Dysbiosis and Alzheimer's disease: role of probiotics, prebiotics and synbiotics.
Alzheimer’s disease
Dysbiosis
Gut microbiota
Probiotics
Journal
Naunyn-Schmiedeberg's archives of pharmacology
ISSN: 1432-1912
Titre abrégé: Naunyn Schmiedebergs Arch Pharmacol
Pays: Germany
ID NLM: 0326264
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
received:
11
02
2023
accepted:
26
05
2023
medline:
23
10
2023
pubmed:
7
6
2023
entrez:
7
6
2023
Statut:
ppublish
Résumé
Alzheimer's disease (AD) is a neurodegenerative disease characterized by dementia and the accumulation of amyloid beta in the brain. Recently, microbial dysbiosis has been identified as one of the major factors involved in the onset and progression of AD. Imbalance in gut microbiota is known to affect central nervous system (CNS) functions through the gut-brain axis and involves inflammatory, immune, neuroendocrine and metabolic pathways. An altered gut microbiome is known to affect the gut and BBB permeability, resulting in imbalance in levels of neurotransmitters and neuroactive peptides/factors. Restoration of levels of beneficial microorganisms in the gut has demonstrated promising effects in AD in pre-clinical and clinical studies. The current review enlists the important beneficial microbial species present in the gut, the effect of their metabolites on CNS, mechanisms involved in dysbiosis related to AD and the beneficial effects of probiotics on AD. It also highlights challenges involved in large-scale manufacturing and quality control of probiotic formulations.
Identifiants
pubmed: 37284896
doi: 10.1007/s00210-023-02554-x
pii: 10.1007/s00210-023-02554-x
doi:
Substances chimiques
Prebiotics
0
Amyloid beta-Peptides
0
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2911-2923Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
2021 Alzheimer’s disease facts and figures (2021) Alzheimers Dement 17:327–406
doi: 10.1002/alz.12328
Aeron G, Morya S (2017) Probiotics as therapeutics. J Adv Res Biotechnol 2:1–6
doi: 10.15226/2475-4714/2/3/00127
Ahmad W, Ijaz B, Shabbiri K et al (2017) Oxidative toxicity in diabetes and Alzheimer’s disease: mechanisms behind ROS/ RNS generation. J Biomed Sci 24:1–10
doi: 10.1186/s12929-017-0379-z
Ait-Belgnaoui A, Durand H, Cartier C et al (2012) Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology 37:1885–1895
pubmed: 22541937
doi: 10.1016/j.psyneuen.2012.03.024
Altaib H, Badr Y, Suzuki T (2021) Bifidobacteria and psychobiotic therapy: current evidence and future prospects. Rev Agricult Sci 9:74–91
doi: 10.7831/ras.9.0_74
Amorim Neto DP, Bosque BP, de Pereira Godoy JV et al (2022) Akkermansia muciniphila induces mitochondrial calcium overload and α -synuclein aggregation in an enteroendocrine cell line. iScience; 25. Epub ahead of print 3 March. https://doi.org/10.1016/J.ISCI.2022.103908
Armstrong RA (2019) Risk factors for Alzheimer’s disease. Folia Neuropathol 57:87–105
doi: 10.5114/fn.2019.85929
Arora K, Green M, Prakash S (2020) The microbiome and Alzheimer’s disease: potential and limitations of prebiotic, synbiotic, and probiotic formulations. Front Bioeng Biotechnol 8:1411
doi: 10.3389/fbioe.2020.537847
Arumugam M, Raes J, Pelletier E et al (2011) Enterotypes of the human gut microbiome. Nature 473:174
pubmed: 21508958
pmcid: 3728647
doi: 10.1038/nature09944
Asaoka D, Xiao J, Takeda T et al (2022) Effect of probiotic Bifidobacterium breve in improving cognitive function and preventing brain atrophy in older patients with suspected mild cognitive impairment: results of a 24-week randomized, double-blind, placebo-controlled trial. J Alzheimers Dis 88:1–21
doi: 10.3233/JAD-220148
Azam S, Jakaria M, Kim IS et al (2019) Regulation of toll-like receptor (TLR) signaling pathway by polyphenols in the treatment of age-linked neurodegenerative diseases: focus on TLR4 signaling. Front Immunol 10:1000
pubmed: 31134076
pmcid: 6522942
doi: 10.3389/fimmu.2019.01000
Bäuerl C, Collado MC, Diaz Cuevas A et al (2018) Shifts in gut microbiota composition in an APP/PSS1 transgenic mouse model of Alzheimer’s disease during lifespan. Lett Appl Microbiol 66:464–471
pubmed: 29575030
doi: 10.1111/lam.12882
Bedu-Ferrari C, Biscarrat P, Langella P et al (2022) Prebiotics and the human gut microbiota: from breakdown mechanisms to the impact on metabolic health. Nutrients 14:2096
pubmed: 35631237
pmcid: 9147914
doi: 10.3390/nu14102096
Bello-Medina PC, Hernández-Quiroz F, Pérez-Morales M et al (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. Epub ahead of print 29 April. https://doi.org/10.3389/fnins.2021.595583
Bercik P, Denou E, Collins J et al (2011) The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology; 141. Epub ahead of print. https://doi.org/10.1053/J.GASTRO.2011.04.052
Blennow K, de Leon MJ, Zetterberg H (2006) Alzheimer’s disease. Lancet 368:387–403
pubmed: 16876668
doi: 10.1016/S0140-6736(06)69113-7
Bonfili L, Cecarini V, Gogoi O et al (2020) Gut microbiota manipulation through probiotics oral administration restores glucose homeostasis in a mouse model of Alzheimer’s disease. Neurobiol Aging 87:35–43
pubmed: 31813629
doi: 10.1016/j.neurobiolaging.2019.11.004
Bravo JA, Forsythe P, Chew MV 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 U S A 108:16050–16055
pubmed: 21876150
pmcid: 3179073
doi: 10.1073/pnas.1102999108
Bull MJ, Plummer NT (2014) Part 1: The human gut microbiome in health and disease. Integ Med: Clinician’s J 13:17
Chen Y, Xu J, Chen Y (2021) Regulation of neurotransmitters by the gut microbiota and effects on cognition in neurological disorders. Nutrients; 13. Epub ahead of print 1 June 2021. https://doi.org/10.3390/NU13062099
Coman V, Vodnar DC (2020) Gut microbiota and old age: modulating factors and interventions for healthy longevity. Exp Gerontol; 141. Epub ahead of print 1 November. https://doi.org/10.1016/J.EXGER.2020.111095
Dando SJ, Mackay-Sim A, Norton R et al (2014) Pathogens penetrating the central nervous system: infection pathways and the cellular and molecular mechanisms of invasion. Clin Microbiol Rev 27:691–726
pubmed: 25278572
pmcid: 4187632
doi: 10.1128/CMR.00118-13
Davani-Davari D, Negahdaripour M, Karimzadeh I, et al. (2019) Prebiotics: definition, types, sources, mechanisms, and clinical applications. Foods; 8. Epub ahead of print 1 March 2019. https://doi.org/10.3390/FOODS8030092
Dementia statistics | Alzheimer’s Disease International (ADI), https://www.alzint.org/about/dementia-facts-figures/dementia-statistics/
Deng H, Dong X, Chen M et al (2020) Efficacy of probiotics on cognition, and biomarkers of inflammation and oxidative stress in adults with Alzheimer’s disease or mild cognitive impairment — a meta-analysis of randomized controlled trials. Aging (Albany NY) 12:4010
Du X, Wang X, Geng M (2018) Alzheimer’s disease hypothesis and related therapies. Transl Neurodegener; 7. Epub ahead of print 30 January. https://doi.org/10.1186/S40035-018-0107-Y
Durack J, Lynch SV (2019) The gut microbiome: relationships with disease and opportunities for therapy. J Exp Med 216:20
pubmed: 30322864
pmcid: 6314516
doi: 10.1084/jem.20180448
Feigin VL, Nichols E, Alam T et al (2019) Global, regional, and national burden of neurological disorders, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 18:459
doi: 10.1016/S1474-4422(18)30499-X
Ferro A, Auguste YSS, Cheadle L (2021) Microglia, cytokines, and neural activity: unexpected interactions in brain development and function. Front Immunol 12:2546
doi: 10.3389/fimmu.2021.703527
Galland L (2014) The gut microbiome and the brain. J Med Food 17:1261
pubmed: 25402818
pmcid: 4259177
doi: 10.1089/jmf.2014.7000
Geng S, Yang L, Cheng F et al (2020) Gut microbiota are associated with psychological stress-induced defections in intestinal and blood–brain barriers. Front Microbiol 10:3067
pubmed: 32010111
pmcid: 6974438
doi: 10.3389/fmicb.2019.03067
Gomaa EZ (2020) Human gut microbiota/microbiome in health and diseases: a review. Antonie Van Leeuwenhoek 113:2019–2040
pubmed: 33136284
doi: 10.1007/s10482-020-01474-7
Guerreiro CS, Calado Â, Sousa J et al (2018) Diet, microbiota, and gut permeability-the unknown triad in rheumatoid arthritis. Front Med (Lausanne) 5:349
pubmed: 30619860
doi: 10.3389/fmed.2018.00349
Guinane CM, Cotter PD (2013) Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Ther Adv Gastroenterol 6:295
doi: 10.1177/1756283X13482996
Gupta V, Garg R (2009) Probiotics. Indian J Med Microbiol 27:202–209
pubmed: 19584499
doi: 10.4103/0255-0857.53201
Hakansson A, Molin G (2011) Gut microbiota and inflammation. Nutrients 3:637
pubmed: 22254115
pmcid: 3257638
doi: 10.3390/nu3060637
Hasan N, Yang H (2019) Factors affecting the composition of the gut microbiota, and its modulation. Peer J; 7. Epub ahead of print. https://doi.org/10.7717/PEERJ.7502
Hassel B, Dahlberg D, Mariussen E et al (2014) Brain infection with Staphylococcus aureus leads to high extracellular levels of glutamate, aspartate, γ-aminobutyric acid, and zinc. J Neurosci Res 92:1792–1800
pubmed: 25043715
doi: 10.1002/jnr.23444
Ho L, Ono K, Tsuji M et al (2018) Protective roles of intestinal microbiota derived short chain fatty acids in Alzheimer’s disease-type beta-amyloid neuropathological mechanisms. Expert Rev Neurother 18:83–90
pubmed: 29095058
doi: 10.1080/14737175.2018.1400909
Holzer P, Farzi A (2014) Neuropeptides and the microbiota-gut-brain axis. Adv Exp Med Biol 817:196–219
Houser MC, Tansey MG (2017) The gut-brain axis: is intestinal inflammation a silent driver of Parkinson’s disease pathogenesis? npj Parkinson’s Disease 3:1 2017; 3: 1–9
Islam SU (2016) Clinical uses of probiotics. Medicine 95:e2658
pubmed: 26844491
pmcid: 4748908
doi: 10.1097/MD.0000000000002658
Jiang C, Li G, Huang P et al (2017) The gut microbiota and Alzheimer’s disease. J Alzheimers Dis 58:1–15
pubmed: 28372330
doi: 10.3233/JAD-161141
Kar F, Hacioglu C, Kar E et al (2022) Probiotics ameliorates LPS induced neuroinflammation injury on Aβ 1-42, APP, γ-β secretase and BDNF levels in maternal gut microbiota and fetal neurodevelopment processes. Metab Brain Dis. Epub ahead of print. https://doi.org/10.1007/S11011-022-00964-Z
Kaur H, Bose C, Mande SS (2019) Tryptophan metabolism by gut microbiome and gut-brain-axis: an in silico analysis. Front Neurosci 13:1365
pubmed: 31920519
pmcid: 6930238
doi: 10.3389/fnins.2019.01365
Kaur H, Nagamoto-Combs K, Golovko S et al (2020) Probiotics ameliorate intestinal pathophysiology in a mouse model of Alzheimer’s disease. Neurobiol Aging 92:114–134
pubmed: 32417748
pmcid: 7269849
doi: 10.1016/j.neurobiolaging.2020.04.009
Kelly JR, Kennedy PJ, Cryan JF et al (2015) Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders. Front Cell Neurosci 9:392
pubmed: 26528128
pmcid: 4604320
doi: 10.3389/fncel.2015.00392
Khalifeh M, Read MI, Barreto GE et al (2020) Trehalose against Alzheimer’s disease: insights into a potential therapy. Bioessays; 42. Epub ahead of print 1 August. https://doi.org/10.1002/BIES.201900195
Kho ZY, Lal SK (2018) The human gut microbiome - a potential controller of wellness and disease. Front Microbiol 9:1835
pubmed: 30154767
pmcid: 6102370
doi: 10.3389/fmicb.2018.01835
Kim CS, Cha L, Sim M et al (2021b) Probiotic supplementation improves cognitive function and mood with changes in gut microbiota in community-dwelling older adults: a randomized, double-blind, placebo-controlled, multicenter trial. J Gerontol A Biol Sci Med Sci 76:32–40
pubmed: 32300799
doi: 10.1093/gerona/glaa090
Kim H, Kim S, Park SJ et al (2021a) Administration of Bifidobacterium bifidum BGN4 and Bifidobacterium longum BORI improves cognitive and memory function in the mouse model of Alzheimer’s disease. Front Aging Neurosci; 13. Epub ahead of print 6 August. https://doi.org/10.3389/FNAGI.2021.709091
Kim MS, Kim Y, Choi H et al (2020) Transfer of a healthy microbiota reduces amyloid and tau pathology in an Alzheimer’s disease animal model. Gut 69:283–294
pubmed: 31471351
doi: 10.1136/gutjnl-2018-317431
Kobayashi Y, Kinoshita T, Matsumoto A et al (2019b) Bifidobacterium Breve A1 supplementation improved cognitive decline in older adults with mild cognitive impairment: an open-label, single-arm study. J Prev Alzheimers Dis 6:70–75
pubmed: 30569089
Kobayashi Y, Kuhara T, Oki M et al (2019a) Effects of Bifidobacterium breve A1 on the cognitive function of older adults with memory complaints: a randomised, double-blind, placebo-controlled trial. Benefic Microbes 10:511–520
doi: 10.3920/BM2018.0170
Kobayashi Y, Sugahara H, Shimada K et al (2017) Therapeutic potential of Bifidobacterium breve strain A1 for preventing cognitive impairment in Alzheimer’s disease. Scientific Reports; 7: 1–10
Krüger JF, Hillesheim E, Pereira ACSN et al (2021) Probiotics for dementia: a systematic review and meta-analysis of randomized controlled trials. Nutr Rev 79:160–170
pubmed: 32556236
doi: 10.1093/nutrit/nuaa037
Lee DY, Shin YJ, Kim JK et al (2021) Alleviation of cognitive impairment by gut microbiota lipopolysaccharide production-suppressing Lactobacillus plantarum and Bifidobacterium longum in mice. Food Funct 12:10750–10763
pubmed: 34608923
doi: 10.1039/D1FO02167B
Li Z, Zhu H, Guo Y et al (2020) Gut microbiota regulate cognitive deficits and amyloid deposition in a model of Alzheimer’s disease. J Neurochem 155:448–461
pubmed: 32319677
doi: 10.1111/jnc.15031
Limon A, Reyes-Ruiz JM, Miledi R (2012) Loss of functional GABA A receptors in the Alzheimer diseased brain. Proc Natl Acad Sci U S A 109:10071–10076
pubmed: 22691495
pmcid: 3382476
doi: 10.1073/pnas.1204606109
Liu J, Chang L, Song Y et al (2019) The role of NMDA receptors in Alzheimer’s disease. Front Neurosci 13:43
pubmed: 30800052
pmcid: 6375899
doi: 10.3389/fnins.2019.00043
Liu S, Gao J, Zhu M et al (2020) Gut microbiota and dysbiosis in Alzheimer’s disease: implications for pathogenesis and treatment. Mol Neurobiol 57:5026
pubmed: 32829453
pmcid: 7541367
doi: 10.1007/s12035-020-02073-3
Lupien SJ, McEwen BS, Gunnar MR et al (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445
pubmed: 19401723
doi: 10.1038/nrn2639
Madison A, Kiecolt-Glaser JK (2019) Stress, depression, diet, and the gut microbiota: human–bacteria interactions at the core of psychoneuroimmunology and nutrition. Curr Opin Behav Sci 28:105
pubmed: 32395568
pmcid: 7213601
doi: 10.1016/j.cobeha.2019.01.011
Marizzoni M, Cattaneo A, Mirabelli P et al (2020) Short-chain fatty acids and lipopolysaccharide as mediators between gut dysbiosis and amyloid pathology in Alzheimer’s disease. J Alzheimers Dis 78:683–697
pubmed: 33074224
doi: 10.3233/JAD-200306
Markowiak-Kopeć P, Śliżewska K (2020) The effect of probiotics on the production of short-chain fatty acids by human intestinal microbiome. Nutrients; 12. Epub ahead of print 1 April. https://doi.org/10.3390/NU12041107
Mazzoli R, Pessione E (2016) The neuro-endocrinological role of microbial glutamate and GABA signaling. Front Microbiol; 7. Epub ahead of print 30 November 2016. https://doi.org/10.3389/FMICB.2016.01934
McGeer PL, McGeer EG (2002) Local neuroinflammation and the progression of Alzheimer’s disease. J NeuroVirolog 8:529–538
doi: 10.1080/13550280290100969
Miranda M, Morici JF, Zanoni MB et al (2019) Brain-derived neurotrophic factor: a key molecule for memory in the healthy and the pathological brain. Front Cell Neurosci 13:363
pubmed: 31440144
pmcid: 6692714
doi: 10.3389/fncel.2019.00363
Misiak B, Łoniewski I, Marlicz W et al (2020) The HPA axis dysregulation in severe mental illness: can we shift the blame to gut microbiota? Prog Neuro-Psychopharmacol Biol Psychiatry 102:109951
doi: 10.1016/j.pnpbp.2020.109951
Morais LH, Schreiber HL, Mazmanian SK (2020) The gut microbiota–brain axis in behaviour and brain disorders. Nat Rev Microbiol 19:241–255
pubmed: 33093662
doi: 10.1038/s41579-020-00460-0
Morgan MJ, Liu ZG (2011) Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res 21:103
pubmed: 21187859
doi: 10.1038/cr.2010.178
Mufson EJ, Counts SE, Perez SE et al (2014) Cholinergic system during the progression of Alzheimer’s disease: therapeutic implications 8: 1703–1718. https://doi.org/10.1586/147371758111703
Naomi R, Embong H, Othman F et al (2021) Probiotics for Alzheimer’s disease: a systematic review. Nutrients; 14. Epub ahead of print 1 January. https://doi.org/10.3390/NU14010020
Ng TKS, Ho CSH, Tam WWS et al (2019) Decreased serum brain-derived neurotrophic factor (BDNF) levels in patients with Alzheimer’s disease (AD): a systematic review and meta-analysis. Int J Mol Sci; 20. Epub ahead of print. https://doi.org/10.3390/IJMS20020257
Nishimori JH, Newman TN, Oppong GO et al (2012) Microbial amyloids induce interleukin 17A (IL-17A) and IL-22 responses via toll-like receptor 2 activation in the intestinal mucosa. Infect Immun 80:4398
pubmed: 23027540
pmcid: 3497426
doi: 10.1128/IAI.00911-12
Ohsawa K, Nakamura F, Uchida N et al (2018) Lactobacillus helveticus-fermented milk containing lactononadecapeptide (NIPPLTQTPVVVPPFLQPE) improves cognitive function in healthy middle-aged adults: a randomised, double-blind, placebo-controlled trial. Int J Food Sci Nutr 69:369–376
pubmed: 28819993
doi: 10.1080/09637486.2017.1365824
Padgett LE, Broniowska KA, Hansen PA et al (2013) The role of reactive oxygen species and proinflammatory cytokines in type 1 diabetes pathogenesis. Ann N Y Acad Sci 1281:16
pubmed: 23323860
pmcid: 3715103
doi: 10.1111/j.1749-6632.2012.06826.x
Papadopoulos G, Weinberg EO, Massari P et al (2013) Macrophage-specific TLR2 signaling mediates pathogen-induced TNF-dependent inflammatory oral bone loss. J Immunol Auth Choi 190:1148
doi: 10.4049/jimmunol.1202511
Park SJ, Kim DH, Kang HJ et al. (2021) Enhanced production of γ-aminobutyric acid (GABA) using Lactobacillus plantarum EJ2014 with simple medium composition. LWT; 137. Epub ahead of print 1 February 2021. https://doi.org/10.1016/J.LWT.2020.110443
Picciotto MR, Higley MJ, Mineur YS (2012) Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior. Neuron 76:116
pubmed: 23040810
pmcid: 3466476
doi: 10.1016/j.neuron.2012.08.036
Quigley EMM (2017) Microbiota-brain-gut axis and neurodegenerative diseases. Curr Neurol Neurosci Rep; 17. Epub ahead of print 1 December. https://doi.org/10.1007/S11910-017-0802-6
Quigley EMM (2019) Prebiotics and probiotics in digestive health. Clin Gastroenterol Hepatol 17:333–344
pubmed: 30267869
doi: 10.1016/j.cgh.2018.09.028
Rai SN, Tiwari N, Singh P et al (2021) Therapeutic potential of vital transcription factors in Alzheimer’s and Parkinson’s disease with particular emphasis on transcription factor EB mediated autophagy. Front Neurosci 15:1703
doi: 10.3389/fnins.2021.777347
Rinninella E, Raoul P, Cintoni M et al (2019) What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms 7:14
pubmed: 30634578
pmcid: 6351938
doi: 10.3390/microorganisms7010014
Rodríguez JJ, Olabarria M, Chvatal A et al (2009) Astroglia in dementia and Alzheimer’s disease. Cell Death & Differentiation 16:3 2008; 16: 378–385
Ronald de Kloet E, Schmidt M, Meijer OC (2005) Corticosteroid receptors and HPA-axis regulation. Techniq Behav Neural Sci 15:265–294
doi: 10.1016/S0921-0709(05)80016-1
Ruiz L, Delgado S, Ruas-Madiedo P et al (2017) Bifidobacteria and their molecular communication with the immune system. Front Microbiol 8:2345
pubmed: 29255450
pmcid: 5722804
doi: 10.3389/fmicb.2017.02345
Russell WR, Hoyles L, Flint HJ et al (2013) Colonic bacterial metabolites and human health. Curr Opin Microbiol 16:246–254
pubmed: 23880135
doi: 10.1016/j.mib.2013.07.002
Rutsch A, Kantsjö JB, Ronchi F (2020) The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology. Front Immunol 11:3237
doi: 10.3389/fimmu.2020.604179
Saeedi M, Rashidy-Pour A (2021) Association between chronic stress and Alzheimer’s disease: therapeutic effects of Saffron. Biomed Pharmacother 133:110995
pubmed: 33232931
doi: 10.1016/j.biopha.2020.110995
Saify ZS, Sultana N (2014) Role of acetylcholinesterase inhibitors and Alzheimer disease. Drug Design Discov Alzheimer’s Dis:387–425
Salleh RM, Kuan G, Aziz MNA et al (2021) Effects of probiotics on anxiety, stress, mood and fitness of badminton players. Nutrients; 13. Epub ahead of print 1 June. https://doi.org/10.3390/NU13061783
Savignac HM, Corona G, Mills H et al (2013) Prebiotic feeding elevates central brain derived neurotrophic factor, N-methyl-d-aspartate receptor subunits and d-serine. Neurochem Int 63:756
pubmed: 24140431
pmcid: 3858812
doi: 10.1016/j.neuint.2013.10.006
Saxelin M (2008) Probiotic formulations and applications, the current probiotics market, and changes in the marketplace: a European perspective. Clin Infect Dis; 46 Suppl 2. Epub ahead of print 1 February. https://doi.org/10.1086/523337
Schindowski K, Belarbi K, Buée L (2008) Neurotrophic factors in Alzheimer’s disease: role of axonal transport. Genes Brain Behav 7:43
pubmed: 18184369
doi: 10.1111/j.1601-183X.2007.00378.x
Shamsipour S, Sharifi G, Taghian F (2021) Impact of interval training with probiotic (L. plantarum / Bifidobacterium bifidum) on passive avoidance test, ChAT and BDNF in the hippocampus of rats with Alzheimer’s disease. Neurosci Lett; 756. Epub ahead of print 21 June. https://doi.org/10.1016/J.NEULET.2021.135949
Sheffler ZM, Reddy V, Pillarisetty LS (2022) Physiology, neurotransmitters. StatPearls, https://www.ncbi.nlm.nih.gov/books/NBK539894/ (2022, accessed 15 July 2022)
Shen L, Ji HF (2019) Associations between gut microbiota and Alzheimer’s disease: current evidences and future therapeutic and diagnostic perspectives. J Alzheimers Dis 68:25–31
pubmed: 30814354
doi: 10.3233/JAD-181143
Sheng JA, Bales NJ, Myers SA et al (2021) The hypothalamic-pituitary-adrenal axis: development, programming actions of hormones, and maternal-fetal interactions. Front Behav Neurosci 14:256
doi: 10.3389/fnbeh.2020.601939
Silva YP, Bernardi A, Frozza RL (2020) The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front Endocrinol (Lausanne) 11:25
pubmed: 32082260
doi: 10.3389/fendo.2020.00025
Singh AK, Rai SN, Maurya A, et al (2021a) Therapeutic potential of phytoconstituents in management of Alzheimer’s disease. Evidence-based Complementary and Alternative Medicine; 2021. Epub ahead of print. https://doi.org/10.1155/2021/5578574
Singh AK, Sen SS, Rathore AS et al (2021b) Lipid-coated MCM-41 mesoporous silica nanoparticles loaded with berberine improved inhibition of acetylcholine esterase and amyloid formation. ACS Biomater Sci Eng 7:3737–3753
pubmed: 34297529
doi: 10.1021/acsbiomaterials.1c00514
Stephens MAC, Wand G (2012) Stress and the HPA axis: role of glucocorticoids in alcohol dependence. Alcohol Res 34:468
pubmed: 23584113
pmcid: 3860380
Stoeva MK, Garcia-So J, Justice N et al (2021) Butyrate-producing human gut symbiont, Clostridium butyricum, and its role in health and disease. Gut Microbes 13:1–28
pubmed: 33874858
doi: 10.1080/19490976.2021.1907272
Sultana R, Butterfield DA (2010) Role of oxidative stress in the progression of Alzheimer’s disease. J Alzheimers Dis 19:341–353
pubmed: 20061649
doi: 10.3233/JAD-2010-1222
Sun J, Xu J, Ling Y, et al (2019) Fecal microbiota transplantation alleviated Alzheimer’s disease-like pathogenesis in APP/PS1 transgenic mice. Translational Psychiatry 9:1 2019; 9: 1–13
Sun J, Xu J, Yang B, et al (2020) Effect of Clostridium butyricum against microglia-mediated neuroinflammation in Alzheimer’s disease via regulating gut microbiota and metabolites butyrate. Mol Nutr Food Res; 64. Epub ahead of print 1 January. https://doi.org/10.1002/MNFR.201900636
Tamtaji OR, Heidari-soureshjani R, Mirhosseini N et al (2019) Probiotic and selenium co-supplementation, and the effects on clinical, metabolic and genetic status in Alzheimer’s disease: a randomized, double-blind, controlled trial. Clin Nutr 38:2569–2575
pubmed: 30642737
doi: 10.1016/j.clnu.2018.11.034
Tarawneh R, Penhos E (2022) The gut microbiome and Alzheimer’s disease: complex and bidirectional interactions. Neurosci Biobehav Rev 141:104814
pubmed: 35934087
pmcid: 9637435
doi: 10.1016/j.neubiorev.2022.104814
Thursby E, Juge N (2017) Introduction to the human gut microbiota. Biochem J 474:1823
pubmed: 28512250
doi: 10.1042/BCJ20160510
Ton AMM, Campagnaro BP, Alves GA, et al (2020) Oxidative stress and dementia in Alzheimer’s patients: effects of synbiotic supplementation. Oxid Med Cell Longev. Epub ahead of print 2020. https://doi.org/10.1155/2020/2638703
Tyszkowski R, Mehrzad R (2023) Inflammation: a multifaceted and omnipresent phenomenon. Inflammation and Obesity: A New and Novel Approach to Manage Obesity and its Consequences; 19–30
Umeno A, Biju V, Yoshida Y (2017) In vivo ROS production and use of oxidative stress-derived biomarkers to detect the onset of diseases such as Alzheimer’s disease, Parkinson’s disease, and diabetes. Free Radic Res 51:413–427. https://doi.org/10.1080/1071576220171315114
doi: 10.1080/1071576220171315114
pubmed: 28372523
Vagnerová K, Vodička M, Hermanová P et al (2019) Interactions between gut microbiota and acute restraint stress in peripheral structures of the hypothalamic–pituitary–adrenal axis and the intestine of male mice. Front Immunol 10:2655
pubmed: 31798585
pmcid: 6878942
doi: 10.3389/fimmu.2019.02655
Varatharaj A, Galea I (2017) The blood-brain barrier in systemic inflammation. Brain Behav Immun 60:1–12
pubmed: 26995317
doi: 10.1016/j.bbi.2016.03.010
Wang H, Lee IS, Braun C et al (2016) Effect of probiotics on central nervous system functions in animals and humans: a systematic review. J Neurogastroenterol Motil 22:589
pubmed: 27413138
pmcid: 5056568
doi: 10.5056/jnm16018
Wang R, Reddy PH (2017) Role of glutamate and NMDA receptors in Alzheimer’s disease. J Alzheimers Dis 57:1041
pubmed: 27662322
pmcid: 5791143
doi: 10.3233/JAD-160763
Wang WY, Tan MS, Yu JT et al (2015) Role of pro-inflammatory cytokines released from microglia in Alzheimer’s disease. Ann Transl Med 3:136
pubmed: 26207229
pmcid: 4486922
Wang X, Zhang P, Zhang X (2021) Probiotics regulate gut microbiota: an effective method to improve immunity. Molecules; 26. Epub ahead of print 1 October . https://doi.org/10.3390/MOLECULES26196076
Wieërs G, Belkhir L, Enaud R et al (2019) How probiotics affect the microbiota. Front Cell Infect Microbiol 9:454
pubmed: 32010640
doi: 10.3389/fcimb.2019.00454
Won E, Kim Y-K (2016) Stress, the autonomic nervous system, and the immune-kynurenine pathway in the etiology of depression. Curr Neuropharmacol 14:665
pubmed: 27640517
pmcid: 5050399
doi: 10.2174/1570159X14666151208113006
Xiao J, Katsumata N, Bernier F et al (2020) Probiotic Bifidobacterium breve in improving cognitive functions of older adults with suspected mild cognitive impairment: a randomized, double-blind, placebo-controlled trial. J Alzheimers Dis 77:139
pubmed: 32623402
pmcid: 7592675
doi: 10.3233/JAD-200488
Xu Q, Wen L, Wei G, et al (2022) Marked response of rat ileal and colonic microbiota after the establishment of Alzheimer’s disease model with bilateral intraventricular injection of Aβ (1-42). Front Microbiol; 13. Epub ahead of print 11 February. https://doi.org/10.3389/FMICB.2022.819523
Yaghoubfar R, Behrouzi A, Ashrafian F, et al (2020) Modulation of serotonin signaling/metabolism by Akkermansia muciniphila and its extracellular vesicles through the gut-brain axis in mice. Scientific Reports 10:1 2020; 10: 1–12
Zecca C, Pasculli G, Tortelli R et al (2021) The role of age on beta-amyloid1–42 plasma levels in healthy subjects. Front Aging Neurosci 13:563
doi: 10.3389/fnagi.2021.698571
Zhai S, Zhu L, Qin S, et al (2018) Effect of lactulose intervention on gut microbiota and short chain fatty acid composition of C57BL/6J mice. Microbiologyopen; 7. Epub ahead of print 1 December. https://doi.org/10.1002/MBO3.612
Zhang N, Zhang Y, Li M, et al (2020) Efficacy of probiotics on stress in healthy volunteers: a systematic review and meta-analysis based on randomized controlled trials. Brain Behav; 10. Epub ahead of print 1 September. https://doi.org/10.1002/BRB3.1699
Zhao Y, Dua P, Lukiw WJ (2015) Microbial sources of amyloid and relevance to amyloidogenesis and Alzheimer’s disease (AD). J Alzheimers Dis Parkinsonism 5:177
pubmed: 25977840
pmcid: 4428612
Zhou Y, Wang Y, Quan M et al (2021) Gut microbiota changes and their correlation with cognitive and neuropsychiatric symptoms in Alzheimer’s disease. J Alzheimers Dis 81:583–595
pubmed: 33814442
doi: 10.3233/JAD-201497
Zhu G, Zhao J, Zhang H, et al. (2021) Administration of Bifidobacterium breve improves the brain function of Aβ 1-42-treated mice via the modulation of the gut microbiome. Nutrients; 13. Epub ahead of print 1 May 2021. https://doi.org/10.3390/NU13051602
Zhu X, Han Y, Du J et al (2017) Microbiota-gut-brain axis and the central nervous system. Oncotarget 8:53829
pubmed: 28881854
pmcid: 5581153
doi: 10.18632/oncotarget.17754