Lactobacillus plantarum DP189 prevents cognitive dysfunction in D-galactose/AlCl₃ induced mouse model of Alzheimer’s disease via modulating gut microbiota and PI3K/Akt/GSK-3β signaling pathway

References

• Alzheimer Disease International. World Alzheimer report 2019: attitudes to dementia. London: Alzheimer Disease International; 2019.
   Google Scholar
• Tarawneh R, Holtzman DM. The clinical problem of symptomatic Alzheimer disease and mild cognitive impairment. Cold Spring Harb Perspect Med. 2012;2(5):1–16.
   Web of Science ®Google Scholar
• Zubenko G, Zubenko W, McPherson S, Spoor E, Marin D, Farlow M, et al. A collaborative study of the emergence and clinical features of the major depressive syndrome of Alzheimer's disease. Am J Psychiat. 2003;160(5):857–66.
   PubMed Web of Science ®Google Scholar
• Tiwari S, Atluri V, Kaushik A, Yndart A, Nair M. Alzheimer's disease: pathogenesis, diagnostics, and therapeutics. Int J Nanomedicine. 2019;14:5541–54.
   PubMed Web of Science ®Google Scholar
• Li Z, Zhu H, Zhang L, Qin C. The intestinal microbiome and Alzheimer's disease: A review. Animal Model Exp Med. 2018;1(3):180–8.
   PubMedGoogle Scholar
• Cryan JF, O'Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, et al. The microbiota-gut-brain axis. Physiol Rev. 2019;99(4):1877–2013.
   PubMed Web of Science ®Google Scholar
• Hu X, Wang T, Jin F. Alzheimer's disease and gut microbiota. Sci China Life Sci. 2016;59(10):1006–23.
   PubMed Web of Science ®Google Scholar
• Dang F, Jiang Y, Pan R, Zhou Y, Wu S, Wang R, et al. Administration of Lactobacillus paracasei ameliorates type 2 diabetes in mice. Food Funct. 2018;9(7):3630–39.
   PubMed Web of Science ®Google Scholar
• Lee E, Jung S, Lee S, Lee N, Paik H, Lim S. Lactobacillus plantarum strain Ln4 attenuates diet-induced obesity, insulin resistance, and changes in hepatic mRNA levels associated with glucose and lipid metabolism. Nutrients. 2018;10(5):1–15.
   Web of Science ®Google Scholar
• Oh N, Joung J, Lee J, Kim Y. Probiotic and anti-inflammatory potential of Lactobacillus rhamnosus 4B15 and Lactobacillus gasseri 4M13 isolated from infant feces. Plos One. 2018;13(2):1–15.
   Web of Science ®Google Scholar
• Hibberd A, Lyra A, Ouwehand AC, Rolny P, Lindegren H, Cedgård L, et al. Intestinal microbiota is altered in patients with colon cancer and modified by probiotic intervention. BMJOG. 2017;4(1):1–12.
   Web of Science ®Google Scholar
• Kukkonen K, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, et al. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol. 2007;119(1):192–8.
   PubMed Web of Science ®Google Scholar
• Shaaban SY, Gendy Y E, Mehanna NS, El-Senousy WM, El-Feki H, Saad K, et al. The role of probiotics in children with autism spectrum disorder: a prospective, open-label study. Nutr Neurosci. 2018;21(9):676–1.
   PubMed Web of Science ®Google Scholar
• Akkasheh G, Kashani-Poor Z, Tajabadi-Ebrahimi M, Jafari P, Akbari H, Taghizadeh M, et al. Clinical and metabolic response to probiotic administration in patients with major depressive disorder: a randomized, double-blind, placebo-controlled trial. Nutr. 2016;32(3):315–20.
   PubMed Web of Science ®Google Scholar
• Akbari E, Asemi Z, Daneshvar Kakhaki R, Bahmani F, Kouchaki E, Tamtaji O, et al. Effect of probiotic supplementation on cognitive function and metabolic status in Alzheimer's disease: a randomized, double-blind and controlled trial. Front Aging Neurosci. 2016;8(256):1–8.
   PubMedGoogle Scholar
• Athari Nik Azm S, Djazayeri A, Safa M, Azami K, Ahmadvand B, Sabbaghziarani F, et al. Lactobacilli and bifidobacteria ameliorate memory and learning deficits and oxidative stress in β-amyloid (1–42) injected rats. Appl Physiol Nutr Metab. 2018;43(7):718–26.
   PubMed Web of Science ®Google Scholar
• Kobayashi Y, Sugahara H, Shimada K, Mitsuyama E, Kuhara T, Yasuoka A, et al. Therapeutic potential of Bifidobacterium breve strain A1 for preventing cognitive impairment in Alzheimer's disease. Sci Rep. 2017;7(1):1–10.
   PubMedGoogle Scholar
• Sun J, Xu J, Yang B, Chen K, Kong Y, Fang N, et al. Effect of Clostridium butyricum against microglia-mediated neuroinflammation in Alzheimer's disease via regulating gut microbiota and metabolites butyrate. Mol Nutr Food Res. 2020;64(2):1–11.
   Web of Science ®Google Scholar
• Nimgampalle M, Kuna Y. Anti-Alzheimer properties of probiotic, Lactobacillus plantarum MTCC 1325 in Alzheimer’s disease induced albino rats. JCDR. 2017;11(8):KC01–KC05.
   PubMed Web of Science ®Google Scholar
• Seddik H, Bendali F, Gancel F, Fliss I, Spano G, Drider D. Lactobacillus plantarum and its probiotic and food potentialities. Probiotics & Antimicro Prot. 2017;9:111–22.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Yang G, Zhao Z, Wang C, Duan C, Gao L, et al. Antidepressant-like effects of Lactobacillus plantarum DP189 in a corticosterone-induced rat model of chronic stress. Behav Brain Res. 2020;395:112853.
   PubMed Web of Science ®Google Scholar
• Luo Y, Niu F, Sun Z, Cao W, Zhang X, Guan D, et al. Altered expression of Aβ metabolism-associated molecules from D-galactose/AlCl3 induced mouse brain. Mech Ageing Dev. 2009;130(4):248–52.
   PubMed Web of Science ®Google Scholar
• Vorhees C, Williams M. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc. 2006;1(2):848–58.
   PubMed Web of Science ®Google Scholar
• Nishino K, Nishida A, Inoue R, Kawada Y, Ohno M, Sakai S, et al. Analysis of endoscopic brush samples identified mucosa-associated dysbiosis in inflammatory bowel disease. J Gastroenterol. 2018;53(1):95–106.
   PubMed Web of Science ®Google Scholar
• Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. PNAS. 2005;102(31):11070–5.
   PubMed Web of Science ®Google Scholar
• Das T, Jayasudha R, Chakravarthy S, Prashanthi GS, Bhargava A, Tyagi M, et al. Alterations in the gut bacterial microbiome in people with type 2 diabetes mellitus and diabetic retinopathy. Sci Rep. 2021;11(2738):1–15.
   PubMedGoogle Scholar
• Iannone LF, Preda A, Blottière HM, Clarke G, Albani D, Belcastro V, et al. Microbiota-gut brain axis involvement in neuropsychiatric disorders. Expert Rev Neurother. 2019;19(10):1037–50.
   PubMed Web of Science ®Google Scholar
• Kobayashi Y, Kinoshita T, Matsumoto A, Yoshino K, Saito I, Xiao J. Bifidobacterium breve A1 supplementation improved cognitive decline in older adults with mild cognitive impairment: an open-label, single-arm study. JPAD. 2019;6(1):70–5.
   Google Scholar
• Takashima A. Amyloid-beta, tau, and dementia. J Alzheimers Dis. 2009;17(4):729–36.
   PubMed Web of Science ®Google Scholar
• Martorana A, Koch G. Is dopamine involved in Alzheimer's disease? Front Aging Neurosci. 2014;6(252):1–6.
   PubMedGoogle Scholar
• O'Mahony SM, Clarke G, Borre YE, Dinan TG, Cryan JF. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res. 2015;277:32–48.
   PubMed Web of Science ®Google Scholar
• Rodríguez JJ, Noristani HN, Verkhratsky A. The serotonergic system in ageing and Alzheimer's disease. Prog Neurobiol. 2012;99(1):15–41.
   PubMed Web of Science ®Google Scholar
• Solas M, Puerta E, Ramirez MJ. Treatment options in Alzheimeŕs disease: the GABA story. Curr Pharm Des. 2015;21(34):4960–71.
   PubMed Web of Science ®Google Scholar
• Das D, Goyal A. Antioxidant activity and γ-aminobutyric acid (GABA) producing ability of probiotic Lactobacillus plantarum DM5 isolated from Marcha of Sikkim. LWT. 2015;61(1):263–8.
   Web of Science ®Google Scholar
• Corpuz HM, Ichikawa S, Arimura M, Mihara T, Kumagai T, Mitani T, et al. Long-term diet supplementation with Lactobacillus paracasei K71 prevents age-related cognitive decline in senescence-accelerated mouse prone 8. Nutrients. 2018;10(762):1–13.
   Google Scholar
• Iqbal K, Alonso AC, Chen S, Chohan MO, El-Akkad E, Gong C, et al. Tau pathology in Alzheimer disease and other tauopathies. Biochim Biophys Acta. 2005;1739:198–210.
   PubMed Web of Science ®Google Scholar
• Hu Y, He S, Wang X, Duan Q, Grundke-Iqbal I, Iqbal K, et al. Levels of nonphosphorylated and phosphorylated tau in cerebrospinal fluid of Alzheimer's disease patients: an ultrasensitive bienzyme-substrate-recycle enzyme-linked immunosorbent assay. Am J Pathol. 2002;160(4):1269–78.
   PubMed Web of Science ®Google Scholar
• Hooper C, Killick R, Lovestone S. The GSK3 hypothesis of Alzheimer's disease. J Neurochem. 2008;104(6):1433–39.
   PubMed Web of Science ®Google Scholar
• Llorens-Martín M, Jurado J, Hernández F, Avila J. GSK-3β, a pivotal kinase in Alzheimer’s disease. Front Mol Neurosci. 2014;7(46):1–11.
   PubMedGoogle Scholar
• Lucas JJ, Hernández F, Gómez-Ramos P, Morán MA, Hen R, Avila J. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3β conditional transgenic mice. EMBO. 2001;20(1):27–39.
   PubMed Web of Science ®Google Scholar
• de Barreda E G, Pérez M, Gómez Ramos P, de Cristobal J, Martín-Maestro P, Morán A, et al. Tau-knockout mice show reduced GSK3-induced hippocampal degeneration and learning deficits. Neurobiol Dis. 2010;37(3):622–9.
   PubMed Web of Science ®Google Scholar
• Moloney AM, Griffin RJ, Timmons S, O’Connor R, Ravid R, O’Neill C. Defects in IGF-1 receptor, insulin receptor and IRS-1/2 in Alzheimer's disease indicate possible resistance to IGF-1 and insulin signalling. Neurobiol Aging. 2010;31(2):224–43.
   PubMed Web of Science ®Google Scholar
• Steen E, Terry BM, Rivera EJ, Cannon JL, Neely TR, Tavares R, et al. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease–is this type 3 diabetes? J Alzheimers Dis. 2005;7(1):63–80.
   PubMed Web of Science ®Google Scholar
• Pistollato F, Iglesias RC, Ruiz R, Aparicio S, Crespo J, Lopez L, et al. Nutritional patterns associated with the maintenance of neurocognitive functions and the risk of dementia and Alzheimer's disease: a focus on human studies. Pharmacol Res. 2018;131:32–43.
   PubMed Web of Science ®Google Scholar
• Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B, et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology. 2013;144(7):1394–401.
   PubMed Web of Science ®Google Scholar
• Yu L, Zhai Q, Tian F, Liu X, Wang G, Zhao J, et al. Potential of Lactobacillus plantarum CCFM639 in protecting against Aluminum toxicity mediated by intestinal barrier function and oxidative stress. Nutrients. 2016;8(783):1–14.
   Google Scholar
• Vogt N, Kerby R, Dill-McFarland K, Harding S, Merluzzi A, Johnson S, et al. Gut microbiome alterations in Alzheimer's disease. Sci Rep. 2017;7(1):13537.
   PubMedGoogle Scholar
• Zhang L, Wang Y, Xiayu X, Shi C, Chen W, Song N, et al. Altered gut microbiota in a mouse model of Alzheimer's disease. J Alzheimers Dis. 2017;60(4):1241–57.
   PubMed Web of Science ®Google Scholar
• Mariat D, Firmesse O, Levenez F, Guimarăes VD, Sokol H, Doré J, et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. Bmc Microbiol. 2009;9(123):1–6.
   PubMedGoogle Scholar
• Hor Y, Lew L, Jaafar MH, Lau AS, Ong J, Kato T, et al. Lactobacillus sp. improved microbiota and metabolite profiles of aging rats. Pharmacol Res. 2019;146:104312.
   PubMed Web of Science ®Google Scholar
• Williams B, Hornig M, Parekh T, Lipkin W. Application of novel PCR-based methods for detection, quantitation, and phylogenetic characterization of Sutterella species in intestinal biopsy samples from children with autism and gastrointestinal disturbances. Mbio. 2012;3(1):54–64.
   Web of Science ®Google Scholar
• Maldonado Weng J, Parikh I, Naqib A, York J, Green S, Estus S, et al. Synergistic effects of APOE and sex on the gut microbiome of young EFAD transgenic mice. Mol Neurodegener. 2019;14(47):1–9.
   PubMedGoogle Scholar
• Roubaud-Baudron C, Krolak-Salmon P, Quadrio I, Mégraud F, Salles N. Impact of chronic Helicobacter pylori infection on Alzheimer's disease: preliminary results. Neurobiol Aging. 2012;33(5):1009.e11–19.
   Web of Science ®Google Scholar
• Wang J, Ye F, Cheng X, Zhang X, Liu F, Liu G, et al. The effects of LW-AFC on intestinal microbiome in senescence-accelerated mouse prone 8 strain, a mouse model of Alzheimer's disease. J Alzheimers Dis. 2016;53(3):907–19.
   PubMed Web of Science ®Google Scholar
• Li L, Su Q, Xie B, Duan L, Zhao W, Hu D, et al. Gut microbes in correlation with mood: case study in a closed experimental human life support system. Neurogastroenterol Motil. 2016;28(8):1233–40.
   PubMed Web of Science ®Google Scholar