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Soybean Meal Extract Preserves Memory Ability by Increasing Presynaptic Function and Modulating Gut Microbiota in Rats

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Abstract

Age-related degenerative brain diseases frequently manifest as memory deficits. Dietary interventions or nutraceuticals may provide efficacious treatments through prevention and cure. Soybean meal, a byproduct of soy oil refining, has health benefits, but its effect on memory function is unknown. Therefore, we evaluated the effect of the oral administration of soybean meal extract (SME) for 2 weeks on memory function using the Morris water maze (MWM) test in healthy rats and investigated the possible underlying mechanisms. First, analysis of the composition revealed that SME is rich in isoflavones; SME did not exhibit hepatotoxicity or renal toxicity at the different doses tested. The MWM results revealed that the escape latency and movement distance of rats were significantly shorter in the SME group than in the control group, indicating that SME can help in memory preservation. In addition, SME increased the levels of presynaptic proteins such as synaptophysin, synaptobrevin, synaptotagmin, syntaxin, synapsin I, and 25-kDa synaptosome-associated protein as well as protein kinases and their phosphorylated expression, including extracellular signal-regulated kinases 1 and 2 (ERK1/2), protein kinase C (PKC), and Ca2+/calmodulin-dependent protein kinase II (CaMKII) in the hippocampal nerve terminals (synaptosomes). Transmission electron microscopy also indicated that SME increased the number of synaptic vesicles in hippocampal synaptosomes. Furthermore, SME rats exhibited altered microbiota composition compared with control rats. Therefore, our data suggest that SME can increase presynaptic function and modulate gut microbiota, thus aiding in memory preservation in rats.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Hou Y, Dan X, Babbar M, Wei Y, Hasselbalch SG, Croteau DL, Bohr VA (2019) Ageing as a risk factor for neurodegenerative disease. Nat Rev Neurol 15(10):565–581. https://doi.org/10.1038/s41582-019-0244-7

    Article  PubMed  Google Scholar 

  2. Lutz W, Sanderson W, Scherbov S (2008) The coming acceleration of global population ageing. Nature 451(7179):716–719. https://doi.org/10.1038/nature06516

    Article  CAS  PubMed  Google Scholar 

  3. Harada CN, Natelson Love MC, Triebel KL (2013) Normal cognitive aging. Clin Geriatr Med 29(4):737–752. https://doi.org/10.1016/j.cger.2013.07.002

    Article  PubMed  PubMed Central  Google Scholar 

  4. Williams P, Sorribas A, Howes MJ (2011) Natural products as a source of Alzheimer’s drug leads. Nat Prod Rep 28(1):48–77. https://doi.org/10.1039/c0np00027b

    Article  CAS  PubMed  Google Scholar 

  5. Miquel S, Champ C, Day J, Aarts E, Bahr BA, Bakker M, Bánáti D, Calabrese V, Cederholm T, Cryan J, Dye L, Farrimond JA, Korosi A, Layé S, Maudsley S, Milenkovic D, Mohajeri MH, Sijben J, Solomon A, Spencer JPE, Thuret S, Vanden Berghe W, Vauzour D, Vellas B, Wesnes K, Willatts P, Wittenberg R, Geurts L (2018) Poor cognitive ageing: vulnerabilities, mechanisms and the impact of nutritional interventions. Ageing Res Rev 42:40–55. https://doi.org/10.1016/j.arr.2017.12.004

    Article  PubMed  Google Scholar 

  6. Gkotzamanis V, Panagiotakos D (2020) Dietary interventions and cognition: a systematic review of clinical trials. Psychiatriki 31(3):248–256. https://doi.org/10.22365/jpsych.2020.313.248

    Article  CAS  PubMed  Google Scholar 

  7. Howes MR, Perry NSL, Vásquez-Londoño C, Perry EK (2020) Role of phytochemicals as nutraceuticals for cognitive functions affected in ageing. Br J Pharmacol 177(6):1294–1315. https://doi.org/10.1111/bph.14898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hu N, Yu JT, Tan L, Wang YL, Sun L, Tan L (2013) Nutrition and the risk of Alzheimer’s disease. Biomed Res Int 2013:524820. https://doi.org/10.1155/2013/524820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Parletta N, Milte CM, Meyer BJ (2013) Nutritional modulation of cognitive function and mental health. J Nutr Biochem 24(5):725–743. https://doi.org/10.1016/j.jnutbio.2013.01.002

    Article  CAS  PubMed  Google Scholar 

  10. Otaegui-Arrazola A, Amiano P, Elbusto A, Urdaneta E, Martínez-Lage P (2014) Diet, cognition, and Alzheimer’s disease: food for thought. Eur J Nutr 53(1):1–23. https://doi.org/10.1007/s00394-013-0561-3

    Article  CAS  PubMed  Google Scholar 

  11. Barnes S (2010) The biochemistry, chemistry and physiology of the isoflavones in soybeans and their food products. Lymphat Res Biol 8(1):89–98. https://doi.org/10.1089/lrb.2009.0030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Pan M, Li Z, Yeung V, Xu RJ (2010) Dietary supplementation of soy germ phytoestrogens or estradiol improves spatial memory performance and increases gene expression of BDNF, TrkB receptor and synaptic factors in ovariectomized rats. Nutr Metab 7:75. https://doi.org/10.1186/1743-7075-7-75

    Article  CAS  Google Scholar 

  13. Murphy PA, Hu J, Barua K, Hauck CC (2008) Group B saponins in soy products in the US Department of Agriculture-Iowa State University isoflavone database and their comparison with isoflavone contents. J Agric Food Chem 56(18):8534–8540. https://doi.org/10.1021/jf800491p

    Article  CAS  PubMed  Google Scholar 

  14. Cha YS, Park Y, Lee M, Chae SW, Park K, Kim Y, Lee HS (2014) Doenjang, a Korean fermented soy food, exerts antiobesity and antioxidative activities in overweight subjects with the PPAR-γ2 C1431T polymorphism: 12-week, double-blind randomized clinical trial. J Med Food 17(1):119–127. https://doi.org/10.1089/jmf.2013.2877

    Article  CAS  PubMed  Google Scholar 

  15. Young D, Ibuki M, Nakamori T, Fan M, Mine Y (2012) Soy-derived di- and tripeptides alleviate colon and ileum inflammation in pigs with dextran sodium sulfate-induced colitis. J Nutr 142(2):363–368. https://doi.org/10.3945/jn.111.149104

    Article  CAS  PubMed  Google Scholar 

  16. Schreihofer DA, Do KD, Schreihofer AM (2005) High-soy diet decreases infarct size after permanent middle cerebral artery occlusion in female rats. Am J Physiol Regul Integr Comp Physiol 289(1):R103-108. https://doi.org/10.1152/ajpregu.00642.2004

    Article  PubMed  Google Scholar 

  17. Qian Y, Guan T, Huang M, Cao L, Li Y, Cheng H, Jin H, Yu D (2012) Neuroprotection by the soy isoflavone, genistein, via inhibition of mitochondria-dependent apoptosis pathways and reactive oxygen induced-NF-κB activation in a cerebral ischemia mouse model. Neurochem Int 60(8):759–767. https://doi.org/10.1016/j.neuint.2012.03.011

    Article  CAS  PubMed  Google Scholar 

  18. Baião DDS, de Freitas CS, Gomes LP, da Silva D, Correa A, Pereira PR, Aguila EMD, Paschoalin VMF (2017) Polyphenols from root, tubercles and grains cropped in brazil: chemical and nutritional characterization and their effects on human health and diseases. Nutrients 9(9). https://doi.org/10.3390/nu9091044

  19. Ding J, Xi YD, Zhang DD, Zhao X, Liu JM, Li CQ, Han J, Xiao R (2013) Soybean isoflavone ameliorates β-amyloid 1–42-induced learning and memory deficit in rats by protecting synaptic structure and function. Synapse 67(12):856–864. https://doi.org/10.1002/syn.21692

    Article  CAS  PubMed  Google Scholar 

  20. Lee HJ, Lim SM, Ko DB, Jeong JJ, Hwang YH, Kim DH (2017) Soyasapogenol B and genistein attenuate lipopolysaccharide-induced memory impairment in mice by the modulation of NF-κB-mediated BDNF expression. J Agric Food Chem 65(32):6877–6885. https://doi.org/10.1021/acs.jafc.7b02569

    Article  CAS  PubMed  Google Scholar 

  21. Essawy AE, Abdou HM, Ibrahim HM, Bouthahab NM (2019) Soybean isoflavone ameliorates cognitive impairment, neuroinflammation, and amyloid β accumulation in a rat model of Alzheimer’s disease. Environ Sci Pollut Res 26(25):26060–26070. https://doi.org/10.1007/s11356-019-05862-z

    Article  CAS  Google Scholar 

  22. Kao TH, Lu YF, Chen BH (2005) Preparative column chromatography of four groups of isoflavones from soybean cake. Eur Food Res Technol 221(3):459–465. https://doi.org/10.1007/s00217-005-1206-4

    Article  CAS  Google Scholar 

  23. Cyntia SF, Alves da Silva G, Perrone D, M AV, Dos SBD, P RP, V MFP, E MDA (2018) Recovery of antimicrobials and bioaccessible isoflavones and phenolics from soybean (Glycine max) meal by aqueous extraction. Molecules 24(1). https://doi.org/10.3390/molecules24010074

  24. Kao TH, Chen BH (2006) Functional components in soybean cake and their effects on antioxidant activity. J Agric Food Chem 54(20):7544–7555. https://doi.org/10.1021/jf061586x

    Article  CAS  PubMed  Google Scholar 

  25. Kao TH, Wu WM, Hung CF, Wu WB, Chen BH (2007) Anti-inflammatory effects of isoflavone powder produced from soybean cake. J Agric Food Chem 55(26):11068–11079. https://doi.org/10.1021/jf071851u

    Article  CAS  PubMed  Google Scholar 

  26. Huang CC, Hsu BY, Wu NL, Tsui WH, Lin TJ, Su CC, Hung CF (2010) Anti-photoaging effects of soy isoflavone extract (aglycone and acetylglucoside form) from soybean cake. Int J Mol Sci 11(12):4782–4795. https://doi.org/10.3390/ijms11124782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Chu T, Wu NL, Hsiao CY, Li HJ, Lin TY, Ku CH, Hung CF (2020) An isoflavone extract from soybean cake suppresses 2,4-dinitrochlorobenzene-induced contact dermatitis. J Ethnopharmacol 263:113037. https://doi.org/10.1016/j.jep.2020.113037

    Article  CAS  PubMed  Google Scholar 

  28. Jang SE, Lim SM, Jeong JJ, Jang HM, Lee HJ, Han MJ, Kim DH (2018) Gastrointestinal inflammation by gut microbiota disturbance induces memory impairment in mice. Mucosal Immunol 11(2):369–379. https://doi.org/10.1038/mi.2017.49

    Article  CAS  PubMed  Google Scholar 

  29. Lu CW, Lin TY, Pan TL, Wang PW, Chiu KM, Lee MY, Wang SJ (2021) Asiatic acid prevents cognitive deficits by inhibiting calpain activation and preserving synaptic and mitochondrial function in rats with kainic acid-induced seizure. Biomedicines 9(3). https://doi.org/10.3390/biomedicines9030284

  30. Feng Y, Cui R, Li Z, Zhang X, Jia Y, Zhang X, Shi J, Qu K, Liu C, Zhang J (2019) Methane alleviates acetaminophen-induced liver injury by inhibiting inflammation, oxidative stress, endoplasmic reticulum stress, and apoptosis through the Nrf2/HO-1/NQO1 signaling pathway. Oxid Med Cell Longev 2019:7067619. https://doi.org/10.1155/2019/7067619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Tu MY, Han KY, Chang GR, Lai GD, Chang KY, Chen CF, Lai JC, Lai CY, Chen HL, Chen CM (2020) Kefir peptides prevent estrogen deficiency-induced bone loss and modulate the structure of the gut microbiota in ovariectomized mice. Nutrients 12(11). https://doi.org/10.3390/nu12113432

  32. Stern Y (2009) Cognitive reserve. Neuropsychologia 47(10):2015–2028. https://doi.org/10.1016/j.neuropsychologia.2009.03.004

    Article  PubMed  PubMed Central  Google Scholar 

  33. Leenders AG, Sheng ZH (2005) Modulation of neurotransmitter release by the second messenger-activated protein kinases: implications for presynaptic plasticity. Pharmacol Ther 105(1):69–84. https://doi.org/10.1016/j.pharmthera.2004.10.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Dinel AL, Lucas C, Guillemet D, Layé S, Pallet V, Joffre C (2020) Chronic supplementation with a mix of Salvia officinalis and Salvia lavandulaefolia improves morris water maze learning in normal adult C57Bl/6J mice. Nutrients 12(6). https://doi.org/10.3390/nu12061777

  35. Lv J, Lu C, Jiang N, Wang H, Huang H, Chen Y, Li Y, Liu X (2021) Protective effect of ginsenoside Rh2 on scopolamine-induced memory deficits through regulation of cholinergic transmission, oxidative stress and the ERK-CREB-BDNF signaling pathway. Phytother Res 35(1):337–345. https://doi.org/10.1002/ptr.6804

    Article  CAS  PubMed  Google Scholar 

  36. Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1(2):848–858. https://doi.org/10.1038/nprot.2006.116

    Article  PubMed  PubMed Central  Google Scholar 

  37. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711. https://doi.org/10.1146/annurev.neuro.23.1.649

    Article  CAS  PubMed  Google Scholar 

  38. Rosenberg T, Gal-Ben-Ari S, Dieterich DC, Kreutz MR, Ziv NE, Gundelfinger ED, Rosenblum K (2014) The roles of protein expression in synaptic plasticity and memory consolidation. Front Mol Neurosci 7:86. https://doi.org/10.3389/fnmol.2014.00086

    Article  PubMed  PubMed Central  Google Scholar 

  39. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313(5790):1141–1144. https://doi.org/10.1126/science.1128657

    Article  CAS  PubMed  Google Scholar 

  40. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313(5790):1093–1097. https://doi.org/10.1126/science.1128134

    Article  CAS  PubMed  Google Scholar 

  41. Südhof TC (2013) Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80(3):675–690. https://doi.org/10.1016/j.neuron.2013.10.022

    Article  CAS  PubMed  Google Scholar 

  42. Rizo J, Xu J (2015) The synaptic vesicle release machinery. Annu Rev Biophys 44:339–367. https://doi.org/10.1146/annurev-biophys-060414-034057

    Article  CAS  PubMed  Google Scholar 

  43. Jovanovic JN, Benfenati F, Siow YL, Sihra TS, Sanghera JS, Pelech SL, Greengard P, Czernik AJ (1996) Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proc Natl Acad Sci USA 93(8):3679–3683. https://doi.org/10.1073/pnas.93.8.3679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Jarvis SE, Zamponi GW (2001) Distinct molecular determinants govern syntaxin 1A-mediated inactivation and G-protein inhibition of N-type calcium channels. J Neurosci 21(9):2939–2948. https://doi.org/10.1523/jneurosci.21-09-02939.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Hinds HL, Goussakov I, Nakazawa K, Tonegawa S, Bolshakov VY (2003) Essential function of alpha-calcium/calmodulin-dependent protein kinase II in neurotransmitter release at a glutamatergic central synapse. Proc Natl Acad Sci USA 100(7):4275–4280. https://doi.org/10.1073/pnas.0530202100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Yamagata Y, Jovanovic JN, Czernik AJ, Greengard P, Obata K (2002) Bidirectional changes in synapsin I phosphorylation at MAP kinase-dependent sites by acute neuronal excitation in vivo. J Neurochem 80(5):835–842. https://doi.org/10.1046/j.0022-3042.2001.00753.x

    Article  CAS  PubMed  Google Scholar 

  47. Chi P, Greengard P, Ryan TA (2003) Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38(1):69–78. https://doi.org/10.1016/s0896-6273(03)00151-x

    Article  CAS  PubMed  Google Scholar 

  48. Lynch MA, Voss KL, Rodriguez J, Bliss TV (1994) Increase in synaptic vesicle proteins accompanies long-term potentiation in the dentate gyrus. Neuroscience 60(1):1–5. https://doi.org/10.1016/0306-4522(94)90197-x

    Article  CAS  PubMed  Google Scholar 

  49. Mullany P, Lynch MA (1997) Changes in protein synthesis and synthesis of the synaptic vesicle protein, synaptophysin, in entorhinal cortex following induction of long-term potentiation in dentate gyrus: an age-related study in the rat. Neuropharmacology 36(7):973–980. https://doi.org/10.1016/s0028-3908(97)00073-7

    Article  CAS  PubMed  Google Scholar 

  50. Schmitt U, Tanimoto N, Seeliger M, Schaeffel F, Leube RE (2009) Detection of behavioral alterations and learning deficits in mice lacking synaptophysin. Neuroscience 162(2):234–243. https://doi.org/10.1016/j.neuroscience.2009.04.046

    Article  CAS  PubMed  Google Scholar 

  51. VanGuilder HD, Yan H, Farley JA, Sonntag WE, Freeman WM (2010) Aging alters the expression of neurotransmission-regulating proteins in the hippocampal synaptoproteome. J Neurochem 113(6):1577–1588. https://doi.org/10.1111/j.1471-4159.2010.06719.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Honer WG, Barr AM, Sawada K, Thornton AE, Morris MC, Leurgans SE, Schneider JA, Bennett DA (2012) Cognitive reserve, presynaptic proteins and dementia in the elderly. Transl Psychiatry 2(5):e114. https://doi.org/10.1038/tp.2012.38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ramos-Miguel A, Jones AA, Petyuk VA, Barakauskas VE, Barr AM, Leurgans SE, De Jager PL, Casaletto KB, Schneider JA, Bennett DA, Honer WG (2021) Proteomic identification of select protein variants of the SNARE interactome associated with cognitive reserve in a large community sample. Acta Neuropathol 141(5):755–770. https://doi.org/10.1007/s00401-021-02282-7

    Article  CAS  PubMed  Google Scholar 

  54. Mullany P, Lynch MA (1997) Changes in protein synthesis and synthesis of the synaptic vesicle protein, synaptophysin, in entorhi- nal cortex following induction of long-term potentiation in dentate gyrus: An age-related study in the rat. Neuropharmacology 36(7):973–980. https://doi.org/10.1016/s0028-3908(97)00073-7

    Article  CAS  PubMed  Google Scholar 

  55. McEntee WJ, Crook TH (1993) Glutamate: its role in learning, memory, and the aging brain. Psychopharmacology 111(4):391–401. https://doi.org/10.1007/BF02253527

    Article  CAS  PubMed  Google Scholar 

  56. Hoffman JD, Parikh I, Green SJ, Chlipala G, Mohney RP, Keaton M, Bauer B, Hartz AMS, Lin AL (2017) Age drives distortion of brain metabolic, vascular and cognitive functions, and the gut microbiome. Front Aging Neurosci 9:298. https://doi.org/10.3389/fnagi.2017.00298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Wang S, Jiang W, Ouyang T, Shen XY, Wang F, Qu YH, Zhang M, Luo T, Wang HQ (2019) Jatrorrhizine balances the gut microbiota and reverses learning and memory deficits in APP/PS1 transgenic mice. Sci Rep 9(1):19575. https://doi.org/10.1038/s41598-019-56149-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Shen L, Liu L, Ji HF (2017) Alzheimer’s disease histological and behavioral manifestations in transgenic mice correlate with specific gut microbiome state. J Alzheimer’s Dis 56(1):385–390. https://doi.org/10.3233/jad-160884

    Article  CAS  Google Scholar 

  59. Cowan TE, Palmnäs MS, Yang J, Bomhof MR, Ardell KL, Reimer RA, Vogel HJ, Shearer J (2014) Chronic coffee consumption in the diet-induced obese rat: impact on gut microbiota and serum metabolomics. J Nutr Biochem 25(4):489–495. https://doi.org/10.1016/j.jnutbio.2013.12.009

    Article  CAS  PubMed  Google Scholar 

  60. Vogt NM, Kerby RL, Dill-McFarland KA, Harding SJ, Merluzzi AP, Johnson SC, Carlsson CM, Asthana S, Zetterberg H, Blennow K, Bendlin BB, Rey FE (2017) Gut microbiome alterations in Alzheimer’s disease. Sci Rep 7(1):13537. https://doi.org/10.1038/s41598-017-13601-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Zhuang ZQ, Shen LL, Li WW, Fu X, Zeng F, Gui L, Lü Y, Cai M, Zhu C, Tan YL, Zheng P, Li HY, Zhu J, Zhou HD, Bu XL, Wang YJ (2018) Gut microbiota is altered in patients with Alzheimer’s disease. J Alzheimer’s Dis 63(4):1337–1346. https://doi.org/10.3233/jad-180176

    Article  CAS  Google Scholar 

  62. Sun BL, Li WW, Wang J, Xu YL, Sun HL, Tian DY, Wang YJ, Yao XQ (2019) Gut microbiota alteration and its time course in a tauopathy mouse model. J Alzheimer’s Dis 70(2):399–412. https://doi.org/10.3233/jad-181220

    Article  Google Scholar 

  63. Ticinesi A, Nouvenne A, Tana C, Prati B, Meschi T (2019) Gut microbiota and microbiota-related metabolites as possible biomarkers of cognitive aging. Adv Exp Med Biol 1178:129–154. https://doi.org/10.1007/978-3-030-25650-0_8

    Article  CAS  PubMed  Google Scholar 

  64. Li Y, Ning L, Yin Y, Wang R, Zhang Z, Hao L, Wang B, Zhao X, Yang X, Yin L, Wu S, Guo D, Zhang C (2020) Age-related shifts in gut microbiota contribute to cognitive decline in aged rats. Aging (Albany NY) 12(9):7801–7817. https://doi.org/10.18632/aging.103093

    Article  CAS  Google Scholar 

  65. Bello-Medina PC, Hernández-Quiroz F, Pérez-Morales M, González-Franco DA, Cruz-Pauseno G, García-Mena J, Díaz-Cintra S, Pacheco-López G (2021) Spatial memory and gut microbiota alterations are already present in early adulthood in a pre-clinical transgenic model of Alzheimer’s disease. Front Neurosci 15:595583. https://doi.org/10.3389/fnins.2021.595583

    Article  PubMed  PubMed Central  Google Scholar 

  66. Filosa S, Di Meo F, Crispi S (2018) Polyphenols-gut microbiota interplay and brain neuromodulation. Neural Regen Res 13(12):2055–2059. https://doi.org/10.4103/1673-5374.241429

    Article  PubMed  PubMed Central  Google Scholar 

  67. Rieder R, Wisniewski PJ, Alderman BL, Campbell SC (2017) Microbes and mental health: a review. Brain Behav Immun 66:9–17. https://doi.org/10.1016/j.bbi.2017.01.016

    Article  CAS  PubMed  Google Scholar 

  68. Kao TH, Huang RFS, Chen BH (2007) Antiproliferation of hepatoma cell and progression of cell cycle as affected by isoflavone extracts from soybean cake. Int J Mol Sci 8(11):1095–1110. https://doi.org/10.3390/i8111092

    Article  CAS  PubMed Central  Google Scholar 

  69. Bensalem J, Dal-Pan A, Gillard E, Calon F, Pallet V (2015) Protective effects of berry polyphenols against age-related cognitive impairment. Nutrition and Aging 3:89–106. https://doi.org/10.3233/NUA-150051

    Article  CAS  Google Scholar 

  70. Castelli V, Grassi D, Bocale R, d’Angelo M, Antonosante A, Cimini A, Ferri C, Desideri G (2018) Diet and brain health: which role for polyphenols? Curr Pharm Des 24(2):227–238. https://doi.org/10.2174/1381612824666171213100449

    Article  CAS  PubMed  Google Scholar 

  71. Angeloni C, Vauzour D (2019) Natural products and neuroprotection. Int J Mol Sci 20(22). https://doi.org/10.3390/ijms20225570

  72. Angeloni C, Businaro R, Vauzour D (2020) The role of diet in preventing and reducing cognitive decline. Curr Opin Psychiatry 33(4):432–438. https://doi.org/10.1097/yco.0000000000000605

    Article  PubMed  Google Scholar 

  73. Youdim KA, Shukitt-Hale B, Joseph JA (2004) Flavonoids and the brain: interactions at the blood-brain barrier and their physiological effects on the central nervous system. Free Radic Biol Med 37(11):1683–1693. https://doi.org/10.1016/j.freeradbiomed.2004.08.002

    Article  CAS  PubMed  Google Scholar 

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Funding

This research was funded by grant MOST 109-2320-B-030-009 from the Ministry of Science and Technology and Taiwan, and grant TYAFGH-A-110004 from the Taoyuan Armed Forces General Hospital in Taiwan

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KCH, HLL, and TYH performed the experiments. CFH, HLL, and TYH analyzed the results and edited figures. SJW wrote preliminary draft of the manuscript. SJW and CFH designed experiments and revised the manuscript. All authors approved final version of the manuscript.

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Correspondence to Su-Jane Wang.

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Yeh, KC., Hung, CF., Lee, HL. et al. Soybean Meal Extract Preserves Memory Ability by Increasing Presynaptic Function and Modulating Gut Microbiota in Rats. Mol Neurobiol 59, 1649–1664 (2022). https://doi.org/10.1007/s12035-021-02669-3

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