Journal of Microbiology and Biotechnology

  • 제31권1호
  • /
  • Pages.51-62
  • /
  • 2021
  • /
  • 1017-7825(pISSN)
  • /
  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

Actinidia arguta Sprout as a Natural Antioxidant: Ameliorating Effect on Lipopolysaccharide-Induced Cognitive Impairment

  • Kang, Jeong Eun (Division of Applied Life Science, Institute of Agriculture and Life Science (BK21), Gyeongsang National University) ;
  • Park, Seon Kyeong (Division of Applied Life Science, Institute of Agriculture and Life Science (BK21), Gyeongsang National University) ;
  • Kang, Jin Yong (Division of Applied Life Science, Institute of Agriculture and Life Science (BK21), Gyeongsang National University) ;
  • Kim, Jong Min (Division of Applied Life Science, Institute of Agriculture and Life Science (BK21), Gyeongsang National University) ;
  • Kwon, Bong Seok (Division of Applied Life Science, Institute of Agriculture and Life Science (BK21), Gyeongsang National University) ;
  • Park, Sang Hyun (Division of Applied Life Science, Institute of Agriculture and Life Science (BK21), Gyeongsang National University) ;
  • Lee, Chang Jun (Division of Applied Life Science, Institute of Agriculture and Life Science (BK21), Gyeongsang National University) ;
  • Yoo, Seul Ki (Division of Applied Life Science, Institute of Agriculture and Life Science (BK21), Gyeongsang National University) ;
  • Heo, Ho Jin (Division of Applied Life Science, Institute of Agriculture and Life Science (BK21), Gyeongsang National University)
  • 투고 : 2020.09.08
  • 심사 : 2020.10.07
  • 발행 : 2021.01.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Here, we investigated the prebiotic and antioxidant effects of Actinidia arguta sprout water extract (AASWE) on lipopolysaccharide (LPS)-induced cognitive deficit mice. AASWE increased viable cell count, titratable acidity, and acetic acid production in Lactobacillus reuteri strain and showed a cytoprotective effect on LPS-induced inflammation in HT-29 cells. We assessed the behavior of LPS-induced cognitive deficit mice using Y-maze, passive avoidance and Morris water maze tests and found that administration of AASWE significantly improved learning and memory function. The AASWE group showed antioxidant activity through downregulation of malondialdehyde levels and upregulation of superoxide dismutase levels in brain tissue. In addition, the AASWE group exhibited activation of the cholinergic system with decreased acetylcholinesterase activity in brain tissue. Furthermore, AASWE effectively downregulated inflammatory mediators such as phosphorylated-JNK, phosphorylated-NF-κB, TNF-α and interleukin-6. The major bioactive compounds of AASWE were identified as quercetin-3-O-arabinopyranosyl(1→2)-rhamnopyranosyl(1→6)-glucopyranose, quercetin-3-O-apiosyl(1 → 2)-galactoside, rutin, and 3-caffeoylquinic acid. Based on these results, we suggest that AASWE not only increases the growth of beneficial bacteria in the intestines, but also shows an ameliorating effect on LPS-induced cognitive impairment.

키워드

참고문헌

  1. Duerkop BA, Vaishnava S, Hooper LV. 2009. Immune responses to the microbiota at the intestinal mucosal surface. Immunity 31: 368-376. https://doi.org/10.1016/j.immuni.2009.08.009
  2. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. 2012. Host-gut microbiota metabolic interactions. Science 336: 1262-1267. https://doi.org/10.1126/science.1223813
  3. Caracciolo B, Xu W, Collins S, Fratiglioni L. 2014. Cognitive decline, dietary factors and gut-brain interactions. Mech. Ageing Dev. 136: 59-69. https://doi.org/10.1016/j.mad.2013.11.011
  4. Noble EE, Hsu TM, Kanoski SE. 2017. Gut to brain dysbiosis: Mechanisms linking western diet consumption, the microbiome, and cognitive impairment. Front. Behav. Neurosci. 11: 9. https://doi.org/10.3389/fnbeh.2017.00009
  5. Jia S, Lu Z, Gao Z, An J, Wu X, Li X, et al. 2016. Chitosan oligosaccharides alleviate cognitive deficits in an amyloid-β1-42-induced rat model of Alzheimer's disease. Int. J. Biol. Macromol. 83: 416-425. https://doi.org/10.1016/j.ijbiomac.2015.11.011
  6. Yen CH, Wang CH, Wu WT, Chen HL. 2016. Fructo-oligosaccharide improved brain β-amyloid, β-secretase, cognitive function, and plasma antioxidant levels in D-galactose-treated Balb/cJ mice. Nutr. Neurosci. 20: 228-237. https://doi.org/10.1080/1028415X.2015.1110952
  7. Singh TP, Kaur G, Malik RK, Schillinger U, Guigas C, Kapila S. 2012. Characterization of intestinal Lactobacillus reuteri strains as potential probiotics. Probiotics Antimicrob. Proteins 4: 47-58. https://doi.org/10.1007/s12602-012-9090-2
  8. Cryan JF, O'mahony SM. 2011. The microbiome-gut-brain axis: From bowel to behavior. Neurogastroenterol. Motil. 23: 187-192. https://doi.org/10.1111/j.1365-2982.2010.01664.x
  9. Lee YJ, Choi DY, Yun YP, Han SB, Oh KW, Hong JT. 2013. Epigallocatechin-3-gallate prevents systemic inflammation-induced memory deficiency and amyloidogenesis via its anti-neuroinflammatory properties. J. Nutr. Biochem. 24: 298-310. https://doi.org/10.1016/j.jnutbio.2012.06.011
  10. Lim H, Kang S, Park M, Yoon J, Han B, Choi S, et al. 2006. Anti-oxidative and nitric oxide production inhibitory activities of phenolic compounds from the fruits of Actinidia argute. Nat. Prod. Sci. 12: 221-225.
  11. Ha JS, Jin DE, Park SK, Park CH, Seung TW, Bae DW, et al. 2015. Antiamnesic effect of Actinidia arguta extract intake in a mouse model of TMT-induced learning and memory dysfunction. Evid.-Based Complement. Altern. Med. 2015: 876484.
  12. Kim HY, Hwang KW, Park SY. 2014. Extracts of Actinidia arguta stems inhibited LPS-induced inflammatory responses through nuclear factor-κB pathway in Raw 264.7 cells. Nutr. Res. 34: 1008-1016. https://doi.org/10.1016/j.nutres.2014.08.019
  13. Lee AY, Kang MJ, Choe E, Kim JI. 2015. Hypoglycemic and antioxidant effects of Daraesoon (Actinidia arguta shoot) in animal models of diabetes mellitus. Nutr. Res. Pract. 9: 262-267. https://doi.org/10.4162/nrp.2015.9.3.262
  14. Qiao Y, Sun J, Xia S, Li L, Li Y, Wang P, et al. 2015. Effects of different Lactobacillus reuteri on inflammatory and fat storage in high-fat diet-induced obesity mice model. J. Funct. Food 14: 424-434. https://doi.org/10.1016/j.jff.2015.02.013
  15. Reza MA, Hossain MA, Lee SJ, Kim JC, Park SC. 2016. In vitro prebiotic effects and quantitative analysis of Bulnesia sarmienti extract. J. Food Drug Anal. 24: 822-830. https://doi.org/10.1016/j.jfda.2016.03.015
  16. He W, Liu X, Xu H, Gong Y, Yuan F, Gao Y. 2010. On-line HPLC-ABTS screening and HPLC-DAD-MS/MS identification of free radical scavengers in Gardenia (Gardenia jasminoides Ellis) fruit extracts. Food Chem. 123: 521-528. https://doi.org/10.1016/j.foodchem.2010.04.030
  17. Hvattum E. 2010. Determination of phenolic compounds in rose hip (Rosa canina) using liquid chromatography coupled to electrospray ionisation tandem mass spectrometry and diode-array detection. Rapid Commun. Mass Spectrom. 16: 655-662. https://doi.org/10.1002/rcm.622
  18. Khallouki F, Voggel J, Breuer A, Klika KD, Ulrich CM, Owen RW. 2017. Comparison of the major polyphenols in mature argan fruits from two regions of Morocco. Food Chem. 221: 1034-1040. https://doi.org/10.1016/j.foodchem.2016.11.058
  19. Ye M, Yan Y, Guo DA. 2005. Characterization of phenolic compounds in the Chinese herbal drug Tu-Si-Zi by liquid chromatography coupled to electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 19: 1469-1484. https://doi.org/10.1002/rcm.1944
  20. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, et al. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc. Natl. Acad. Sci. USA 108: 16050-16055. https://doi.org/10.1073/pnas.1102999108
  21. Savignac HM, Kiely B, Dinan TG, Cryan JF. 2014. Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice. Neurogastroenterol. Motil. 26: 1615-1627. https://doi.org/10.1111/nmo.12427
  22. Gareau MG, Jury J, MacQueen G, Sherman PM, Perdue MH. 2007. Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 56: 1522-1528. https://doi.org/10.1136/gut.2006.117176
  23. Parkar SG, Simmons L, Herath TD, Phipps JE, Trower TM, Hedderley DI, et al. 2017. Evaluation of the prebiotic potential of five kiwifruit cultivars after simulated gastrointestinal digestion and fermentation with human faecal bacteria. Int. J. Food Sci. Technol. 53: 1203-1210. https://doi.org/10.1111/ijfs.13697
  24. Duary RK, Batish VK, Grover S. 2014. Immunomodulatory activity of two potential probiotic strains in LPS-stimulated HT-29 cells. Genes Nutr. 9: 398. https://doi.org/10.1007/s12263-014-0398-2
  25. Kanauchi O, Serizawa I, Araki Y, Suzuki A, Andoh A, Fujiyama Y, et al. 2003. Germinated barley foodstuff, a prebiotic product, ameliorates inflammation of colitis through modulation of the enteric environment. J. Gastroenterol. 38: 134-141. https://doi.org/10.1007/s005350300022
  26. Saulnier DM, Ringel Y, Heyman MB, Foster JA, Bercik P, Shulman RJ, et al. 2013. The intestinal microbiome, probiotics and prebiotics in neurogastroenterology. Gut Microbes 4: 17-27. https://doi.org/10.4161/gmic.22973
  27. Patil CS, Singh VP, Satyanarayan PSV, Jain NK, Singh A, Kulkarni SK. 2003. Protective effect of flavonoids against aging-and lipopolysaccharide-induced cognitive impairment in mice. Pharmacology 69: 59-67. https://doi.org/10.1159/000072357
  28. Padurariu M, Ciobica A, Hritcu L, Stoica B, Bild W, Stefanescu C. 2010. Changes of some oxidative stress markers in the serum of patients with mild cognitive impairment and Alzheimer's disease. Neurosci. Lett. 469: 6-10. https://doi.org/10.1016/j.neulet.2009.11.033
  29. Hsia CH, Wang CH, Kuo YW, Ho YJ, Chen HL. 2012. Fructo-oligosaccharide systemically diminished D-galactose-induced oxidative molecule damages in BALB/cJ mice. Br. J. Nutr. 107: 1787-1792. https://doi.org/10.1017/S0007114511005150
  30. Tyagi E, Agrawal R, Nath C, Shukla R. 2008, Influence of LPS-induced neuroinflammation on acetylcholinesterase activity in rat brain. J. Neuroimmunol. 205: 51-56. https://doi.org/10.1016/j.jneuroim.2008.08.015
  31. Lim YJ, Oh CS, Park YD, Eom SH, Kim DO, Kim UJ, et al. 2014. Physiological components of kiwifruits with in vitro antioxidant and acetylcholinesterase inhibitory activities. Food Sci. Biotechnol. 23: 943-949. https://doi.org/10.1007/s10068-014-0127-z
  32. Goujon E, Parnet P, Laye S, Combe C, Dantzer R. 1996. Adrenalectomy enhances pro-inflammatory cytokines gene expression, in the spleen, pituitary and brain of mice in response to lipopolysaccharide. Mol. Brain Res. 36: 53-62. https://doi.org/10.1016/0169-328X(95)00242-K
  33. Roth J, De Souza GEP. 2001. Fever induction pathways: Evidence from responses to systemic or local cytokine formation. Braz. J. Med. Biol. Res. 34: 301-314. https://doi.org/10.1590/s0100-879x2001000300003
  34. Banks WA. 2005. Blood-brain barrier transport of cytokines: A mechanism for neuropathology. Curr. Pharm. Design 11: 973-984. https://doi.org/10.2174/1381612053381684
  35. Savignac HM, Couch Y, Stratford M, Bannerman DM, Tzortzis G, Anthony DC, et al. 2016. Prebiotic administration normalizes lipopolysaccharide (LPS)-induced anxiety and cortical 5-HT2A receptor and IL1-β levels in male mice. Brain Behav. Immun. 52: 120-131. https://doi.org/10.1016/j.bbi.2015.10.007
  36. Shokryazdan P, Jahromi MF, Navidshad B, Liang JB. 2017. Effects of prebiotics on immune system and cytokine expression. Med. Microbiol. Immunol. 206: 1-9. https://doi.org/10.1007/s00430-016-0481-y
  37. Qiao Y, Ruan Y, Xiong C, Xu Q, Wei P, Ma P, et al. 2010. Chitosan oligosaccharides suppressant LPS binding to TLR4/MD-2 receptor complex. Carbohydr. Polym. 82: 405-411. https://doi.org/10.1016/j.carbpol.2010.04.079
  38. Kim HP, Son KH, Chang HW, Kang SS. 2004. Anti-inflammatory plant flavonoids and cellular action mechanisms. J. Pharmacol. Sci. 96: 229-245. https://doi.org/10.1254/jphs.CRJ04003X
  39. Hou Y, Aboukhatwa MA, Lei DL, Manaye K, Khan I, Luo Y. 2010. Anti-depressant natural flavonols modulate BDNF and beta amyloid in neurons and hippocampus of double TgAD mice. Neuropharmacology 58: 911-920. https://doi.org/10.1016/j.neuropharm.2009.11.002
  40. Sergent T, Piront N, Meurice J, Toussaint O, Schneider YJ. 2010. Anti-inflammatory effects of dietary phenolic compounds in an in vitro model of inflamed human intestinal epithelium. Chem. Biol. Interact. 188: 659-667. https://doi.org/10.1016/j.cbi.2010.08.007
  41. Scalbert A, Morand C, Manach C, Remesy C. 2002. Absorption and metabolism of polyphenols in the gut and impact on health. Biomed. Pharmacother. 56: 276-282. https://doi.org/10.1016/S0753-3322(02)00205-6
  42. Wang D, Ho L, Faith J, Ono K, Janle EM, Lachcik PJ, et al. 2015. Role of intestinal microbiota in the generation of polyphenol-derived phenolic acid mediated attenuation of Alzheimer's disease β-amyloid oligomerization. Mol. Nutr. Food Res. 59: 1025-1040. https://doi.org/10.1002/mnfr.201400544
  43. Etxeberria U, Fernandez-Quintela A, Milagro FI, Aguirre L, Martinez JA, Portillo MP. 2013. Impact of polyphenols and polyphenolrich dietary sources on gut microbiota composition. J. Agric. Food Chem. 61: 9517-9533. https://doi.org/10.1021/jf402506c
  44. China R, Mukherjee S, Sen S, Bose S, Datta S, Koley H, et al. 2012. Antimicrobial activity of Sesbania grandiflora flower polyphenol extracts on some pathogenic bacteria and growth stimulatory effect on the probiotic organism Lactobacillus acidophilus. Microbiol. Res. 167: 500-506. https://doi.org/10.1016/j.micres.2012.04.003
  45. Comalada M, Camuesco D, Sierra S, Ballester I, Xaus J, Galvez J, et al. 2005. In vivo quercitrin anti-inflammatory effect involves release of quercetin, which inhibits inflammation through down-regulation of the NF-κB pathway. Eur. J. Immunol. 35: 584-592. https://doi.org/10.1002/eji.200425778