Advertisement

A Review of the Relationship Between Gut Microbiota and Memory

  • Amira Benmelouka
  • Ahmed M. Sherif
  • Mahmoud Ahmed EbadaEmail author
Chapter

Abstract

Alzheimer’s disease (AD) became a public health problem due to its increasing incidence and the dangerous sequences that affect society. Like many other neurodegenerative disorders, the complete mechanism of AD is not known yet. Scientists think that AD is caused by the combination of various factors related to the environment and the genetic basis. Many studies have demonstrated the role of human gut microbiota in different physiological and pathological pathways affecting many distant organs particularly the nervous system. Researchers observed a variety of disturbances of the intestinal microbiota homeostasis in many conditions such as diet changes, aging, probiotic and antibiotic administration. The study of this homeostasis and its different characteristics can help us understand the various mechanisms by which it influences the gut-brain axis. It also helps to find solutions to many health problems including neurodegenerative diseases.

Keywords

Alzheimer’s disease Cognition Dementia Gut microbiota Memory Neurodegeneration Neuroinflammation 

References

  1. Agahi A, Hamidi GA, Daneshvar R, Hamdieh M, Soheili M, Alinaghipour A et al (2018) Does severity of Alzheimer’s disease contribute to its responsiveness to modifying gut microbiota? A double blind clinical trial. Front Neurol 9(August):1–9Google Scholar
  2. Akbari E, Asemi Z, Kakhaki RD, Bahmani F, Kouchaki E, Tamtaji OR, Hamidi GA, Salami M (2016) Effect of probiotic supplementation on cognitive function and metabolic status in Alzheimer’s disease. a randomised double blind and controlled trial. Front Aging Neurosci 8:256PubMedPubMedCentralCrossRefGoogle Scholar
  3. Asiimwe N, Yeo SG, Kim MS, Jung J, Jeong N (2016) Nitric oxide: exploring the contextual link with Alzheimer’s disease. Oxidat Med cell Longev:1–10CrossRefGoogle Scholar
  4. Asti A, Gioglio L (2014) Can a bacterial endotoxin be a key factor in the kinetics of amyloid fibril formation? J Alzheimer’s Dis 39(1):169–179CrossRefGoogle Scholar
  5. Aziz Q, Doré J, Emmanuel A (2013) Gut microbiota and gastrointestinal health: current concepts and future directions. Neurogastroenterol Motil 25:4–15PubMedCrossRefGoogle Scholar
  6. Bajaj JS, Ridlon JM, Hylemon PB, Thacker LR, Heuman DM, Smith S, Sikaroodi M, Gillevet PM (2011) Linkage of gut microbiome with cognition in hepatic encephalopathy. Am J Physiol Liver Physiol 302:G168–G175Google Scholar
  7. Banack SA, Caller TA, Stommel EW (2010) The cyanobacteria derived toxin beta-N-mthylamino-L-alanine and amyotrophic lateral sclerosis. Toxins (Basel) 2(12):2837–2850PubMedCentralCrossRefPubMedGoogle Scholar
  8. Banks WA (2008) The blood-brain barrier: connecting the gut and the brain. Regul Pept 149:11–14PubMedPubMedCentralCrossRefGoogle Scholar
  9. Barberger-Gateau P, Raffaitin C, Letenneur L, Berr C, Tzourio C, Dartigues JF, Alperovitch A (2007) Dietary patterns and risk of dementia: the three-city cohort study. Neurology 69:1921–1930PubMedCrossRefGoogle Scholar
  10. Barrett E, Ross RP, O’Toole PW, Fitzgerald GF, Stanton C (2012) gamma-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol 113:411–417PubMedCrossRefGoogle Scholar
  11. Bekris LM, Yu CE, Bird TD, Tsuang DW (2011) Genetics of Alzheimer disease. J Geriatr Psychiatry Neurol 23(4):213–227CrossRefGoogle Scholar
  12. Biagi E, Candela M, Turroni S, Garagnani P, Franceschi C, Brigidi P (2013) Ageing and gut microbes: perspectives for health maintenance and longevity. Pharmacol Res 69:11–20PubMedCrossRefGoogle Scholar
  13. Bonfili L, Cecarini V, Berardi S, Scarpona S, Suchodolski JS, Nasuti C, Fiorini D, Grame MCB (2017) Microbiota modulation countacts Alzheimer’s disease progression influencing neurnal proteolysis and gut hormones plasma levels. Sci Rep:7, 2426Google Scholar
  14. Borre YE, O’Keeffe GW, Clarke G, Stanton C, Dinan TG, Cryan JF (2014) Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med 20(9):509–518PubMedCrossRefGoogle Scholar
  15. Bradley WGMD (2009) Beyond Guam: the cyanobacteria/BMAA hypothesis of the cause of ALS and other neurodegenerative diseases. Amytroph Lateral Sclera 10:7–20CrossRefGoogle Scholar
  16. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Toth M, Korecka A, Bakocevic N, Ng LG, Kundu P, Gulyas B, Halldin C, Hultenby K, Nilsson H, Hebert H, Volpe BT, Diamod B, Pettersson S (2014) The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med 6:263ra158PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bravo JA, Julio-Pieper M, Forsythe P, Kunze W, Dinan TG, Bienenstock J et al (2012) Communication between gastrointestinal bacteria and the nervous system. Curr Opin Pharmacol 12(6):667–672PubMedCrossRefGoogle Scholar
  18. Brenner SR (2013) Blue-green algae or cyanobacteria in the intestinal micro-flora may produce neurotoxins such as Beta-N-Methylamino-l-Alanine (BMAA) which may be related to development of amyotrophic lateral sclerosis, Alzheimer’s disease and Parkinson-Dementia-Complex. Med Hypotheses 80(1):103PubMedCrossRefGoogle Scholar
  19. Bruce-Keller AJ, Salbaum JM, Luo M, Blanchard ET, Taylor CM, Welsh DA, Berthoud H (2015) Obese-type gut microbiota induce neurobehavioral changes in the absence of obesity. Biol Psychiatry 77:607–615PubMedCrossRefGoogle Scholar
  20. Buford TW (2017) Trust your gut: the gut microbiome in age-related inflammation, health, and disease:1–11Google Scholar
  21. Chen SG, Stribinskis V, Rane MJ, Demuth DR, Gozal E, Roberts AM et al (2016) Exposure to the functional bacterial amyloid protein curli enhances alpha-synuclein aggregation in aged fischer 344 RAts and caenorhabditis elegans. Sci Rep 6(September):1–10Google Scholar
  22. Chen G, Xu T, Yan Y, Zhou Y, Jiang Y, Melcher K et al (2017) Amyloid beta: structure , biology and structure-based therapeutic development. Acta Pharmacologica Sinica 38(9):1205–1235PubMedPubMedCentralCrossRefGoogle Scholar
  23. Choi HH, Cho YS (2016) Fecal microbiota transplantation: current applications, effectiveness, and future perspectives. Clin Endosc. Taylor & Francis 49:257–265Google Scholar
  24. Cho I, Blaser MJ (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13(4):260–70. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22411464PubMedPubMedCentralCrossRefGoogle Scholar
  25. Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, Harris HMB, Coakley M, Lakshminarayanan B, O’Sullivan O, Fitzgerald GF, Deane J, O’Connor M, Harnedy N, O’Connor K, O’Mahony D, van Sinderen D, Wal P (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488:178–184CrossRefGoogle Scholar
  26. Collins SM, Surette M, Bercik P (2012) The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 10:735–742PubMedCrossRefGoogle Scholar
  27. Cox PA, Davis DA, Mash DC, Metcalf JS, Banack S (2016) Dietary exposure to an environmental toxin triggers neurofibrillary tangles and amyloid deposits in the brain. Proc Biol Sci 283:20152397PubMedPubMedCentralCrossRefGoogle Scholar
  28. Crane PK, Walker R, Hubbard RA, Li G, Nathan DM, Zheng H, Haneuse S, Craft S, Montine TJ, Kahn SE, McCormick W, McCurry SM, Bowen JD, Larson E (2013) Glucose levels and risk of dementia. N Engl J Med 369:540–548PubMedPubMedCentralCrossRefGoogle Scholar
  29. Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13(10):701–712PubMedCrossRefGoogle Scholar
  30. Cryan JF, O’Mahony SM (2011) The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil 23(3):187–192PubMedCrossRefGoogle Scholar
  31. Davari S, Talaei SA, Alaei HSM (2013) Probotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: behavioral and electrophysiological proofs for microbiome-gut-brain axis. Neuroscience 240:287–296PubMedCrossRefGoogle Scholar
  32. De Filippo C, Cavalieri D, Di Paola M, Ramzzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 107:14691PubMedPubMedCentralCrossRefGoogle Scholar
  33. Desbonnet L, Clarke G, Traplin A, O’Sullivan O, Crispie F, Moloney RD et al (2015) Gut microbiota depletion from early adolescence in mice: implications for brain and behaviour. Brain Behav Immun 48(April):165–173PubMedCrossRefGoogle Scholar
  34. Distrutti E, O’Reilly JA, McDonald C, Cipriani S, Renga B, Lynch MA et al (2014) Modulation of intestinal microbiota by the probiotic VSL#3 resets brain gene expression and ameliorates the age-related deficit in LTP. PLoS One 9(9):176–184CrossRefGoogle Scholar
  35. Dominicé PF, Lehto L (1991) Koulutuselämäkertojen laatiminen ryhmäreflektion välineenä. Amyloid Depos as Cent event Aetiol Alzheimer’s Dis:214–232Google Scholar
  36. Durães F, Pinto M, Sousa E (2018) Old drugs as new treatments for neurodegenerative diseases. Pharmaceuticals 11(2):1–21CrossRefGoogle Scholar
  37. Erny D, Hrabe de Angelis AL, Prinz M (2017) Communicating systems in the body: how microbiota and microglia cooperate. Immunology 150:7–15PubMedCrossRefPubMedCentralGoogle Scholar
  38. Fassbender K, Walter S, Kühl S, Landmann R, Ishii K, Bertsch T et al (2004) The LPS receptor (CD14) links innate immunity with Alzheimer’s disease. FASEB J 18(1):203–205PubMedCrossRefGoogle Scholar
  39. Foster JA, Neufeld KA (2018) Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 36:305–312CrossRefGoogle Scholar
  40. Friedland RP (2015) Mechanisms of molecular mimicry involving the microbiota in neurodegeneration. J Alzheimer’s Dis 45:349–362CrossRefGoogle Scholar
  41. Gareau MG (2014) Microbiota-gut-brain axis and cognitive function. Adv Exp Med Biol 817:357–372PubMedCrossRefGoogle Scholar
  42. Gareau MG, Wine E, Rodrigues DM, Cho JH, Whary MT, Philpott DJ et al (2011) Bacterial infection causes stress-induced memory dysfunction in mice. Gut 60(3):307–317PubMedCrossRefGoogle Scholar
  43. Gill SR et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hauss-Wegrzyniak B, Vraniak PD, Wenk GL (2000) LPS-induced neuroinflammatory effects do not recover with time. Neuroreport 11(8):1759–1763PubMedCrossRefGoogle Scholar
  45. He Z, Cui B, Zhang T, Li P, Long C, Ji G et al (2017) Fecal microbiota transplantation cured epilepsy in a case with Crohn’s disease: the first report. World J Gastroenterol 23(19):3565–3568PubMedPubMedCentralCrossRefGoogle Scholar
  46. Heijitz RD, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A et al (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 108:3047–3052CrossRefGoogle Scholar
  47. Heneka MT, Golenbock DT, Latz E (2015) Innate immunity in Alzheimer’s disease. Nat Immunol 16:229–236PubMedCrossRefGoogle Scholar
  48. Hoban AE, Stilling RM, Ryan FJ, Dinan TG, Claesson MJ, Clarke G, Cryan J (2016) Regulation of prefrontal cortex myelination by the microbiota. Transl Psychiatry 6:e774PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hornig M (2013) The role of microbes and autoimmunity in the pathogenesis of neuropsychiatric illness. Curr Opin Rheumatol 25:488–795PubMedCrossRefGoogle Scholar
  50. Hu X, Wang T, Jin F (2016) Alzheimer’s disease and gut microbiota. Sci China Life Sci 59:1006–1023PubMedCrossRefGoogle Scholar
  51. Hufeldt MR, Nielsen DS, Vogensen FK, Midtvedt T, Hansen A (2010) Variation in the gut microbiota of laboratory mice is related to both genetic and environmental factors. Comp Med 60:336–347PubMedPubMedCentralGoogle Scholar
  52. Hufnagel DA, Tükel Ç, Chapman MR (2013) Disease to dirt: the biology of microbial amyloids. PLoS Pathog 9(11):1–5CrossRefGoogle Scholar
  53. Jiang C, Li G, Huang P, Liu Z, Zhao B (2017) The gut microbiota and Alzheimer’s disease. J Alzheimer’s Dis 58(1):1–15CrossRefGoogle Scholar
  54. Kobayashi Y, Sugahara H, Shimada K, Mitsuyama E, Kuhara T, Yasuoka A et al (2017) Therapeutic potential of Bifidobacterium breve strain A1 for preventing cognitive impairment in Alzheimer’s disease. Sci Rep 7(1):8614–8622CrossRefGoogle Scholar
  55. Kowalski K, Mulak A, Words K (2019) Brain-gut-microbiota axis in Alzheimer’s disease. J Neurogastroenterol Motil 25(1):48–60PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kumar DKV, Choi HS, Washicosky KJ, Eimer WA, Tucker S, Ghofrani J et al (2016) Amyloid-β peptide protects against microbial infection in mouse and worm models of Alzheimer’s disease. Sci Transl Med 8(340):340ra72PubMedCrossRefGoogle Scholar
  57. La Rosa F, Clerici M, Ratto D, Occhinegro A, Licito A, Romeo M, Lorio CD, Rossi P (2018) The gut-brain axis in Alzheimer’s disease and omega-3. A critical overview of clinical trials. Nutrients 10:E1267PubMedCrossRefGoogle Scholar
  58. Ladner-Keay CL, LeVatte M, Wishart DS (2016) Role of polysaccharide and lipid in lipopolysaccharide induced prion protein conversion. Prion 10(6):466–483PubMedPubMedCentralCrossRefGoogle Scholar
  59. Lakhan SE, Caro M, Hadzimichalis N (2013) NMDA receptor activity in neuropsychiatric disorders. Front Psychiatry 4(June):1–7Google Scholar
  60. Larsen P, Nielson JL, Dueholm MS, Wetzel R, Otzen D, Nielsen P (2007) Biofilms, amyloid adhesins are abundant in natural. Environ Microbiol 9:3077–3090PubMedCrossRefGoogle Scholar
  61. Larsen P, Nielsen JL, Otzen D, Nielsen PH (2008) Amyloid-like adhesins produced by floc-forming and filamentous bacteria in activated sludge. Appl Environ Microbiol 74(5):1517–1526PubMedPubMedCentralCrossRefGoogle Scholar
  62. Liu Y, Walter S, Stagi M, Cherny D, Letiembre M, Schulz-Schaeffer W et al (2005) LPS receptor (CD14): a receptor for phagocytosis of Alzheimer’s amyloid peptide. Brain 128(8):1778–1789PubMedCrossRefGoogle Scholar
  63. Lu B, Nagappan G, Guan X, Nathan PJ, Wren P (2013) BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases. Nat Rev Neurosci 14:401–416PubMedCrossRefGoogle Scholar
  64. Lukiw WJ (2016) Bacteroides fragilis lipopolysaccharide and inflammatory signaling in Alzheimer’s disease. Front Microbiol 7(September):1–6Google Scholar
  65. Meek PD, McKeithan K, Schumock GT (1998) Economic considerations in Alzheimer’s disease. Pharmacotherapy 18:68–72PubMedGoogle Scholar
  66. Mendelsohn D, Riedel WJ, Sambeth A (2009) Effects of acute tryptophan depletion on memory, attention and executive functions: a systematic review. Neurosci Biobehav Rev 33(6):926–952PubMedCrossRefGoogle Scholar
  67. Minter MR, Zhang C, Leone V, Ringus DL, Zhang X, Oyler-Castrillo P et al (2016) Antibiotic-induced perturbations in gut microbial diversity influences neuro-inflammation and amyloidosis in a murine model of Alzheimer’s disease. Sci Rep 6(July):1–12Google Scholar
  68. Mohler L, Mattei D, Heimesaat MM, Bereswill S, Fisher A, Alutis M, French T, Hambardzumyan D, Matzinger P, Dunay IR, Wolf S (2016) Ly6C(hi) monocytes provide a link between antibiotic induced changes in gut microbiota and adult hippocampal neurogenesis. Cell Rep 15:1945–1956CrossRefGoogle Scholar
  69. Nishida A, Inoue R, Inatomi O, Bamba S, Naito Y, Andoh A (2018) Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin J Gastroenterol 11(1):1–10PubMedCrossRefGoogle Scholar
  70. Nunn PB, Ponnusamy M (2009) Beta-N-methylalanine (BMAA): metabolism and metabolic effects in model systems and in neural and other tissues of the rat in vitro. Toxicon 54:85–94PubMedCrossRefGoogle Scholar
  71. Ohara T (2016) Epidemiology of diabetes and risk of dementia. Brain Nerve 68:719–728PubMedGoogle Scholar
  72. Ozawa M, Ninomiya T, Ohara T, Doi Y, Uchida K, Shirota T et al (2013) Dietary patterns and risk of dementia in an elderly Japanese. Am J Clin Nutr 97(5):1076–1082PubMedCrossRefGoogle Scholar
  73. Pérez Martinez G, Bauerl C, Collado M (2014) Understanding gut microbiota in elderly’s health will enable intervention through probiotics. Benef Microbes 5:235–246PubMedCrossRefGoogle Scholar
  74. Peuhkuri K, Vapaatalo H, Korpela R (2016) Even low-grade inflammation impacts on small intestinal function. World J Gastroenterol 15(5):477–491Google Scholar
  75. Pistollato F, Sumalla CS, Elio I, Masias VM, Giampieri F (2016) Role of gut microbiota and nutrients in amyloids formation and pathogenesis of Alzheimer disease. Nutr Rev 74:624–634PubMedCrossRefGoogle Scholar
  76. Priyamvada S, Gomes R, Gill RK, Saksena S, Alrefai WA, Dudeja PK (2016) Mechanisms underlying dysregulation of electrolyte absorption in IBD associated diarrhea. Inflamm Bowel Dis 21(12):2926–2935CrossRefGoogle Scholar
  77. Proctor C, Thiennimitr P, Chattipakorn N, Chattipakorn SC (2017) Diet, gut microbiota and cognition. Metab Brain Dis 32:1–17PubMedCrossRefGoogle Scholar
  78. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59–65PubMedPubMedCentralCrossRefGoogle Scholar
  79. Rampelli S, Candela M, Turroni S, Biagi E, Collino S, Toole PWO et al (2013) Functional metagenomic profiling of intestinal microbiome in extreme ageing. Aging 5(12):902–912PubMedPubMedCentralCrossRefGoogle Scholar
  80. Reitz C, Brayne C, Mayeux R (2011) Epidemiology of Alzheimer disease. Nat Rev Neurol. 7(3):137–152PubMedPubMedCentralCrossRefGoogle Scholar
  81. Rothhammer V, Borucki DM, Tjon EC, Takenaka MC, Chao CC, Ardura-Fabregat A et al (2018) Microglial control of astrocytes in response to microbial metabolites. Nature 557(7707):724–728PubMedPubMedCentralCrossRefGoogle Scholar
  82. Salazar N, Valdés-Varela L, González S, Gueimonde M, de los Reyes-Gavilán CG (2017) Nutrition and the gut microbiome in the elderly. Gut Microbes 8(2):82–97PubMedCrossRefGoogle Scholar
  83. Saleem F, Bjorndahl TC, Ladner CL, Perez-Pineiro R, Ametaj BN, Wishart DS (2014) Lipopolysaccharide induced conversion of recombinant prion protein. Prion 8(2):1–12CrossRefGoogle Scholar
  84. Sampson TR, Mazmanian S (2015) Control of brain development, function, and behavior by the microbiome. Cell Host Microbe 17:565–576PubMedPubMedCentralCrossRefGoogle Scholar
  85. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH (2013) The influence of diet on the gut microbiota. Pharmacol Res 69(1):52–60PubMedCrossRefGoogle Scholar
  86. Semrin G, Fishman DS, Athos Bousvaros AZ, Grand RJ, Weinstein DA (2016) Impaired intestinal iron absorption in Crohn’s disease correlates with disease activity and markers of inflammation. Inflamm Bowel Dis 33(2):557–573Google Scholar
  87. Smith QR, Nagura H, Takada Y, Duncan M (1992) Facilitated transport of the neurotoxin, beta-N-methylamino-L-alanine, across the blood-brain-barrier. J Neurochem 58(4):1330–1337PubMedCrossRefGoogle Scholar
  88. Solas M, Milagro FI, Ramírez MJ, Martínez JA (2017) Inflammation and gut-brain axis link obesity to cognitive dysfunction: plausible pharmacological interventions. Curr Opin Pharmacol 37:87–92PubMedCrossRefGoogle Scholar
  89. Strooper BDE (2010) Proteases and proteolysis in Alzheimer disease: a multifactorial view on the disease process. Physiol Rev 90:465–494PubMedCrossRefGoogle Scholar
  90. Swerdlow R, Burns J, Khan S (2010) The AD mitochondrial cascade hypothesis. J Alzheimers Dis 20(Suppl 2):265–279PubMedCentralCrossRefPubMedGoogle Scholar
  91. Swerdlow RH, Khan SM (2004) A “mitochondrial cascade hypothesis” for sporadic Alzheimer’s disease. Med Hypotheses 63(1):8–20PubMedCrossRefGoogle Scholar
  92. Taichi A, Suzuki MW (2014) Geographical variation of human gut microbial composition. Biol Lett 10:20131037CrossRefGoogle Scholar
  93. Tang G, Yin W, Liu W (2017) Is frozen fecal microbiota transplantation as effective as fresh fecal microbiota transplantation in patients with recurrent or refractory Clostridium difficile infection: a meta-analysis? Diagn Microbiol Infect Dis. Elsevier Inc. 88:322–329PubMedCrossRefGoogle Scholar
  94. Tiihonen K, Ouwehand AC, Rautonen N (2010) Human intestinal microbiota and healthy aging. Ageing Res Rev 9:107–116PubMedCrossRefGoogle Scholar
  95. Tran L, Greenwood-Van Meerveld B (2013) Age-associated remodeling of the intestinal epithelial barrier. J Gerontol 68(9):1045–1056CrossRefGoogle Scholar
  96. Tse JK (2017) Gut microbiota, nitric oxide and microglia as pre-requisites for neurodegenerative disorders. ACS Chem Neurosci 8:1438–1447PubMedCrossRefGoogle Scholar
  97. Tükel Ç, Nishimori JH, Wilson RP, Winter MG, Keestra AM, van Putten JPM, Baumler AJ (2010) Toll-like receptors 1 and 2 cooperatively mediate immune responses to curli, a common amyloid from enterobacterial biofilms. Cell Microbiol 12:1495–1505PubMedCrossRefGoogle Scholar
  98. United Nations (2017) World Population Prospects The 2017 RevisionGoogle Scholar
  99. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JFWM, Tijssen JGP, Speelman P, Dijkgraaf MGW, Keller JJ (2011) Duodenal infusion of donor feces for recurrent clostridium difficile. Univ Bucharest Rev Lit Cult Stud Ser 13(1):7–20Google Scholar
  100. Walker LC, Schelle J, Jucker M (2016) The prion-like properties of amyloid-β assemblies: implications for Alzheimer’s disease. Cold Spring Harb Perspect Med 6(7):1–14CrossRefGoogle Scholar
  101. Wang T, Hu X, Liang S, Li W, Wu X, Wang L, Jin F (2015) Lactobacillus fermentum NS9 restores the antibiotic induced physiological and psychological abnormalities in rats. Benef Microbes 6:707–717PubMedCrossRefGoogle Scholar
  102. Wang Y, Wang Z, Wang Y, Li F, Jia J, Song X, Qin S, Wang R, Jin F, Kitazato K, Wang Y (2018) The gut miroglia connection: implications for central nervous system diseases. Front Immunol 9:2325PubMedPubMedCentralCrossRefGoogle Scholar
  103. Woodmansey EJ (2007) Intestinal bacteria and ageing. J Appl Microbiol 102:1178–1186PubMedCrossRefGoogle Scholar
  104. Xu R, Wang QQ (2016) Towards understanding brain-gut-microbiome connections in Alzheimer’s disease. BMC Syst Biol 10(Suppl 3)Google Scholar
  105. Zhao Y, Jaber V, Lukiw WJ (2017a) Secretory products of the human GI tract microbiome and their potential impact on Alzheimer’s disease (AD): detection of Lipopolysaccharide (LPS) in AD hippocampus. Front Cell Infect Microbiol 7(July):1–9Google Scholar
  106. Zhao Y, Cong L, Lukiw WJ (2017b) Lipopolysaccharide (LPS) accumulates in neocortical neurons of Alzheimer’s disease (AD) brain and impairs transcription in human neuronal-glial primary co-cultures. Front Aging Neurosci 9(December):1–9Google Scholar
  107. Zhao Y, Cong L, Jaber V, Lukiw WJ (2017c) Microbiome-derived lipopolysaccharide enriched in the perinuclear region of Alzheimer’s disease brain. Front Immunol 8(September):1–6Google Scholar
  108. Zhou Y, Smith D, Leong BJ, Brännström K, Almqvist F, Chapman MR (2012) Promiscuous cross-seeding between bacterial amyloids promotes interspecies biofilms. J Biol Chem 287(42):35092–35103PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Amira Benmelouka
    • 1
  • Ahmed M. Sherif
    • 2
  • Mahmoud Ahmed Ebada
    • 2
    Email author
  1. 1.University of AlgiersSidi M’HamedAlgeria
  2. 2.Faculty of MedicineZagazig UniversityZagazigEgypt

Personalised recommendations