Nutrition Research and Practice

  • 제15권2호
  • /
  • Pages.173-186
  • /
  • 2021
  • /
  • 1976-1457(pISSN)
  • /
  • 2005-6168(eISSN)
한국영양학회 (The Korean Nutrition Society)
권호 표지
DOI QR코드

DOI QR Code

Effects of the fermented Zizyphus jujuba in the amyloid β25-35-induced Alzheimer's disease mouse model

  • Kim, Min Jeong (Department of Food Science and Nutrition, Pusan National University) ;
  • Jung, Ji Eun (Department of Food Science and Nutrition, Pusan National University) ;
  • Lee, Sanghyun (Department of Plant Science and Technology, Chung-Ang University) ;
  • Cho, Eun Ju (Department of Food Science and Nutrition, Pusan National University) ;
  • Kim, Hyun Young (Department of Food Science, Gyeongnam National University of Science and Technology)
  • 투고 : 2020.04.16
  • 심사 : 2020.08.06
  • 발행 : 2021.04.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

BACKGROUD/OBJECTIVES: Alzheimer's disease (AD) is the most common cause of dementia in the elderly. Due to the increased incidence of dementia, there is a corresponding increase concerning the importance of AD. In this study, we investigated the protective effects conferred by Zizyphus jujuba (Zj) and Zizyphus jujuba fermented by yeast (Zj-Y), on cognitive impairment in an AD mouse model. MATERIALS/METHODS: AD was induced by injecting amyloid beta25-35 (Aβ25-35) in ICR mice, and subsequently 200 mg/kg Zj or Zj-Y was administered daily for 14 days. The cognitive ability of AD mice was observed through behavioral experiments in T-maze, novel object recognition, and Morris water maze tests. We subsequently measured the levels of malondialdehyde (MDA), nitric oxide (NO), aspartate aminotransferase, and alanine aminotransferase in either tissues or serum. RESULTS: In behavioral tests, deterioration was revealed in the short- and long-term learning and memory functions in the Aβ25-35-injected control group compared to the normal group, indicating that Aβ25-35 injection impairs cognitive functions. However, administration of Zj and Zj-Y improved cognitive function in mice, as compared to the Aβ25-35-injected control mice. In addition, the Aβ25-35 induced elevations of MDA and NO in the brain, kidney, and liver were suppressed after exposure to Zj and Zj-Y. Especially, Zj-Y showed stronger scavenging effect against MDA and NO, as compared to Zj. CONCLUSIONS: Results of the present study indicate that Zj-Y exerts a protective effect on cognitive impairment and memory dysfunction, which is exerted by attenuating the oxidative stress induced by Aβ25-35.

키워드

참고문헌

  1. Tsunekawa H, Noda Y, Mouri A, Yoneda F, Nabeshima T. Synergistic effects of selegiline and donepezil on cognitive impairment induced by amyloid beta (25-35). Behav Brain Res 2008;190:224-32. https://doi.org/10.1016/j.bbr.2008.03.002
  2. Moreira PI. Alzheimer's disease and diabetes: an integrative view of the role of mitochondria, oxidative stress, and insulin. J Alzheimers Dis 2012;30 Suppl 2:S199-215. https://doi.org/10.3233/JAD-2011-111127
  3. Coley N, Andrieu S, Gardette V, Gillette-Guyonnet S, Sanz C, Vellas B, Grand A. Dementia prevention: methodological explanations for inconsistent results. Epidemiol Rev 2008;30:35-66. https://doi.org/10.1093/epirev/mxn010
  4. Selkoe DJ. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 2001;81:741-66. https://doi.org/10.1152/physrev.2001.81.2.741
  5. Reddy PH, Beal MF. Amyloid beta, mitochondrial dysfunction and synaptic damage: implications for cognitive decline in aging and Alzheimer's disease. Trends Mol Med 2008;14:45-53. https://doi.org/10.1016/j.molmed.2007.12.002
  6. Chang SC, Hsu BY, Chen BH. Structural characterization of polysaccharides from Zizyphus jujuba and evaluation of antioxidant activity. Int J Biol Macromol 2010;47:445-53. https://doi.org/10.1016/j.ijbiomac.2010.06.010
  7. Li J, Liu Y, Fan L, Ai L, Shan L. Antioxidant activities of polysaccharides from the fruiting bodies of Zizyphus Jujuba cv. Jinsixiaozao. Carbohydr Polym 2011;84:390-4. https://doi.org/10.1016/j.carbpol.2010.11.051
  8. Jung JE, Cho EJ. Protective effects of Zizyphus jujuba and fermented Zizyphus jujuba from free radicals and hair loss. J Korean Soc Food Sci Nutr 2014;43:1174-80. https://doi.org/10.3746/JKFN.2014.43.8.1174
  9. Yu L, Jiang BP, Luo D, Shen XC, Guo S, Duan JA, Tang YP. Bioactive components in the fruits of Ziziphus jujuba Mill. against the inflammatory irritant action of Euphorbia plants. Phytomedicine 2012;19:239-44. https://doi.org/10.1016/j.phymed.2011.09.071
  10. Kaeidi A, Taati M, Hajializadeh Z, Jahandari F, Rashidipour M. Aqueous extract of Zizyphus jujuba fruit attenuates glucose induced neurotoxicity in an in vitro model of diabetic neuropathy. Iran J Basic Med Sci 2015;18:301-6.
  11. Gao QH, Wu CS, Wang M. The jujube (Ziziphus jujuba Mill.) fruit: a review of current knowledge of fruit composition and health benefits. J Agric Food Chem 2013;61:3351-63. https://doi.org/10.1021/jf4007032
  12. Zhang Y, Yang X, Jin G, Yang X, Zhang Y. Polysaccharides from Pleurotus ostreatus alleviate cognitive impairment in a rat model of Alzheimer's disease. Int J Biol Macromol 2016;92:935-41. https://doi.org/10.1016/j.ijbiomac.2016.08.008
  13. Deng LL, Yuan D, Zhou ZY, Wan JZ, Zhang CC, Liu CQ, Dun YY, Zhao HX, Zhao B, Yang YJ, Wang T. Saponins from Panax japonicus attenuate age-related neuroinflammation via regulation of the mitogen-activated protein kinase and nuclear factor kappa B signaling pathways. Neural Regen Res 2017;12:1877-84. https://doi.org/10.4103/1673-5374.219047
  14. Stanton C, Ross RP, Fitzgerald GF, Van Sinderen D. Fermented functional foods based on probiotics and their biogenic metabolites. Curr Opin Biotechnol 2005;16:198-203. https://doi.org/10.1016/j.copbio.2005.02.008
  15. Gumienna M, Szwengiel A, Górna B. Bioactive components of pomegranate fruit and their transformation by fermentation processes. Eur Food Res Technol 2016;242:631-40. https://doi.org/10.1007/s00217-015-2582-z
  16. Milani EA, Silva FV. Ultrasound assisted thermal pasteurization of beers with different alcohol levels: Inactivation of Saccharomyces cerevisiae ascospores. J Food Eng 2017;198:45-53. https://doi.org/10.1016/j.jfoodeng.2016.11.015
  17. Struyf N, Laurent J, Verspreet J, Verstrepen KJ, Courtin CM. Substrate-limited Saccharomyces cerevisiae yeast strains allow control of fermentation during bread making. J Agric Food Chem 2017;65:3368-77. https://doi.org/10.1021/acs.jafc.7b00313
  18. Ju HK, Cho EJ, Jang MH, Lee YY, Hong SS, Park JH, Kwon SW. Characterization of increased phenolic compounds from fermented Bokbunja (Rubus coreanus Miq.) and related antioxidant activity. J Pharm Biomed Anal 2009;49:820-7. https://doi.org/10.1016/j.jpba.2008.12.024
  19. Jung YM, Lee SH, Lee DS, You MJ, Chung IK, Cheon WH, Kwon YS, Lee YJ, Ku SK. Fermented garlic protects diabetic, obese mice when fed a high-fat diet by antioxidant effects. Nutr Res 2011;31:387-96. https://doi.org/10.1016/j.nutres.2011.04.005
  20. Pawlowska AM, Camangi F, Bader A, Braca A. Flavonoids of Zizyphus jujuba L. and Zizyphus spina-christi (L.) Willd (Rhamnaceae) fruits. Food Chem 2009;112:858-62. https://doi.org/10.1016/j.foodchem.2008.06.053
  21. Laursen SE, Belknap JK. Intracerebroventricular injections in mice. Some methodological refinements. J Pharmacol Methods 1986;16:355-7. https://doi.org/10.1016/0160-5402(86)90038-0
  22. Montgomery KC. A test of two explanations of spontaneous alternation. J Comp Physiol Psychol 1952;45:287-93. https://doi.org/10.1037/h0058118
  23. Bevins RA, Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory'. Nat Protoc 2006;1:1306-11. https://doi.org/10.1038/nprot.2006.205
  24. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984;11:47-60. https://doi.org/10.1016/0165-0270(84)90007-4
  25. Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 1978;86:271-8. https://doi.org/10.1016/0003-2697(78)90342-1
  26. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 1982;126:131-8. https://doi.org/10.1016/0003-2697(82)90118-X
  27. Schmidt HH, Warner TD, Nakane M, Forstermann U, Murad F. Regulation and subcellular location of nitrogen oxide synthases in RAW264.7 macrophages. Mol Pharmacol 1992;41:615-24.
  28. Reitman S, Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol 1957;28:56-63. https://doi.org/10.1093/ajcp/28.1.56
  29. Woo M, Noh JS, Cho EJ, Song YO. Bioactive compounds of kimchi inhibit apoptosis by attenuating endoplasmic reticulum stress in the brain of amyloid β-injected mice. J Agric Food Chem 2018;66:4883-90. https://doi.org/10.1021/acs.jafc.8b01686
  30. Shen X, Tang Y, Yang R, Yu L, Fang T, Duan JA. The protective effect of Zizyphus jujube fruit on carbon tetrachloride-induced hepatic injury in mice by anti-oxidative activities. J Ethnopharmacol 2009;122:555-60. https://doi.org/10.1016/j.jep.2009.01.027
  31. Blennow K, de Leon MJ, Zetterberg H. Alzheimer's disease. Lancet 2006;368:387-403. https://doi.org/10.1016/S0140-6736(06)69113-7
  32. Lu P, Mamiya T, Lu L, Mouri A, Ikejima T, Kim HC, Zou LB, Nabeshima T. Xanthoceraside attenuates amyloid β peptide25-35-induced learning and memory impairments in mice. Psychopharmacology (Berl) 2012;219:181-90. https://doi.org/10.1007/s00213-011-2386-1
  33. Lee AY, Hwang BR, Lee MH, Lee S, Cho EJ. Perilla frutescens var. japonica and rosmarinic acid improve amyloid-β25-35 induced impairment of cognition and memory function. Nutr Res Pract 2016;10:274-81. https://doi.org/10.4162/nrp.2016.10.3.274
  34. Kim JH, Lee JM, Lee SH, Cho EJ. Quercetin and quercetin-3-β-d-glucoside improve cognitive and memory function in Alzheimer's disease mouse. Appl Biol Chem 2016;59:721-8. https://doi.org/10.1007/s13765-016-0217-0
  35. Splittstoesser DF. Microorganisms involved in the spoilage of fermented fruit juices. J Food Prot 1982;45:874-7. https://doi.org/10.4315/0362-028x-45.9.874
  36. Romero AM, Doval MM, Sturla MA, Judis MA. Antioxidant properties of polyphenol-containing extract from soybean fermented with Saccharomyces cerevisiae. Eur J Lipid Sci Technol 2004;106:424-31. https://doi.org/10.1002/ejlt.200400953
  37. Zhao L, Liu F, Wu L, Xue X, Hou F. Fate of triadimefon and its metabolite triadimenol in jujube samples during jujube wine and vinegar processing. Food Control 2017;73:468-73. https://doi.org/10.1016/j.foodcont.2016.08.039
  38. Jung SW, Noh WS. The effect of jujube extract on the growth of lactic acid bacteria. J East Asian Soc Diet Life 2006;16:349-56.
  39. Eom IJ, Choi JI, Kim IH, Kim TH, Kim SH. Changes in the physicochemical and antioxidant characteristics during the fermentation of jujube wine using hot water extract of dried jujube. J Life Sci 2016;26:1298-307. https://doi.org/10.5352/JLS.2016.26.11.1298
  40. Jung JE. The protective effects of Zizyphus jujuba and fermented Zizyphus jujuba from oxidative stress, recognition impairment and hair loss [Master's thesis]. Busan: Pusan National University; 2011.
  41. Ghaly IS, Said A, Abdel-Wahhab MA. Zizyphus jujuba and Origanum majorana extracts protect against hydroquinone-induced clastogenicity. Environ Toxicol Pharmacol 2008;25:10-9. https://doi.org/10.1016/j.etap.2007.07.002
  42. Dudchenko PA. An overview of the tasks used to test working memory in rodents. Neurosci Biobehav Rev 2004;28:699-709. https://doi.org/10.1016/j.neubiorev.2004.09.002
  43. Frick KM, Baxter MG, Markowska AL, Olton DS, Price DL. Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol Aging 1995;16:149-60. https://doi.org/10.1016/0197-4580(94)00155-3
  44. Antunes M, Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 2012;13:93-110. https://doi.org/10.1007/s10339-011-0430-z
  45. Reisel D, Bannerman DM, Schmitt WB, Deacon RM, Flint J, Borchardt T, Seeburg PH, Rawlins JN. Spatial memory dissociations in mice lacking GluR1. Nat Neurosci 2002;5:868-73. https://doi.org/10.1038/nn910
  46. Vorhees CV, Williams MT. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 2006;1:848-58. https://doi.org/10.1038/nprot.2006.116
  47. Rabiei Z, Rafieian-Kopaei M, Heidarian E, Saghaei E, Mokhtari S. Effects of Zizyphus jujube extract on memory and learning impairment induced by bilateral electric lesions of the nucleus Basalis of Meynert in rat. Neurochem Res 2014;39:353-60. https://doi.org/10.1007/s11064-013-1232-8
  48. Butterfield DA, Lauderback CM. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress. Free Radic Biol Med 2002;32:1050-60. https://doi.org/10.1016/S0891-5849(02)00794-3
  49. Tullberg C, Larsson K, Carlsson NG, Comi I, Scheers N, Vegarud G, Undeland I. Formation of reactive aldehydes (MDA, HHE, HNE) during the digestion of cod liver oil: comparison of human and porcine in vitro digestion models. Food Funct 2016;7:1401-12. https://doi.org/10.1039/c5fo01332a
  50. Fonseca I, Reguengo H, Almeida M, Dias L, Martins LS, Pedroso S, Santos J, Lobato L, Henriques AC, Mendonca D. Oxidative stress in kidney transplantation: malondialdehyde is an early predictive marker of graft dysfunction. Transplantation 2014;97:1058-65. https://doi.org/10.1097/01.TP.0000438626.91095.50
  51. Greilberger J, Koidl C, Greilberger M, Lamprecht M, Schroecksnadel K, Leblhuber F, Fuchs D, Oettl K. Malondialdehyde, carbonyl proteins and albumin-disulphide as useful oxidative markers in mild cognitive impairment and Alzheimer's disease. Free Radic Res 2008;42:633-8. https://doi.org/10.1080/10715760802255764
  52. Wallace MN, Geddes JG, Farquhar DA, Masson MR. Nitric oxide synthase in reactive astrocytes adjacent to β-amyloid plaques. Exp Neurol 1997;144:266-72. https://doi.org/10.1006/exnr.1996.6373
  53. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996;271:C1424-37. https://doi.org/10.1152/ajpcell.1996.271.5.C1424
  54. Law A, Gauthier S, Quirion R. Neuroprotective and neurorescuing effects of isoform-specific nitric oxide synthase inhibitors, nitric oxide scavenger, and antioxidant against beta-amyloid toxicity. Br J Pharmacol 2001;133:1114-24. https://doi.org/10.1038/sj.bjp.0704179
  55. Jung JE, Cho EJ. Enhancement of anti-inflammatory effect of Zizyphus jujuba var. inermis fruits by fermentation. Cancer Prev Res 2011;16:263-8.
  56. Whitehead MW, Hawkes ND, Hainsworth I, Kingham JG. A prospective study of the causes of notably raised aspartate aminotransferase of liver origin. Gut 1999;45:129-33. https://doi.org/10.1136/gut.45.1.129
  57. Kim WR, Flamm SL, Di Bisceglie AM, Bodenheimer HC; Public Policy Committee of the American Association for the Study of Liver Disease. Serum activity of alanine aminotransferase (ALT) as an indicator of health and disease. Hepatology 2008;47:1363-70. https://doi.org/10.1002/hep.22109
  58. Chen J, Li Z, Maiwulanjiang M, Zhang WL, Zhan JY, Lam CT, Zhu KY, Yao P, Choi RC, Lau DT, Dong TT, Tsim KW. Chemical and biological assessment of Ziziphus jujuba fruits from China: different geographical sources and developmental stages. J Agric Food Chem 2013;61:7315-24. https://doi.org/10.1021/jf402379u
  59. Kwon H, Jung IH, Yi JH, Kim JH, Park JH, Lee S, Jung JW, Lee YC, Ryu JH, Kim DH. The seed of Zizyphus jujuba var. spinosa attenuates Alzheimer's disease-associated hippocampal synaptic deficits through BDNF/TrkB signaling. Biol Pharm Bull 2017;40:2096-104. https://doi.org/10.1248/bpb.b17-00378
  60. Ko SY, Lee HE, Park SJ, Jeon SJ, Kim B, Gao Q, Jang DS, Ryu JH. Spinosin, a C-Glucosylflavone, from Zizyphus jujuba var. spinosa ameliorates Aβ1-42 oligomer-induced memory impairment in mice. Biomol Ther 2015;23:156-64. https://doi.org/10.4062/biomolther.2014.110
  61. Chen J, Maiwulanjiang M, Lam KY, Zhang WL, Zhan JY, Lam CT, Xu SL, Zhu KY, Yao P, Lau DT, Dong TT, Tsim KW. A standardized extract of the fruit of Ziziphus jujuba (Jujube) induces neuronal differentiation of cultured PC12 cells: a signaling mediated by protein kinase A. J Agric Food Chem 2014;62:1890-7. https://doi.org/10.1021/jf405093f
  62. Chen J, Yan AL, Lam KY, Lam CT, Li N, Yao P, Xiong A, Dong TT, Tsim KW. A chemically standardized extract of Ziziphus jujuba fruit (Jujube) stimulates expressions of neurotrophic factors and anti-oxidant enzymes in cultured astrocytes. Phytother Res 2014;28:1727-30. https://doi.org/10.1002/ptr.5202
  63. Hwang IK, Yoo KY, Yoo DY, Choi JH, Lee CH, Kang IJ, Kwon DY, Kim YS, Kim DW, Won MH. Zizyphus enhances cell proliferation and neuroblast differentiation in the subgranular zone of the dentate gyrus in middle-aged mice. J Med Food 2011;14:195-200. https://doi.org/10.1089/jmf.2010.1123
  64. Chen J, Liu X, Li Z, Qi A, Yao P, Zhou Z, Dong TT, Tsim KW. A review of dietary Ziziphus jujuba Fruit (Jujube): developing health food supplements for brain protection. Evid Based Complement Alternat Med 2017;2017:3019568.
  65. Kim NM, Lee JW, Do JH, Park CK, Yang JW. Effects of the fermentation periods on the qualities and functionality of the vegetable fermented broth. Korean J Med Crop Sci 2005;13:293-9.
  66. Hyon JS, Kang SM, Han SW, Kang MC, Oh MC, Oh CK, Kim DW, Jeon YJ, Kim SH. Flavonoid component changes and antioxidant activities of fermented Citrus gradis osbeck peel. J Korean Soc Food Sci Nutr 2009;38:1310-6. https://doi.org/10.3746/JKFN.2009.38.10.1310