2022) Effects of Lactobacillus plantarum Wlpl01 fermentation on antioxidant activities, bioactive compounds, and flavor profile of Artemisia Argyi. Food Biosci 49: 101908. doi: 10.1016/j.fbio.2022.101908 
  34. Shin JY, Kang MJ, Kang JR, Choi JS, Seo WT, Shin JH (2020) Quality characteristics of fermented vinegar containing different concentration of an ethanol extract from 'Seomaeyaksuk' (Artemisia argyi H.). Korean J Food Preserv 27(2): 212-223. doi: 10.11002/kjfp.2020.27.2.212 
  35. Lipinski B (2011) Hydroxyl radical and its scavengers in health and disease. Oxid Med Cell Longev 2011: 809696. doi: 10.1155/2011/809696 
  36. Panda SK (2012) Assay guided comparison for enzymatic and nonenzymatic antioxidant activities with special reference to medicinal plants. Antioxidant Enzyme 15: 381-400. doi: 10.5772/50782 
  37. Mebius Re, Kraal G (2005) Structure and function of the spleen. Nat Rev Immunol 5: 606-616. doi: 10.1038/nri1669 
  38. Fan Y, Hu Y, Wang D, Guo Z, Zhao X, Guo L, Zhao B, Zhang J, Wang Y, Nguyen T (2010) Epimedium polysaccharide and propolis flavone can synergistically stimulate lymphocyte proliferation in vitro and enhance the immune responses to ND vaccine in chickens. Int J Biol Macromol 47(2): 87-92. doi: 10.1016/j.ijbiomac.2010.05.017 
  39. Caspi RR, Shahrabani R, Kehatidan T, Avtalion RR (1984) Heterogeneity of mitogen-responsive lymphocytes in carp (Cyprinus carpio). Dev Comp Immunol 8(1): 61-70. doi: 10.1016/0145-305x(84)90010-7 
  40. Li Q, Zhou Y, Dong K, Guo X (2010) Potential therapeutic efficacy of a bactericidal-immunomodulatory fusion peptide against methicillin-resistant Staphylococcus aureus skin infection. Appl Microbiol Biotechnol 86(1): 305-309. doi: 10.1007/s00253-009-2313-0 
  41. Kidd P (2003) Th1/Th2 balance: The hypothesis, its limitations, and implications for health and disease. Altern Med Rev 8(3): 223-246 
  42. Rinniella E, Raoul P, Cintoni M, Franceschi F, Miggiano GAD, Gasbarrini A, Mele MC (2019) What is the healthy gut microbiota composition? a changing ecosystem across age, environment, diet, and diseases. Microorganisms 7(1): 14. doi: 10.3390/microorganisms7010014 
  43. Seong CN, Kang JW, Lee JH, Seo SY, Woo JJ, Park C, Bae KS, Kim MS (2018) Taxonomic hierarchy of the phylum Firmicutes and novel Firmicutes species originated from various environments in Korea. J Microbiol 56(1): 1-10. doi: 10.1007/s12275-018-7318-x 
  44. Gibiino G, Lopetuso LR, Scaldaferri F, Rizzatti G, Binda C, Gasbarrini A (2018) Exploring Bacteroidetes: Metabolic key points and immunological tricks of our gut commensals. Dig Liver Dis 50(7): 635-639. doi: 10.1016/j.dld.2018.03.016 
  45. Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, Zhu D, Koya JB, Wei L, Li J, Chen ZS (2022) Microbiota in health and diseases. Signal Transduct Target Ther 7(1): 135. doi: 10.1038/s41392-022-00974-4 
  46. Derrien M, Vaughan EE, Plugge CM, de VOS WM (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54: 1469-1476. doi: 10.1099/ijs.0.02873-0 
  47. Derrien M, Collado MC, Ben-Amor K, Salminen S, De Vos WM (2008) The mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol 74(5): 1646-1648. doi: 10.1128/AEM.01226-07 
  48. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-y M, Glickman JN, Garrett WS (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341(6145): 567-573. doi: 10.1126/science.1241165 
  49. Madsen K (2006) Probiotics and the immune response. J Clin Gastroenterol 40(3): 232-234. doi: 10.1097/00004836-200603000-00014 
  50. Galdeano CM, Perdigon G (2006) The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol 13(2): 219-226. doi: 10.1128/CVI.13.2.219-226.2006 
  51. Kim SM, Lee SJ, Venkatarame Gowda Saralamma V, Ha SE, Vetrivel P, Desta KT, Choi JY, Lee WS, Shin SC, Kim GS (2019) Polyphenol mixture of a native Korean variety of Artemisia argyi H. (Seomae mugwort) and its anti-inflammatory effects. Int J Mol Med 44(5): 1741-1752. doi: 10.3892/ijmm.2019.4334 
  52. Del Carmen Juarez-Vazquez M, Josabad Alonso-Castro A, Garcia-Carranca A (2013) Kaempferitrin induces immunostimulatory effects in vitro. J Ethnopharmacol 148(1):337-40. doi: 10.1016/j.jep.2013.03.072 
  53. Oliveira TT, Campos KM, Cerqueira-Lima AT, Cana Brasil Carneiro T, da Silva Velozo E, Ribeiro Melo IC, Figueiredo EA, de Jesus Oliveira E, de Vasconcelos DF, Pontes-de-Carvalho LC, Alcantara-Neves NM, Figueiredo CA (2015) Potential therapeutic effect of Allium cepa L. and quercetin in a murine model of Blomia tropicalis induced asthma. Daru 23(1): 18. doi: 10.1186/s40199-015-0098-5 
  54. Amevor FK, Cui Z, Du X, Ning Z, Deng X, Xu D, Shu G, Wu Y, Cao X, Shuo W, Tian Y, Li D, Wang Y, Zhang Y, Du X, Zhu Q, Han X, Zhao X (2022) Supplementation of dietary quercetin and vitamin E promotes the intestinal structure and immune barrier integrity in aged breeder hens. Front Immunol 13: 860889. doi: 10.3389/fimmu.2022.860889 
  55. Cardenas H, Arango D, Nicholas C, Duarte S, Nuovo GJ, He W, Voss OH, Gonzalez-Mejia ME, Guttridge DC, Grotewold E, Doseff AI (2016) Dietary apigenin exerts immune-regulatory activity in vivo by reducing NF-κB activity, halting leukocyte infiltration and restoring normal metabolic function. Int J Mol Sci 17(3): 323. doi: 10.3390/ijms17030323 
  56. Wang M, Firrman J, Zhang L, Arango-Argoty G, Tomasula P, Liu L, Xiao W, Yam K (2017) Apigenin impacts the growth of the gut microbiota and alters the gene expression of enterococcus. Molecules 22(8): 1292. doi: 10.3390/molecules22081292