Generic placeholder image

CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Review Article

Direct Modulation of the Gut Microbiota as a Therapeutic Approach for Alzheimer’s Disease

Author(s): Yi Wang* and Gary A. Dykes

Volume 21, Issue 1, 2022

Published on: 06 August, 2021

Page: [14 - 25] Pages: 12

DOI: 10.2174/1871527320666210806165751

Price: $65

Abstract

Alzheimer’s disease is a neurodegenerative disease characterized by a progressive decline in memory and cognitive functions. It is a multifactorial disease involving a wide range of pathological factors that are not fully understood. As supported by a growing amount of evidence in recent years, gut microbiota plays an important role in the pathogenesis of Alzheimer’s disease through the brain-gut-microbiota axis. This suggests that direct modulation of the gut microbiota can be a potential therapeutic target for Alzheimer’s disease. This review summarizes recent research findings on the modulation of the gut microbiota by probiotic therapies and faecal microbiota transplantation for controlling the pathologies of Alzheimer’s disease. Current limitations and future research directions of this field are also discussed.

Keywords: Alzheimer’s disease, gut microbiota, probiotics, faecal microbiota transplantation, beta-amyloid, central nervous system.

Graphical Abstract

[1]
Reitz C, Mayeux R. Alzheimer disease: epidemiology, diagnostic criteria, risk factors and biomarkers. Biochem Pharmacol 2014; 88(4): 640-51.
[http://dx.doi.org/10.1016/j.bcp.2013.12.024] [PMID: 24398425]
[2]
Nagpal R, Neth BJ, Wang S, Craft S, Yadav H. Modified Mediterranean-ketogenic diet modulates gut microbiome and short-chain fatty acids in association with Alzheimer’s disease markers in subjects with mild cognitive impairment. EBioMedicine 2019; 47: 529-42.
[http://dx.doi.org/10.1016/j.ebiom.2019.08.032] [PMID: 31477562]
[3]
Pluta R, Ułamek-Kozioł M, Januszewski S, Czuczwar SJ. Gut microbiota and pro/prebiotics in Alzheimer’s disease. Aging (Albany NY) 2020; 12(6): 5539-50.
[http://dx.doi.org/10.18632/aging.102930] [PMID: 32191919]
[4]
Köhler CA, Maes M, Slyepchenko A, et al. The gut-brain axis, including the microbiome, leaky gut and bacterial translocation: mechanisms and pathophysiological role in Alzheimer’s disease. Curr Pharm Des 2016; 22(40): 6152-66.
[http://dx.doi.org/10.2174/1381612822666160907093807] [PMID: 27604604]
[5]
Lee C D, Daggett A, Gu X, et al. Elevated TREM2 gene dosage reprograms microglia responsivity and ameliorates pathological phenotypes in Alzheimer’s disease models. Neuron 2018; 97(5): 1032-48.
[http://dx.doi.org/10.1016/j.neuron.2018.02.002]
[6]
Kowalski K, Mulak A. Brain-gut-microbiota axis in Alzheimer’s disease. J Neurogastroenterol Motil 2019; 25(1): 48-60.
[http://dx.doi.org/10.5056/jnm18087] [PMID: 30646475]
[7]
Sochocka M, Donskow-Łysoniewska K, Diniz BS, Kurpas D, Brzozowska E, Leszek J. The gut microbiome alterations and inflammation-driven pathogenesis of Alzheimer’s disease-a critical review. Mol Neurobiol 2019; 56(3): 1841-51.
[http://dx.doi.org/10.1007/s12035-018-1188-4] [PMID: 29936690]
[8]
Asti A, Gioglio L. Can a bacterial endotoxin be a key factor in the kinetics of amyloid fibril formation? J Alzheimers Dis 2014; 39(1): 169-79.
[http://dx.doi.org/10.3233/JAD-131394] [PMID: 24150108]
[9]
Bostanciklioğlu M. The role of gut microbiota in pathogenesis of Alzheimer’s disease. J Appl Microbiol 2019; 127(4): 954-67.
[http://dx.doi.org/10.1111/jam.14264] [PMID: 30920075]
[10]
Johnson KV-A, Foster KR. Why does the microbiome affect behaviour? Nat Rev Microbiol 2018; 16(10): 647-55.
[http://dx.doi.org/10.1038/s41579-018-0014-3] [PMID: 29691482]
[11]
Chen SG, Stribinskis V, Rane MJ, et al. Exposure to the functional bacterial amyloid protein curli enhances alpha-synuclein aggregation in aged Fischer 344 rats and Caenorhabditis elegans. Sci Rep 2016; 6(1): 34477.
[http://dx.doi.org/10.1038/srep34477] [PMID: 27708338]
[12]
Bhandage AK, Jin Z, Korol SV, et al. GABA regulates release of inflammatory cytokines from peripheral blood mononuclear cells and CD4+ T cells and is immunosuppressive in type 1 diabetes. EBioMedicine 2018; 30: 283-94.
[http://dx.doi.org/10.1016/j.ebiom.2018.03.019] [PMID: 29627388]
[13]
Del Rio D, Zimetti F, Caffarra P, et al. The gut microbial metabolite trimethylamine-N-oxide is present in human cerebrospinal fluid. Nutrients 2017; 9(10): 1053.
[http://dx.doi.org/10.3390/nu9101053] [PMID: 28937600]
[14]
Ledo JH, Azevedo EP, Beckman D, et al. Cross talk between brain innate immunity and serotonin signaling underlies depressive-like behavior induced by Alzheimer’s amyloid-β oligomers in mice. J Neurosci 2016; 36(48): 12106-16.
[http://dx.doi.org/10.1523/JNEUROSCI.1269-16.2016] [PMID: 27903721]
[15]
Nelson PT, Braak H, Markesbery WR. Neuropathology and cognitive impairment in Alzheimer disease: a complex but coherent relationship. J Neuropathol Exp Neurol 2009; 68(1): 1-14.
[http://dx.doi.org/10.1097/NEN.0b013e3181919a48] [PMID: 19104448]
[16]
Ho L, Ono K, Tsuji M, Mazzola P, Singh R, Pasinetti GM. Protective roles of intestinal microbiota derived short chain fatty acids in Alzheimer’s disease-type beta-amyloid neuropathological mechanisms. Expert Rev Neurother 2018; 18(1): 83-90.
[http://dx.doi.org/10.1080/14737175.2018.1400909] [PMID: 29095058]
[17]
Venegas DP, Marjorie K, Landskron G, et al. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol 2019; 10.
[18]
Erny D, Hrabě de Angelis AL, Jaitin D, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 2015; 18(7): 965-77.
[http://dx.doi.org/10.1038/nn.4030] [PMID: 26030851]
[19]
Caballero-Villarraso J, Galvan A, Escribano B M, Tunez I. Interrelationships among gut microbiota and host: paradigms, role in neurodegenerative diseases and future prospects. CNS & neurological disorders-drug targets (formerly current drug targets-CNS & neurological disorders) 2017; 16(8): 945-64.
[20]
Vendrik KEW, Ooijevaar RE, de Jong PRC, et al. Fecal microbiota transplantation in neurological disorders. Front Cell Infect Microbiol 2020; 10: 98.
[http://dx.doi.org/10.3389/fcimb.2020.00098] [PMID: 32266160]
[21]
Ozawa M, Ohara T, Ninomiya T, et al. Milk and dairy consumption and risk of dementia in an elderly Japanese population: the Hisayama Study. J Am Geriatr Soc 2014; 62(7): 1224-30.
[http://dx.doi.org/10.1111/jgs.12887] [PMID: 24916840]
[22]
Rahman A, Sawyer Baker P, Allman RM, Zamrini E. Dietary factors and cognitive impairment in community-dwelling elderly. J Nutr Health Aging 2007; 11(1): 49-54.
[PMID: 17315080]
[23]
Akbari E, Asemi Z, Daneshvar Kakhaki R, 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.
[http://dx.doi.org/10.3389/fnagi.2016.00256] [PMID: 27891089]
[24]
Yang X, Yu D, Xue L, Li H, Du J. Probiotics modulate the microbiota-gut-brain axis and improve memory deficits in aged SAMP8 mice. Acta Pharm Sin B 2020; 10(3): 475-87.
[http://dx.doi.org/10.1016/j.apsb.2019.07.001] [PMID: 32140393]
[25]
Wang Q-J, Shen Y-E, Wang X, et al. Concomitant memantine and Lactobacillus plantarum treatment attenuates cognitive impairments in APP/PS1 mice. Aging (Albany NY) 2020; 12(1): 628-49.
[http://dx.doi.org/10.18632/aging.102645] [PMID: 31907339]
[26]
Li H, Sun J, Du J, et al. Clostridium butyricum exerts a neuroprotective effect in a mouse model of traumatic brain injury via the gut-brain axis. Neurogastroenterol Motil 2018; 30(5): e13260.
[http://dx.doi.org/10.1111/nmo.13260] [PMID: 29193450]
[27]
Athari Nik Azm S, Djazayeri A, Safa M, 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.
[http://dx.doi.org/10.1139/apnm-2017-0648] [PMID: 29462572]
[28]
Wang I-K, Wu Y-Y, Yang Y-F, et al. The effect of probiotics on serum levels of cytokine and endotoxin in peritoneal dialysis patients: a randomised, double-blind, placebo-controlled trial. Benef Microbes 2015; 6(4): 423-30.
[http://dx.doi.org/10.3920/BM2014.0088] [PMID: 25609654]
[29]
Bonfili L, Cecarini V, Berardi S, et al. Microbiota modulation counteracts Alzheimer’s disease progression influencing neuronal proteolysis and gut hormones plasma levels. Sci Rep 2017; 7(1): 2426.
[http://dx.doi.org/10.1038/s41598-017-02587-2] [PMID: 28546539]
[30]
Musa NH, Mani V, Lim SM, Vidyadaran S, Abdul Majeed AB, Ramasamy K. Lactobacilli-fermented cow’s milk attenuated lipopolysaccharide-induced neuroinflammation and memory impairment in vitro and in vivo. J Dairy Res 2017; 84(4): 488-95.
[http://dx.doi.org/10.1017/S0022029917000620] [PMID: 29154736]
[31]
Toumi R, Abdelouhab K, Rafa H, et al. Beneficial role of the probiotic mixture Ultrabiotique on maintaining the integrity of intestinal mucosal barrier in DSS-induced experimental colitis. Immunopharmacol Immunotoxicol 2013; 35(3): 403-9.
[http://dx.doi.org/10.3109/08923973.2013.790413] [PMID: 23638770]
[32]
Abraham D, Feher J, Scuderi GL, et al. Exercise and probiotics attenuate the development of Alzheimer’s disease in transgenic mice: Role of microbiome. Exp Gerontol 2019; 115: 122-31.
[http://dx.doi.org/10.1016/j.exger.2018.12.005] [PMID: 30529024]
[33]
Athari Nik Azm S, Djazayeri A, Safa M, et al. Probiotics improve insulin resistance status in an experimental model of Alzheimer’s disease. Med J Islam Repub Iran 2017; 31: 103.
[http://dx.doi.org/10.14196/mjiri.31.103] [PMID: 29951404]
[34]
Ríos JA, Cisternas P, Arrese M, Barja S, Inestrosa NC. Is Alzheimer’s disease related to metabolic syndrome? A Wnt signaling conundrum. Prog Neurobiol 2014; 121: 125-46.
[http://dx.doi.org/10.1016/j.pneurobio.2014.07.004] [PMID: 25084549]
[35]
Kim B, Feldman EL. Insulin resistance as a key link for the increased risk of cognitive impairment in the metabolic syndrome. Exp Mol Med 2015; 47(3): e149-9.
[http://dx.doi.org/10.1038/emm.2015.3] [PMID: 25766618]
[36]
Burns JM, Honea RA, Vidoni ED, Hutfles LJ, Brooks WM, Swerdlow RH. Insulin is differentially related to cognitive decline and atrophy in Alzheimer’s disease and aging. Biochim Biophys Acta 2012; 1822(3): 333-9.
[http://dx.doi.org/10.1016/j.bbadis.2011.06.011] [PMID: 21745566]
[37]
Schiffrin EJ, Morley JE, Donnet-Hughes A, Guigoz Y. The inflammatory status of the elderly: the intestinal contribution. Mutat Res 2010; 690(1-2): 50-6.
[http://dx.doi.org/10.1016/j.mrfmmm.2009.07.011] [PMID: 19666034]
[38]
Solfrizzi V, D’Introno A, Colacicco AM, et al. Circulating biomarkers of cognitive decline and dementia. Clin Chim Acta 2006; 364(1-2): 91-112.
[http://dx.doi.org/10.1016/j.cca.2005.06.015] [PMID: 16139826]
[39]
Shimizu M, Hashiguchi M, Shiga T, Tamura HO, Mochizuki M. Meta-analysis: effects of probiotic supplementation on lipid profiles in normal to mildly hypercholesterolemic individuals. PLoS One 2015; 10(10): e0139795.
[http://dx.doi.org/10.1371/journal.pone.0139795] [PMID: 26473340]
[40]
Ruan Y, Sun J, He J, Chen F, Chen R, Chen H. Effect of probiotics on glycemic control: a systematic review and meta-analysis of randomized, controlled trials. PLoS One 2015; 10(7): e0132121.
[http://dx.doi.org/10.1371/journal.pone.0132121] [PMID: 26161741]
[41]
Basson AR, Minh L, Cominelli F. Complementary and Alternative Medicine (CAM) and Next-Generation CAM (NG-CAM) Strategies for Therapeutic Gut Microbiota Modulation in Inflammatory Bowel Disease. Gastroenterol Clin North Am 2017; 46(4): 689.
[http://dx.doi.org/10.1016/j.gtc.2017.08.002] [PMID: 29173517]
[42]
Zmora N, Zilberman-Schapira G, Suez J, et al. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell 2018; 174(6): 1388-405.
[http://dx.doi.org/10.1016/j.cell.2018.08.041]
[43]
Sierra S, Lara-Villoslada F, Sempere L, Olivares M, Boza J, Xaus J. Intestinal and immunological effects of daily oral administration of Lactobacillus salivarius CECT5713 to healthy adults. Anaerobe 2010; 16(3): 195-200.
[http://dx.doi.org/10.1016/j.anaerobe.2010.02.001] [PMID: 20159049]
[44]
Wang C, Nagata S, Asahara T, et al. Intestinal microbiota profiles of healthy pre-school and school-age children and effects of probiotic supplementation. Ann Nutr Metab 2015; 67(4): 257-66.
[http://dx.doi.org/10.1159/000441066] [PMID: 26496372]
[45]
Duan F, March JC. Engineered bacterial communication prevents Vibrio cholerae virulence in an infant mouse model. Proc Natl Acad Sci USA 2010; 107(25): 11260-4.
[http://dx.doi.org/10.1073/pnas.1001294107] [PMID: 20534565]
[46]
Lagenaur LA, Sanders-Beer BE, Brichacek B, et al. Prevention of vaginal SHIV transmission in macaques by a live recombinant Lactobacillus. Mucosal Immunol 2011; 4(6): 648-57.
[http://dx.doi.org/10.1038/mi.2011.30] [PMID: 21734653]
[47]
Vandenbroucke K, de Haard H, Beirnaert E, et al. Orally administered L. lactis secreting an anti-TNF Nanobody demonstrate efficacy in chronic colitis. Mucosal Immunol 2010; 3(1): 49-56.
[http://dx.doi.org/10.1038/mi.2009.116] [PMID: 19794409]
[48]
Motta J-P, Bermúdez-Humarán L G, Deraison C, et al. Food- grade bacteria expressing elafin protect against inflammation and restore colon homeostasis. Sci Transl Med 2012; 4(158): 158-44.
[http://dx.doi.org/10.1126/scitranslmed.3004212]
[49]
Bermúdez-Humarán LG, Cortes-Perez NG, Lefèvre F, et al. A novel mucosal vaccine based on live Lactococci expressing E7 antigen and IL-12 induces systemic and mucosal immune responses and protects mice against human papillomavirus type 16-induced tumors. J Immunol 2005; 175(11): 7297-302.
[http://dx.doi.org/10.4049/jimmunol.175.11.7297] [PMID: 16301635]
[50]
Daniel C, Roussel Y, Kleerebezem M, Pot B. Recombinant lactic acid bacteria as mucosal biotherapeutic agents. Trends Biotechnol 2011; 29(10): 499-508.
[http://dx.doi.org/10.1016/j.tibtech.2011.05.002] [PMID: 21665301]
[51]
Takiishi T, Korf H, Van Belle TL, et al. Reversal of autoimmune diabetes by restoration of antigen-specific tolerance using genetically modified Lactococcus lactis in mice. J Clin Invest 2012; 122(5): 1717-25.
[http://dx.doi.org/10.1172/JCI60530] [PMID: 22484814]
[52]
Chen Z, Guo L, Zhang Y, et al. Incorporation of therapeutically modified bacteria into gut microbiota inhibits obesity. J Clin Invest 2014; 124(8): 3391-406.
[http://dx.doi.org/10.1172/JCI72517] [PMID: 24960158]
[53]
Steidler L, Hans W, Schotte L, et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 2000; 289(5483): 1352-5.
[http://dx.doi.org/10.1126/science.289.5483.1352] [PMID: 10958782]
[54]
Braat H, Rottiers P, Hommes DW, et al. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn’s disease. Clin Gastroenterol Hepatol 2006; 4(6): 754-9.
[http://dx.doi.org/10.1016/j.cgh.2006.03.028] [PMID: 16716759]
[55]
Fossati E, Ekins A, Narcross L, et al. Reconstitution of a 10-gene pathway for synthesis of the plant alkaloid dihydrosanguinarine in Saccharomyces cerevisiae. Nat Commun 2014; 5(1): 3283.
[http://dx.doi.org/10.1038/ncomms4283] [PMID: 24513861]
[56]
Hawkins KM, Smolke CD. Production of benzylisoquinoline alkaloids in Saccharomyces cerevisiae. Nat Chem Biol 2008; 4(9): 564-73.
[http://dx.doi.org/10.1038/nchembio.105] [PMID: 18690217]
[57]
Nakagawa A, Matsuzaki C, Matsumura E, et al. (R,S)-tetrahydropapaveroline production by stepwise fermentation using engineered Escherichia coli. Sci Rep 2014; 4: 6695.
[http://dx.doi.org/10.1038/srep06695] [PMID: 25331563]
[58]
Zhang C, Liu L, Teng L, et al. Metabolic engineering of Escherichia coli BL21 for biosynthesis of heparosan, a bioengineered heparin precursor. Metab Eng 2012; 14(5): 521-7.
[http://dx.doi.org/10.1016/j.ymben.2012.06.005] [PMID: 22781283]
[59]
Li X-R, Tian G-Q, Shen H-J, Liu J-Z. Metabolic engineering of Escherichia coli to produce zeaxanthin. J Ind Microbiol Biotechnol 2015; 42(4): 627-36.
[http://dx.doi.org/10.1007/s10295-014-1565-6] [PMID: 25533633]
[60]
Marienhagen J, Bott M. Metabolic engineering of microorganisms for the synthesis of plant natural products. J Biotechnol 2013; 163(2): 166-78.
[http://dx.doi.org/10.1016/j.jbiotec.2012.06.001] [PMID: 22687248]
[61]
Mora-Pale M, Sanchez-Rodriguez SP, Linhardt RJ, Dordick JS, Koffas MA. Metabolic engineering and in vitro biosynthesis of phytochemicals and non-natural analogues. Plant Sci 2013; 210: 10-24.
[http://dx.doi.org/10.1016/j.plantsci.2013.05.005] [PMID: 23849109]
[62]
Zhao J, Li Q, Sun T, et al. Engineering central metabolic modules of Escherichia coli for improving β-carotene production. Metab Eng 2013; 17: 42-50.
[http://dx.doi.org/10.1016/j.ymben.2013.02.002] [PMID: 23500001]
[63]
Wang J, Guleria S, Koffas MA, Yan Y. Microbial production of value-added nutraceuticals. Curr Opin Biotechnol 2016; 37: 97-104.
[http://dx.doi.org/10.1016/j.copbio.2015.11.003] [PMID: 26716360]
[64]
Howes MR, Perry NSL, Vásquez-Londoño C, Perry EK. Role of phytochemicals as nutraceuticals for cognitive functions affected in ageing. Br J Pharmacol 2020; 177(6): 1294-315.
[http://dx.doi.org/10.1111/bph.14898] [PMID: 31650528]
[65]
An X, Bao Q, Di S, et al. The interaction between the gut Microbiota and herbal medicines. Biomed Pharmacother 2019; 118: 109252.
[http://dx.doi.org/10.1016/j.biopha.2019.109252] [PMID: 31545247]
[66]
Wang J, Song Y, Chen Z, Leng S X. Connection between systemic inflammation and neuroinflammation underlies neuroprotective mechanism of several phytochemicals in neurodegenerative diseases. Oxid Med Cell Longev 2018; 2018: 1972714.
[http://dx.doi.org/10.1155/2018/1972714]
[67]
Soucy SM, Huang J, Gogarten JP. Horizontal gene transfer: building the web of life. Nat Rev Genet 2015; 16(8): 472-82.
[http://dx.doi.org/10.1038/nrg3962] [PMID: 26184597]
[68]
Sola-Oladokun B, Culligan EP, Sleator RD. Engineered probiotics: applications and biological containment. Annu Rev Food Sci Technol 2017; 8: 353-70.
[http://dx.doi.org/10.1146/annurev-food-030216-030256] [PMID: 28125354]
[69]
Kelly CR, Khoruts A, Staley C, et al. Effect of fecal microbiota transplantation on recurrence in multiply recurrent Clostridium difficile infection: a randomized trial. Ann Intern Med 2016; 165(9): 609-16.
[http://dx.doi.org/10.7326/M16-0271] [PMID: 27547925]
[70]
Zhang F, Luo W, Shi Y, Fan Z, Ji G. Should we standardize the 1,700-year-old fecal microbiota transplantation? Am J Gastroenterol 2012; 107(11): 1755.
[http://dx.doi.org/10.1038/ajg.2012.251] [PMID: 23160295]
[71]
van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 2013; 368(5): 407-15.
[http://dx.doi.org/10.1056/NEJMoa1205037] [PMID: 23323867]
[72]
Valiquette L, Laupland KB. Something old, something new, something borrowed. Can J Infect Dis Med Microbiol 2013; 24(2): 63-4.
[http://dx.doi.org/10.1155/2013/514130] [PMID: 24421800]
[73]
Zhan G, Yang N, Li S, et al. Abnormal gut microbiota composition contributes to cognitive dysfunction in SAMP8 mice. Aging (Albany NY) 2018; 10(6): 1257-67.
[http://dx.doi.org/10.18632/aging.101464] [PMID: 29886457]
[74]
Yu F, Han W, Zhan G, et al. Abnormal gut microbiota composition contributes to cognitive dysfunction in streptozotocin-induced diabetic mice. Aging (Albany NY) 2019; 11(10): 3262-79.
[http://dx.doi.org/10.18632/aging.101978] [PMID: 31123221]
[75]
Dodiya HB, Kuntz T, Shaik SM, et al. Sex-specific effects of microbiome perturbations on cerebral Aβ amyloidosis and microglia phenotypes. J Exp Med 2019; 216(7): 1542-60.
[http://dx.doi.org/10.1084/jem.20182386] [PMID: 31097468]
[76]
Harach T, Marungruang N, Duthilleul N, et al. Reduction of Abeta amyloid pathology in APPPS1 transgenic mice in the absence of gut microbiota. Sci Rep 2017; 7: 41802.
[http://dx.doi.org/10.1038/srep41802] [PMID: 28176819]
[77]
Cui B, Su D, Li W, et al. Effects of chronic noise exposure on the microbiome-gut-brain axis in senescence-accelerated prone mice: implications for Alzheimer’s disease. J Neuroinflammation 2018; 15(1): 190.
[http://dx.doi.org/10.1186/s12974-018-1223-4] [PMID: 29933742]
[78]
Fujii Y, Nguyen TTT, Fujimura Y, et al. Fecal metabolite of a gnotobiotic mouse transplanted with gut microbiota from a patient with Alzheimer’s disease. Biosci Biotechnol Biochem 2019; 83(11): 2144-52.
[http://dx.doi.org/10.1080/09168451.2019.1644149] [PMID: 31327302]
[79]
Zhou H, Tai J, Xu H, Lu X, Meng D. Xanthoceraside could ameliorate Alzheimer’s disease symptoms of rats by affecting the gut microbiota composition and modulating the endogenous metabolites levels. Front Pharmacol 2019; 10: 1035.
[http://dx.doi.org/10.3389/fphar.2019.01035] [PMID: 31572201]
[80]
Spychala MS, Venna VR, Jandzinski M, et al. Age-related changes in the gut microbiota influence systemic inflammation and stroke outcome. Ann Neurol 2018; 84(1): 23-36.
[http://dx.doi.org/10.1002/ana.25250] [PMID: 29733457]
[81]
Zhou Z-L, Jia X-B, Sun M-F, et al. Neuroprotection of fasting mimicking diet on MPTP-induced Parkinson’s disease mice via gut microbiota and metabolites. Neurotherapeutics 2019; 16(3): 741-60.
[http://dx.doi.org/10.1007/s13311-019-00719-2] [PMID: 30815845]
[82]
Pigneur B, Sokol H. Fecal microbiota transplantation in inflammatory bowel disease: the quest for the holy grail. Mucosal Immunol 2016; 9(6): 1360-5.
[http://dx.doi.org/10.1038/mi.2016.67] [PMID: 27461176]
[83]
Rubin DT. Curbing our enthusiasm for fecal transplantation in ulcerative colitis. Am J Gastroenterol 2013; 108(10): 1631-3.
[http://dx.doi.org/10.1038/ajg.2013.279] [PMID: 24091506]
[84]
Jiang ZD, Ajami NJ, Petrosino JF, et al. Randomised clinical trial: faecal microbiota transplantation for recurrent Clostridum difficile infection - fresh, or frozen, or lyophilised microbiota from a small pool of healthy donors delivered by colonoscopy. Aliment Pharmacol Ther 2017; 45(7): 899-908.
[http://dx.doi.org/10.1111/apt.13969] [PMID: 28220514]
[85]
Hu X, Wang T, Jin F. Alzheimer’s disease and gut microbiota. Sci China Life Sci 2016; 59(10): 1006-23.
[http://dx.doi.org/10.1007/s11427-016-5083-9] [PMID: 27566465]
[86]
Jiang C, Li G, Huang P, Liu Z, Zhao B. The gut microbiota and Alzheimer’s disease. J Alzheimers Dis 2017; 58(1): 1-15.
[http://dx.doi.org/10.3233/JAD-161141] [PMID: 28372330]
[87]
Kobayashi Y, Kinoshita T, Matsumoto A, Yoshino K, Saito I, Xiao J-Z. Bifidobacterium breve A1 supplementation improved cognitive decline in older adults with mild cognitive impairment: an open-label, single-arm study. J Prev Alzheimers Dis 2019; 6(1): 70-5.
[PMID: 30569089]
[88]
Kobayashi Y, Kuhara T, Oki M, Xiao J-Z. Effects of Bifidobacterium breve A1 on the cognitive function of older adults with memory complaints: a randomised, double-blind, placebo-controlled trial. Benef Microbes 2019; 10(5): 511-20.
[http://dx.doi.org/10.3920/BM2018.0170] [PMID: 31090457]
[89]
Tamtaji OR, Heidari-Soureshjani R, Mirhosseini N, et al. 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 2019; 38(6): 2569-75.
[http://dx.doi.org/10.1016/j.clnu.2018.11.034] [PMID: 30642737]
[90]
Reid G, Younes JA, Van der Mei HC, Gloor GB, Knight R, Busscher HJ. Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol 2011; 9(1): 27-38.
[http://dx.doi.org/10.1038/nrmicro2473] [PMID: 21113182]
[91]
Seedorf H, Griffin NW, Ridaura VK, et al. Bacteria from diverse habitats colonize and compete in the mouse gut. Cell 2014; 159(2): 253-66.
[http://dx.doi.org/10.1016/j.cell.2014.09.008] [PMID: 25284151]
[92]
Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 2016; 14(1): 20-32.
[http://dx.doi.org/10.1038/nrmicro3552] [PMID: 26499895]
[93]
Cullen TW, Schofield WB, Barry NA, et al. Gut microbiota. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 2015; 347(6218): 170-5.
[http://dx.doi.org/10.1126/science.1260580] [PMID: 25574022]
[94]
Wu M, McNulty NP, Rodionov DA, et al. Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides. Science 2015; 350(6256): aac5992.
[http://dx.doi.org/10.1126/science.aac5992] [PMID: 26430127]
[95]
Hamady ZZ, Scott N, Farrar MD, et al. Treatment of colitis with a commensal gut bacterium engineered to secrete human TGF-β1 under the control of dietary xylan 1. Inflamm Bowel Dis 2011; 17(9): 1925-35.
[http://dx.doi.org/10.1002/ibd.21565] [PMID: 21830271]
[96]
Mimee M, Citorik RJ, Lu TK. Microbiome therapeutics - Advances and challenges. Adv Drug Deliv Rev 2016; 105(Pt A): 44-54.
[http://dx.doi.org/10.1016/j.addr.2016.04.032] [PMID: 27158095]
[97]
Van den Abbeele P, Belzer C, Goossens M, et al. Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. ISME J 2013; 7(5): 949-61.
[http://dx.doi.org/10.1038/ismej.2012.158] [PMID: 23235287]
[98]
Auchtung JM, Robinson CD, Britton RA. Cultivation of stable, reproducible microbial communities from different fecal donors using minibioreactor arrays (MBRAs). Microbiome 2015; 3(1): 42.
[http://dx.doi.org/10.1186/s40168-015-0106-5] [PMID: 26419531]
[99]
Costello CM, Sorna RM, Goh Y-L, Cengic I, Jain NK, March JC. 3-D intestinal scaffolds for evaluating the therapeutic potential of probiotics. Mol Pharm 2014; 11(7): 2030-9.
[http://dx.doi.org/10.1021/mp5001422] [PMID: 24798584]
[100]
Lukovac S, Belzer C, Pellis L, et al. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. MBio 2014; 5(4): e01438-14.
[http://dx.doi.org/10.1128/mBio.01438-14] [PMID: 25118238]
[101]
Kim HJ, Li H, Collins JJ, Ingber DE. Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut-on-a-chip. Proc Natl Acad Sci USA 2016; 113(1): E7-E15.
[http://dx.doi.org/10.1073/pnas.1522193112] [PMID: 26668389]
[102]
Lloyd-Price J, Abu-Ali G, Huttenhower C. The healthy human microbiome. Genome Med 2016; 8(1): 51.
[http://dx.doi.org/10.1186/s13073-016-0307-y] [PMID: 27122046]
[103]
Angelberger S, Reinisch W, Makristathis A, et al. Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation. Am J Gastroenterol 2013; 108(10): 1620-30.
[http://dx.doi.org/10.1038/ajg.2013.257] [PMID: 24060759]
[104]
Petrof EO, Gloor GB, Vanner SJ, et al. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: ‘RePOOPulating’ the gut. Microbiome 2013; 1(1): 3.
[http://dx.doi.org/10.1186/2049-2618-1-3] [PMID: 24467987]
[105]
Brandt LJ. American Journal of Gastroenterology Lecture: Intestinal microbiota and the role of fecal microbiota transplant (FMT) in treatment of C. difficile infection. Am J Gastroenterol 2013; 108(2): 177-85.
[http://dx.doi.org/10.1038/ajg.2012.450] [PMID: 23318479]
[106]
Mancuso C, Santangelo R. Alzheimer’s disease and gut microbiota modifications: The long way between preclinical studies and clinical evidence. Pharmacol Res 2018; 129: 329-36.
[http://dx.doi.org/10.1016/j.phrs.2017.12.009] [PMID: 29233677]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy