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Role of Microbiota in Neurodegenerative Diseases

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Abstract

Functional interaction of the gastrointestinal tract (GI) and the central nervous system (CNS) is due to various relationships, which includes autonomic and enteral nervous systems as well as the immune and neuroendocrine systems. The microbiota of the macroorganism plays the central role in this interaction. Microbiota produces hundreds of biologically active substances that have a neurochemical effects through neuroendocrine, immune, and metabolic pathways. The microbiota also synthesizes and releases products (neurotoxins, neurotransmitters, lipopolysaccharides, amyloids, etc.) that can negatively affect the neurochemistry of the CNS, stimulating the development of amyloidosis, synucleinopathies, and tauopathies, thereby promoting the development and/or progression of neurodegenerative diseases. Under the influence of external and internal factors, human microbiota can be changed and the symbionts/pathogens ratio is also changed. The permeability of intestinal and blood-brain barrier varies. Metabolites produced by the altered microflora are able to enter the bloodstream and possibly into the CNS, thereby disrupting its functioning. Infections can play a significant role and even act as a cofactor in the induction of neurodegenerative diseases. Disturbance of the functions of the GI can precede long before the neurodegenerative processes. Early diagnosis, detection, monitoring, and treatment of negative gastrointestinal symptoms, including normalization of the microbiota, can lead to a significant improvement in the quality of life of patients with neurodegenerative diseases.

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REFERENCES

  1. Agostini, S., Clerici, M., and Mancuso, R., How plausible is a link between HSV-1 and AD?, Expert Rev. Anti. Infect. Ther., 2014, vol. 12, pp. 275–278. doi 10.1586/ 14787210.2014.887442

    Article  CAS  PubMed  Google Scholar 

  2. Albenberg, L.G. and Wu, G.D., Diet and the intestinal microbiome: associations, functions, and implications for health and disease, Gastroenterology, 2014, vol. 146, no. 6, pp. 1564–1572. doi 10.1053/j.gastro.2014.01.058

    Article  CAS  PubMed  Google Scholar 

  3. Allen, K.D., Wegrzyn, R.D., Chernova, T.A., et al., Hsp70 chaperones as modulators of prion life cycle: novel effects of Ssa and Ssb on the Saccharomyces cerevisiae prion [PSI+], Genetics, 2005, vol. 169, no. 3, pp. 1227–1242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Alonso, R., Pisa, D., Marina, A.I., et al., Fungal infection in patients with Alzheimer’s disease, J. Alzheimers Dis., 2014, vol. 41, pp. 301–311. doi 10.3233/JAD-132681

  5. Álvarez, G., Aldudo, J., Alonso, M., et al., Herpes simplex virus type 1 induces nuclear accumulation of hyperphosphorylated tau in neuronal cells, J. Neurosci. Res., 2012, vol. 90, no. 5, pp. 1020–1029.

    Article  CAS  PubMed  Google Scholar 

  6. Arroyo, D.S., Soria, J.A., Gaviglio, E.A., et al., Toll-like receptors are key players in neurodegeneration, Int. Immunopharmacol., 2011, vol. 11, no. 10, pp. 1415–1421. doi 10.1016/j.intimp.2011.05.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Asti, A. and Gioglio, L., Can a bacterial endotoxin be a key factor in the kinetics of amyloid fibril formation?, J. Alzheimer’s Dis., 2014, vol. 39, no. 1, pp. 169–179. doi 10.3233/JAD-131394

    Article  CAS  Google Scholar 

  8. Aziz, Q., Doré, J., Emmanuel, A., Guarner, F., and Quigley, E.M., Gut microbiota and gastrointestinal health: current concepts and future directions, Neurogastroenterol. Motil., 2013, vol. 25, pp. 4–15. doi 10.1111/nmo.12046

    Article  CAS  PubMed  Google Scholar 

  9. Backhed, F., Ley, R.E., Sonnenburg, J.L., et al., Host–acterial mutualism in the human intestine, Science, 2005, vol. 307, pp. 1915–1920. doi 10.1126/science.1104816

    Article  CAS  PubMed  Google Scholar 

  10. Ball, M.J., Lukiw, W.J., Kammerman, E.M., and Hill, J.M., Intracerebral propagation of Alzheimer’s disease: strengthening evidence of a herpes simplex virus etiology, Alzheimer’s Dement., 2013, vol. 9, pp. 169–175. doi 10.1016/j.jalz.2012.07.005

  11. Barajon, I., Serrao, G., Arnaboldi, F., et al., Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia, J. Histochem. Cytochem., 2009, vol. 57, no. 11, pp. 1013–1023. doi 10.1369/jhc.2009.953539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Barrett, E., Ross, R.P., O’Toole, P.W., et al., γ-Aminobutyric acid production by culturable bacteria from the human intestine, J. Appl. Microbiol., 2012, vol. 113, pp. 411–417. doi 10.1111/j.1365-2672.2012.05344.x

    Article  CAS  PubMed  Google Scholar 

  13. Berer, K., Mues, M., Koutrolos, M., et al., Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination, Nature, 2011, vol. 479, no. 7374, pp. 538–541. doi 10.1038/nature10554

    Article  CAS  PubMed  Google Scholar 

  14. Bhattacharjee, S. and Lukiw, W.J., Alzheimer’s disease and the microbiome, Front. Cell Neurosci., 2013, vol. 7, p. 153. doi 10.3389/fncel.2013.00153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bojarski, L., Herms, J., and Kuznicki, J., Calcium dysregulation in Alzheimer’s disease, Neurochem. Int., 2008, vol. 52, nos. 4–5, pp. 621–633.

    Article  CAS  PubMed  Google Scholar 

  16. Borjabad, A. and Volsky, D.J., Common transcriptional signatures in brain from patients with HIV-associated neurocognitive disorders, Alzheimer’s, and multiple sclerosis, J. Neuroimmune Pharmacol., 2012, vol. 7, pp. 914–926. doi 10.1007/s11481-012-9409-5

    Article  PubMed  PubMed Central  Google Scholar 

  17. Bowery, N.G., Bagetta, G., and Nistico, G., Intrahippocampal tetanus toxin produces generalized convulsions and neurodegeneration in rats: antagonism by NMDA receptor blockers, Epilepsy Res. Suppl., 1992, vol. 9, pp. 249–256.

    CAS  PubMed  Google Scholar 

  18. Bowma, C.C., Rasley, A., Tranguch, S.L., and Marriott, I., Cultured astrocytes express toll-like receptors for bacterial products, Glia, 2003, vol. 43, pp. 281–291.

    Article  Google Scholar 

  19. Braak, H., Rüb, U., Gai, W.P., and Del Tredici, K., Idiopathic Parkinson’s disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen, J. Neural Transm. (Vienna), 2003, vol. 110, no. 5, pp. 517–536.

    Article  CAS  Google Scholar 

  20. Bradley, W.G. and Mash, D.C., Beyond Guam: the cyanobacteria/BMAA hypothesis of the cause of ALS and other neurodegenerative diseases, Amyotroph. Lateral Scler., 2009, vol. 10, suppl. 2, pp. 7–20. doi 10.3109/ 17482960903286009

    Article  CAS  PubMed  Google Scholar 

  21. Braniste, V., Al-Asmakh, M., Kowal, C., et al., The gut microbiota influences blood-brain barrier permeability in mice, Sci. Transl. Med., 2014, vol. 6, p. 263ra158.

  22. Branton, W.G., Lu, J.Q., Surette, M.G., et al., Brain microbiota disruption within inflammatory demyelinating lesions in multiple sclerosis, Sci. Rep., 2016, vol. 6, p. 37344. doi 10.1038/srep37344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bravo, J.A., Forsythe, P., Chew, M.V., et al., 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., 2011, vol. 108, no. 38, pp. 16050–16055. doi 10.1073/pnas.1102999108

    Article  PubMed  PubMed Central  Google Scholar 

  24. Bravo, J.A., Julio-Pieper, M., Forsythe, P., et al., Communication between gastrointestinal bacteria and the nervous system, Curr. Opin. Pharmacol., 2012, vol. 12, no. 6, pp. 667–672. doi 10.1016/j.coph.2012.09.010

    Article  CAS  PubMed  Google Scholar 

  25. Brenner, S.R., Blue-green algae or cyanobacteria in the intestinal microflora 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 Parkinsons-Dementia-Complex in humans and Equine Motor Neuron Disease in horses, Med. Hypotheses, 2013, vol. 80, pp. 103–108. doi 10.1016/j.mehy.2012.10.010

    Article  CAS  PubMed  Google Scholar 

  26. Brew, B.J., Robertson, K., and Wright, E.J., HIV eradication symposium: will the brain be left behind?, J. Neurovirol., 2015, vol. 21, no. 3, pp. 322–334. http://dx.doi.org/ 10.1007/s13365-015-0322-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Camfield, D.A., Owen, L., Scholey, A.B., et al., Dairy constituents and neurocognitive health in ageing, Br. J. Nutr., 2011, vol. 106, pp. 159–174. doi 10.1017/ S0007114511000158

    Article  CAS  PubMed  Google Scholar 

  28. Carlino, D., DeVanna, M., and Tongiorgi, E., Is altered BDNF biosynthesis a general feature in patients with cognitive dysfunction?, Neuroscientist, 2013, vol. 19, pp. 345–353. doi 10.1177/1073858412469444

    Article  CAS  PubMed  Google Scholar 

  29. Carter, C.J., Alzheimer’s disease: a pathogenetic autoimmune disorder caused by herpes simplex in a gene-dependent manner, Int. J. Alzheimers Dis., 2010, p. 140539. doi 10.4061/2010/140539

  30. Carty, M. and Bowie, A.G., Evaluating the role of toll-like receptors in diseases of the central nervous system, Biochem. Pharmacol., 2011, vol. 81, no. 7, pp. 825–837. doi 10.1016/j.bcp.2011.01.003

    Article  CAS  PubMed  Google Scholar 

  31. Chen, B., Soto, C., and Morales, R., Peripherally administrated prions reach the brain at sub-infectious quantities, FEBS Lett., 2014, vol. 588, pp. 795–800. doi 10.1016/j.febslet.2014.01.038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Chiu, A.S., Gehringer, M.M., and Braidy, N., Gliotoxicity of the cyanotoxin, β-methyl-amino-L-alanine (BMAA), Sci. Rep., 2013, vol. 3, p. 1482. doi 10.1038/srep01482

  33. Chiu, W.C., Tsan, Y.T., Tsai, S.L., et al., Hepatitis C viral infection and the risk of dementia, Eur. J. Neurol., 2013, vol. 21, no. 8, p. 1068-e59. doi 10.1111/ene.12317

  34. Cho, I. and Blaser, M.J., The human microbiome: at the interface of health and disease, Nat. Rev. Genet., 2012, vol. 13, pp. 260–270. doi 10.1038/nrg3182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Churchill, M.J., Wesselingh, S.L., and Cowley, D., Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia, Ann. Neurol., 2009, vol. 66, no. 2, pp. 253–258. http://dx.doi.org/ 10.1002/ana.21697.

    Article  PubMed  Google Scholar 

  36. Clarke, G., Stilling, R.M., Kennedy, P.J., et al., Gut microbiota: the neglected endocrine organ, Mol. Endocrinol., 2014, vol. 28, pp. 1221–1238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Cox, P.A., Banack, S.A., and Murch, S.J., Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam, Proc. Natl. Acad. Sci. U. S. A., 2003, vol. 100, no. 23, pp. 13380–13383.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Cox, P.A., Davis, D.A., Mash, D.C., et al., Dietary exposure to an environmental toxin triggers neurofibrillary tangles and amyloid deposits in the brain, Proc. Biol. Sci., 2016, vol. 283, no. 1823, p. 20152397. doi 10.1098/rspb.2015.2397

  39. Cribbs, D.H., Azizeh, B.Y., Cotman, C.W., and Laferla, F.M., Fibril formation and neurotoxicity by a herpes simplex virus glycoprotein B fragment with homology to the Alzheimer’s Aβ peptide, Biochemistry, 2000, vol. 39, pp. 5988–5994.

    Article  CAS  PubMed  Google Scholar 

  40. Dasari, M., Espargaro, A., Sabate, R., et al., Bacterial inclusion bodies of Alzheimer’s disease β-amyloid peptides can be employed to study native-like aggregation intermediate states, Chembiochem, 2011, vol. 12, pp. 407–423.

    Article  CAS  PubMed  Google Scholar 

  41. Derkinderen, P., Rouaud, T., Lebouvier, T., et al., Parkinson disease: the enteric nervous system spills its guts, Neurology, 2011, vol. 77, pp. 1761–1767. doi 10.1212/ WNL.0b013e318236ef60

    Article  CAS  PubMed  Google Scholar 

  42. Devos, D., Lebouvier, T., Lardeux, B., et al., Colonic inflammation in Parkinson’s disease, Neurobiol. Dis., 2013, vol. 50, pp. 42–48.

    Article  CAS  PubMed  Google Scholar 

  43. Diaz Heijtz, R., Wang, S., Anuar, F., et al., Normal gut microbiota modulates brain development and behavior, Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, pp. 3047–3052. doi 10.1073/pnas.1010529108

    Article  PubMed  Google Scholar 

  44. Dickens, A.M., Yoo, S.W., Chin, A.C., et al., Chronic low-level expression of hiv-1 tat promotes a neurodegenerative phenotype with aging, Sci. Rep., 2017, vol. 7, p. 7748. doi 10.1038/s41598-017-07570-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Dinan, T.G. and Cryan, J.F., Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration, J. Physiol., 2017, vol. 595, no. 2, pp. 489–503. doi 10.1113/JP273106

    Article  CAS  PubMed  Google Scholar 

  46. Douglas-Escobar, M., Elliott, E., and Neu, J., Effect of intestinal microbial ecology on the developing brain, JAMA Pediatr., 2013, vol. 167, pp. 374–379. doi 10.1001/jamapediatrics.2013.497

    Article  PubMed  Google Scholar 

  47. Dreses-Werringloer, U., Lambert, J.C., Vingtdeux, V., et al., A polymorphism in CALHM1 influences Ca2+ homeostasis, Abeta levels, and Alzheimer’s disease risk, Cell, 2008, vol. 133, no. 7, pp. 1149–1161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Dunlop, R.A., Cox, P.A., Banack, S.A., and Rodgers, J.K., The non-protein amino acid BMAA is misincorporated into human proteins in place of L-serine causing protein misfolding and aggregation, PLoS One, 2013, vol. 8, no. 9. e75376. doi 10.1371/journal.pone.0075376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Eisenhofer, G., Aneman, A., Friberg, P., et al., Substantial production of dopamine in the human gastrointestinal tract, J. Clin. Endocrinol. Metab., 1997, vol. 82, pp. 3864–3871.

    Article  CAS  PubMed  Google Scholar 

  50. Foley, N.C., Affoo, R.H., and Martin, R.E., A systematic review and meta-analysis examining pneumonia-associated mortality in dementia, Dement. Geriatr. Cogn. Disord., 2015, vol. 39, nos. 1–2, pp. 52–67. doi 10.1159/000367783

    Article  PubMed  Google Scholar 

  51. Forsythe, P., Kunze, W.A., and Bienenstock, J., On communication between gut microbes and the brain, Curr. Opin. Gastroenterol., 2012, vol. 28, pp. 557–562. doi 10.1097/MOG.0b013e3283572ffa

    Article  PubMed  Google Scholar 

  52. Foster, J.A., Lyte, M., Meyer, E., and Cryan, J.F., Gut microbiota and brain function: an evolving field in neuroscience, Int. J. Neuropsychopharmacol., 2016, vol. 19. yv114. doi 10.1093/ijnp/pyv114

  53. Frye, R.E., Rose, S., Slattery, J., and MacFabe, D.F., Gastrointestinal dysfunction in autism spectrum disorder: the role of the mitochondria and the enteric microbiome, Microb. Ecol. Health Dis., 2015, vol. 26, p. 27458.

    PubMed  Google Scholar 

  54. Furness, J.B., Callaghan, B.P., Rivera, L.R., and Cho, H.J., The enteric nervous system and gastrointestinal innervation: integrated local and central control, Adv. Exp. Med. Biol., 2014, vol. 817, pp. 39–71. doi 10.1007/978-1-4939-0897-4_3

    Article  PubMed  Google Scholar 

  55. Galland, L., The gut microbiome and the brain, J. Med. Food, 2014, vol. 17, pp. 1261–1272.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Gao, B., Bian, X., Mahbub, R., and Lu, K., Sex-specific effects of organophosphate diazinon on the gut microbiome and its metabolic functions, Environ. Health Perspect., 2017, vol. 125, no. 2, pp. 198–206. doi 10.1289/ EHP202

    Article  CAS  PubMed  Google Scholar 

  57. von Geldern, G. and Mowry, E.M., The influence of nutritional factors on the prognosis of multiple sclerosis, Nat. Rev. Neurol., 2012, vol. 8, pp. 678–689. doi 10.1038/nrneurol.2012.194

    Article  CAS  PubMed  Google Scholar 

  58. Gibson, G.E. and Thakkar, A., Interactions of mitochondria/metabolism and calcium regulation in Alzheimer’s disease: a calcinist point of view, Neurochem. Res., 2017. doi 10.1007/s11064-017-2182-3

  59. Glass, C.K., Saijo, K., Winner, B., et al., Mechanisms underlying inflammation in neurodegeneration, Cell, 2010, vol. 140, no. 6, pp. 918–934. doi 10.1016/ j.cell.2010.02.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. González-Scarano, F. and Martín-García, J., The neuropathogenesis of AIDS, Nat. Rev. Immunol., 2005, vol. 5, no. 1, pp. 69–81. http://dx.doi.org/10.1038/nri1527.

    Article  CAS  PubMed  Google Scholar 

  61. van de Haar, H.J., Burgmans, S., Jansen, J.F., et al., Blood-brain barrier leakage in patients with early Alzheimer disease, Radiology, 2016, vol. 281, no. 2, pp. 527–535. doi 10.1148/radiol.2016152244

    Article  PubMed  Google Scholar 

  62. Hammond, C.J., Hallock, L.R., Howanski, R.J., et al., Immunohistological detection of Chlamydia pneumoniae in Alzheimer’s disease, BMC Neurosci., 2010, vol. 11, p. 121. doi 10.1186/1471-2202-11-121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Hanisch, U.K., Microglia as a source and target of cytokines, Glia, 2002, vol. 40, no. 2, pp. 140–155.

    Article  PubMed  Google Scholar 

  64. Hansen, M.B., The enteric nervous system I: organisation and classification, Pharmacol. Toxicol., 2003, vol. 92, no. 3, pp. 105–113. PMID 12753424

    Article  CAS  PubMed  Google Scholar 

  65. Harrington, P.R., Schnell, G., Letendre, S.L., et al., Cross-sectional characterization of HIV-1 env compartmentalization in cerebrospinal fluid over the full disease course, AIDS, 2009, vol. 23, no. 8, pp. 907–915. http://dx.doi.org/10.1097/QAD.0b013e3283299129.

    Article  PubMed  Google Scholar 

  66. Hattori, M. and Taylor, T.D., The human intestinal microbiome: a new frontier of human biology, DNA Res., 2009, vol. 16, pp. 1–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Heaton, R.K., Clifford, D.B., Franklin, D.R., Jr., et al., HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study, Neurology, 2010, vol. 75, no. 23, pp. 2087–2096. http://dx.doi.org/10.1212/WNL.0b013e318200d727.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Heintz, C. and Mair, W., You are what you host: microbiome modulation of the aging process, Cell, 2014, vol. 156, pp. 408–411. doi 10.1016/j.cell.2014.01.025

  69. Hernandez-Rapp, J., Martin-Lannerée, S., Hirsch, T.Z., et al., Hijacking PrP(c)-dependent signal transduction: when prions impair Aβ clearance, Front. Aging Neurosci., 2014, vol. 6, p. 25. doi 10.3389/fnagi.2014.00025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Hill, J.M. and Lukiw, W.J., Comparing miRNAs and viroids; highly conserved molecular mechanisms for the transmission of genetic information, Front. Cell Neurosci., 2014, vol. 8, p. 45. doi 10.3389/fncel.2014.00045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Hill, J.M. and Lukiw, W.J., Microbial-generated amyloids and Alzheimer’s disease (AD), Front. Aging Neurosci., 2015, vol. 7, p. 9. doi 10.3389/fnagi.2015.00009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Hill, J.M., Zhao, Y., Clement, C., et al., HSV-1 infection of human brain cells induces miRNA-146a and Alzheimer-type inflammatory signaling, Neuroreport, 2009, vol. 20, pp. 1500–1505. doi 10.1097/WNR.0b013e3283329c05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Hill, J.M., Clement, C., and Pogue, A.I., Pathogenic microbes, the microbiome, and Alzheimer’s disease (AD), Front. Aging Neurosci., 2014, vol. 6, p. 127. doi 10.3389/fnagi.2014.00127

    PubMed  PubMed Central  Google Scholar 

  74. Holmqvist, S., Chutna, O., Bousset, L., et al., Direct evidence of Parkinson pathology spread from the gastrointestinal tract to the brain in rats, Acta Neuropathol., 2014, vol. 128, no. 6, pp. 805–820. doi 10.1007/s00401-014-1343-6

    Article  PubMed  Google Scholar 

  75. Holtcamp, W., The emerging science of BMAA: do cyanobacteria contribute to neurodegenerative disease?, Environ. Health. Perspect., 2012, vol. 120, no. 3, pp. A110–A116. doi 10.1289/ehp.120-a110

    PubMed  PubMed Central  Google Scholar 

  76. Holzer, P. and Farzi, A., Neuropeptides and the microbiota–gut–brain axis, in Microbial Endocrinology: The Microbiota-Gut-Brain Axis in Health and Disease, Lyte, M. and Cryan, J.F., Eds., Adv. Exp. Med. Biol., New York: Springer, 2014, vol. 817, pp. 195–219.

  77. Hornig, M., The role of microbes and autoimmunity in the pathogenesis of neuropsychiatric illness, Curr. Opin. Rheumatol., 2013, vol. 25, pp. 488–795. doi 10.1097/ BOR.0b013e32836208de

    Article  CAS  PubMed  Google Scholar 

  78. Huang, W.S., Yang, T.Y., Shen, W.C., et al., Association between Helicobacter pylori infection and dementia, J. Clin. Neurosci., 2014, vol. 21, no. 8, pp. 1355–1358. doi 10.1016/j.jocn.2013.11.018

    Article  CAS  PubMed  Google Scholar 

  79. Jangi, S., Gandhi, R., Cox, L.M., et al., Alterations of the human gut microbiome in multiple sclerosis, Nat. Commun., 2016, vol. 7, p. 12015. doi 10.1038/ncomms12015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Kannarkat, G.T., Boss, J.M., and Tansey, M.G., The role of innate and adaptive immunity in Parkinson’s disease, J. Parkinsons Dis., 2013, vol. 3, pp. 493–514.

    PubMed  PubMed Central  Google Scholar 

  81. Karlsson, O., Berg, A.L., Hanrieder, J., et al., Intracellular fibril formation, calcification, and enrichment of chaperones, cytoskeletal, and intermediate filament proteins in the adult hippocampus CA1 following neonatal exposure to the nonprotein amino acid BMAA, Arch. Toxicol., 2015, vol. 89, no. 3, pp. 423–436. doi 10.1007/ s00204-014-1262-2

  82. Kelly, J.R., Allen, A.P., Temko, A., et al., Lost in translation? The potential psychobiotic Lactobacillus rhamnosus (JB-1) fails to modulate stress or cognitive performance in healthy male subjects, Brain Behav. Immun., 2017, vol. 61, pp. 50–59. doi 10.1016/j.bbi.2016.11.018

    Article  CAS  PubMed  Google Scholar 

  83. Kielian, T., Toll-like receptors in central nervous system glial inflammation and homeostasis, J. Neurosci. Res., 2006, vol. 83, no. 5, pp. 711–730.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Kim, J.S. and Sung, H.Y., Gastrointestinal autonomic dysfunction in patients with Parkinson’s disease, J. Mov. Disord., 2015, vol. 8, no. 2, pp. 76–82. doi 10.14802/jmd.15008

    Article  PubMed  PubMed Central  Google Scholar 

  85. Kim, H.S., Lee, J.H., Lee, J.P., et al., Amyloid beta peptide induces cytochrome c release from isolated mitochondria, Neuroreport, 2002, vol. 13, pp. 1989–1993.

    Article  CAS  PubMed  Google Scholar 

  86. Kim, B.S., Jeon, Y.S., and Chun, J., Current status and future promise of the human microbiome, Pediatr. Gastroenterol. Hepatol. Nutr., 2013, vol. 16, pp. 71–79. doi 10.5223/pghn.2013.16.2.71

    Article  PubMed  PubMed Central  Google Scholar 

  87. König, J., Wells, J., Cani, P.D., et al., Human intestinal barrier function in health and disease. Clin. Transl. Gastroenterol., 2016, vol. 7, no. 10. e196. doi 10.1038/ctg.2016.54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Kountouras, J., Tsolaki, M., Gavalas, E., et al., Relationship between Helicobacter pylori infection and Alzheimer disease, Neurology, 2006, vol. 66, pp. 938–940.

    Article  CAS  PubMed  Google Scholar 

  89. Kountouras, J., Boziki, M., Gavalas, E., et al., Five-year survival after Helicobacter pylori eradication in Alzheimer disease patients, Cogn. Behav. Neurol., 2010, vol. 23, no. 3, pp. 199–204. doi 10.1097/WNN.0b013e3181df3034

    Article  PubMed  Google Scholar 

  90. Kramer-Hämmerle, S., Rothenaigner, I., Wolff, H., et al., Cells of the central nervous system as targets and reservoirs of the human immunodeficiency virus, Virus Res., 2005, vol. 111, no. 2, pp. 194–213. http://dx.doi.org/ 10.1016/j.virusres. 2005.04.009. PMID: 15885841.

  91. Krogh, K.A., Lyddon, E., and Thayer, S.A., HIV-1 Tat activates a RhoA signaling pathway to reduce NMDA evoked calcium responses in hippocampal neurons via an actin-dependent mechanism, J. Neurochem., 2015, vol. 132, no. 3, pp. 354–366. http://dx.doi.org/10.1111/jnc.12936.

    Article  CAS  PubMed  Google Scholar 

  92. Laferla, F.M., Calcium dyshomeostasis and intracellular signalling in Alzheimer’s disease, Nat. Rev. Neurosci., 2002, vol. 3, pp. 862–872.

    Article  CAS  PubMed  Google Scholar 

  93. Lakhan, S.E., Caro, M., and Hadzimichalis, N., NMDA receptor activity in neuropsychiatric disorders, Front. Psychiatry, 2013, vol. 4, pp. 52–55. doi 10.3389/ fpsyt.2013.00052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Lehnardt, S., Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury, Glia, 2010, vol. 58, no. 3, pp. 253–263. doi 10.1002/glia.20928

    PubMed  Google Scholar 

  95. Letenneur, L., Peres, K., Fleury, H., et al., Seropositivity to herpes simplex virus antibodies and risk of Alzheimer’s disease: a population-based cohort study, PLoS One, 2008, vol. 3. e3637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Licastro, F., Porcellini, E., Caruso, C., et al., Genetic risk profiles for Alzheimer’s disease: integration of APOE genotype and variants that up-regulate inflammation, Neurobiol. Aging, 2007, vol. 28, pp. 1637–1643.

    Article  CAS  PubMed  Google Scholar 

  97. Liu, M. and Bing, G., Lipopolysaccharide animal models for Parkinson’s disease, Parkinsons Dis., 2011, vol. 2011, p. 327089. doi 10.4061/2011/327089

    PubMed  PubMed Central  Google Scholar 

  98. Lobner, D., Piana, P.M., Salous, A.K., and Peoples, R.W., Beta-N-methylamino-L-alanine enhances neurotoxicity through multiple mechanisms, Neurobiol Dis., 2007, vol. 25, no. 2, pp. 360–366.

    Article  CAS  PubMed  Google Scholar 

  99. Lu, B., Nagappan, G., Guan, X., et al., BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases, Nat. Rev. Neurosci., 2013, vol. 14, pp. 401–416. doi 10.1038/nrn3505

    Article  CAS  PubMed  Google Scholar 

  100. Lukiw, W.J., Bacteroides fragilis lipopolysaccharide and inflammatory signaling in Alzheimer’s disease, Front. Microbiol., 2016, vol. 7, p. 1544. eCollection 2016.

  101. Lyte, M., Microbial endocrinology in the microbiome–gut–rain axis: how bacterial production and utilization of neurochemicals influence behavior, PLoS Pathog., 2013, vol. 9, no. 11. e1003726. doi 10.1371/journal.ppat.1003726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Lyte, M. and Cryan, J.F., Microbial Endocrinology: The Microbiota–Gut–Brain Axis in Health and Disease, Adv. Exp. Med. Biol., New York: Springer, 2014, vol. 817.

    Book  Google Scholar 

  103. MacFabe, D.F., Cain, D.P., Rodriguez-Capote, K., et al., Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders, Behav. Brain Res., 2007, vol. 176, pp. 47–54. doi 10.1016/j.bbr.2010.10.005

    Article  CAS  Google Scholar 

  104. MacFabe, D.F., Cain, N.E., Boon, F., et al., Effects of the enteric bacterial metabolic product propionic acid on object-directed behavior, social behavior, cognition, and neuroinflammation in adolescent rats: relevance to autism spectrum disorder, Behav. Brain Res., 2011, vol. 217, no. 1, pp. 149–169. doi 10.1016/j.bbr.2006.07.025

    Article  CAS  Google Scholar 

  105. Malaguarnera, M., Bella, R., Alagona, G., et al., Helicobacter pylori and Alzheimer’s disease: a possible link, Eur. J. Int. Med., 2004, vol. 15, pp. 381–386.

    Article  Google Scholar 

  106. Manabe, T., Mizukami, K., Akatsu, H., et al., Influence of pneumonia complications on the prognosis of patients with autopsy-confirmed Alzheimer’s disease, dementia with Lewy bodies, and vascular dementia, Psychogeriatrics, 2016, vol. 16, no. 5, pp. 305–314. doi 10.1111/psyg.12163

    Article  PubMed  Google Scholar 

  107. Mancuso, R., Baglio, F., Cabinio, M., et al., Titers of HSV-1 antibodies correlate with grey matter volumes in AD, J. Alzheimers Dis., 2014, vol. 38, no. 4, pp. 741–745. doi 10.3233/JAD-130977

    Article  CAS  PubMed  Google Scholar 

  108. Manuelidis, L., Infectious particles, stress, and induced prion amyloids: a unifying perspective, Virulence, 2013, vol. 4, pp. 373–383. doi 10.4161/viru.24838

    Article  PubMed  PubMed Central  Google Scholar 

  109. Marques, F., Sousa, J.C., Sousa, N., and Palha, J.A., Blood–brain-barriers in aging and in Alzheimer’s disease, Mol. Neurodegener., 2013, vol. 8, p. 38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Maruszak, A., Pilarski, A., Murphy, T., et al., Hippocampal neurogenesis in Alzheimer’s disease: is there a role for dietary modulation?, J. Alzheimers Dis., 2014, vol. 38, pp. 11–38.

    Article  CAS  PubMed  Google Scholar 

  111. Matsumoto, M., Kibe, R. Ooga, T., et al., Cerebral low-molecular metabolites influenced by intestinal microbiota: a pilot study, Front. Syst. Neurosci., 2013, vol. 7, p. 9. doi 10.3389/fnsys.2013.00009

    Article  PubMed  PubMed Central  Google Scholar 

  112. Mattson, M.P., Cheng, B., Davis, D., et al., Beta-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity, J. Neurosci., 1992, vol. 12, no. 2, pp. 376–389.

  113. Mattson, M.P., Infectious agents and age-related neurodegenerative disorders, Ageing Res. Rev., 2004, vol. 3, pp. 105–120.

    Article  PubMed  Google Scholar 

  114. Mayer, E.A., Knight, R., Mazmanian, S.K., et al., Gut microbes and the brain: paradigm shift in neuroscience, J. Neurosci., 2014, vol. 34, no. 46, pp. 15490–15496. doi 10.1523/JNEUROSCI.3299-14.2014

    Article  PubMed  PubMed Central  Google Scholar 

  115. Mayer, E.A., Tillisch, K., and Gupta, A., Gut/brain axis and the microbiota, J. Clin. Invest., 2015, vol. 125, no. 3, pp. 926–938. doi 10.1172/JCI76304

    Article  PubMed  PubMed Central  Google Scholar 

  116. McKimmie, C.S., Johnson, N., Fooks, A.R., and Fazakerley, J.K., Viruses selectively upregulate Toll-like receptors in the central nervous system, Biochem. Biophys. Res. Commun., 2005, vol. 336, pp. 925–933.

    Article  CAS  PubMed  Google Scholar 

  117. McNaught, K.S., Perl, D.P., Brownell, A.L., and Olanow, C.W., Systemic exposure to proteasome inhibitors causes a progressive model of Parkinson’s disease, Ann. Neurol., 2004, vol. 56, no. 1, pp. 149–162.

    Article  CAS  PubMed  Google Scholar 

  118. McVey, NeufeldK.A., Mao, Y.K., Bienenstock, J., et al., The microbiome is essential for normal gut intrinsic primary afferent neuron excitability in the mouse, Neurogastroenterol. Motil., 2013, vol. 25, pp. 183–188. doi 10.1111/nmo.12049

  119. Miklossy, J., Emerging role of pathogens in Alzheimer’s disease, Expert. Rev. Mol. Med., 2011, vol. 13. e30. doi 10.1017/S1462399411002006

    Article  CAS  PubMed  Google Scholar 

  120. Minter, M.R., Taylor, J.M., and Crack, P.J., The contribution of neuroinflammation to amyloid toxicity in Alzheimer’s disease, J. Neurochem., 2016, vol. 136, no. 3, pp. 457–474. doi 10.1111/jnc.13411

    Article  CAS  PubMed  Google Scholar 

  121. Mitew, S., Kirkcaldie, M.T., Dickson, T.C., and Vickers, J.C., Altered synapses and gliotransmission in Alzheimer’s disease and ad model mice, Neurobiol. Aging, 2013, vol. 34, pp. 2341–2351. doi 10.1016/j.neurobiolaging.2013.04.010

    Article  CAS  PubMed  Google Scholar 

  122. Montagne, A., Barnes, S.R., Sweeney, M.D., et al., Blood–brain barrier breakdown in the aging human hippocampus, Neuron, 2015, vol. 85, no. 2, pp. 296–302. doi 10.1016/j.neuron.2014.12.032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Moulignier, A., Gueguen, A., Lescure, F.X., et al., Does HIV infection alter Parkinson disease?, J. Acquir. Immune Defic. Syndr., 2015, vol. 70, no. 2, pp. 129–136. http://dx.doi.org/10.1097/QAI.0000000000000677.

    Article  CAS  PubMed  Google Scholar 

  124. Mulligan, V.K. and Chakrabartty, A., Protein misfolding in the late-onset neurodegenerative diseases: common themes and the unique case of amyotrophic lateral sclerosis, Proteins, 2013, vol. 81, pp. 1285–1303. doi 10.1002/prot.24285

    Article  CAS  PubMed  Google Scholar 

  125. Obata, Y. and Pachnis, V., The effect of microbiota and the immune system on the development and organization of the enteric nervous system, Gastroenterology, 2016, vol. 151, no. 5, pp. 836–844. doi 10.10153/j.gastro.2016.07.044

    Article  CAS  PubMed  Google Scholar 

  126. Oh, S.H., Kim, H.N., Park, H.J., et al., Mesenchymal stem cells increase hippocampal neurogenesis and neuronal differentiation by enhancing the wnt signaling pathway in an Alzheimer’s disease model, Cell Transplant., 2015, vol. 24, pp. 1097–1109.

    Article  PubMed  Google Scholar 

  127. Oleskin, A.V. and Shenderov, B.A., Neuromodulatory effects and targets of the SCFAs and gasotransmitters produced by the human symbiotic microbiota, Microb. Ecol. Health Dis., 2016, vol. 27, p. 30971.

    PubMed  Google Scholar 

  128. Oleskin, A.V., El’-Registan, G.I., and Shenderov, B.A., Role of neuromediators in the functioning of the human microbiota: “business talks” among microorganisms and the microbiota–host dialogue, Microbiology (Moscow), 2016, vol. 85, no. 1, pp. 1–22.

    Article  CAS  Google Scholar 

  129. Pablo, J., Banack, S.A., Cox, P.A., et al., Cyanobacterial neurotoxin BMAA in ALS and Alzheimer’s disease, Acta Neurologica Scandinavica, 2009, vol. 120, no. 4, pp. 216–225. doi 10.1111/j.1600-0404.2008.01150.x

    Article  CAS  PubMed  Google Scholar 

  130. Parashar, A. and Udayabanu, M., Gut microbiota: implications in Parkinson’s disease, Parkinsonism Relat. Disord., 2017, vol. 38, pp. 1–7. doi 10.1016/j.parkreldis.2017.02.002

    Article  PubMed  PubMed Central  Google Scholar 

  131. Prandota, J., Possible link between Toxoplasma gondii and the anosmia associated with neurodegenerative diseases, Am. J. Alzheimers Dis. Other Demen., 2014, vol. 29, pp. 205–214. doi 10.1177/1533317513517049

    Article  PubMed  Google Scholar 

  132. Prusiner, S.B., Biology and genetics of prions causing neurodegeneration, Ann. Rev. Genet., 2013, vol. 47, pp. 601–623. doi 10.1146/annurev-genet-110711-155524

    Article  CAS  PubMed  Google Scholar 

  133. Putney, J.W., Jr., Presenilins, Alzheimer’s disease, and capacitative calcium entry, Neuron, 2000, vol. 27, no. 3, pp. 411–412.

    Article  CAS  PubMed  Google Scholar 

  134. Rao, S.D., Banack, S.A., Cox, P.A., and Weiss, J.H., BMAA selectively injures motor neurons via AMPA/kainate receptor activations. Exp. Neurol., 2006, vol. 201, no. 1, pp. 244–252. doi 10.1016/j.expneurol.2006.04.017

    Article  CAS  PubMed  Google Scholar 

  135. Rhee, S.H., Pothoulakis, C., and Mayer, E.A., Principles and clinical implications of the brain–gut–enteric microbiota axis, Nat. Rev. Gastroenterol. Hepatol., 2009, vol. 6, no. 5, pp. 306–314. doi 10.1038/nrgastro.2009.35

    Article  CAS  PubMed  Google Scholar 

  136. Ritz, B.R., Paul, K.C., and Bronstein, J.M., Of pesticides and men: a California story of genes and environment in Parkinson’s disease, Curr. Environ. Health Rep., 2016, vol. 3, pp. 40–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Rivest, S., Regulation of innate immune responses in the brain, Nat. Rev. Immunol., 2009, vol. 9, pp. 429–439.

    Article  CAS  PubMed  Google Scholar 

  138. Sabatier, J.M., Vives, E., Mabrouk, K., et al., Evidence for neurotoxic activity of tat from human immunodeficiency virus type 1, J. Virol., 1991, vol. 65, pp. 961–967.

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Sampson, T.R., Debelius, J.W., Thron, T., et al., Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson’s disease, Cell, 2016, vol. 167, no. 6, pp. 1469–1480. doi 10.1016/ j.cell.2016.11.018

  140. Sanchez-Guajardo, V., Barnum, C.J., Tansey, M.G., and Romero-Ramos, M., Neuroimmunological processes in Parkinson’s disease and their relation to a-synuclein: microglia as the referee between neuronal processes and peripheral immunity, ASN Neuro, 2013, vol. 5, pp. 113–139.

    Article  CAS  PubMed  Google Scholar 

  141. Santana, S., Recuero, M., Bullido, M.J., et al., Herpes simplex virus type I induces the accumulation of intracellular beta-amyloid in autophagic compartments and the inhibition of the non-amyloidogenic pathway in human neuroblastoma cells, Neurobiol. Aging, 2012, vol. 33, no. 2, p. 430. e19–33

  142. Saulnier, D.M., Ringel, Y., Heyman, M.B., et al., The intestinal microbiome, probiotics and prebiotics in neurogastroenterology, Gut Microbes, 2013, vol. 4, no. 1, pp. 17–27. doi 10.4161/gmic.22973

    Article  PubMed  PubMed Central  Google Scholar 

  143. Di Scala, C., Yahi, N., Boutemeur, S., et al., Common molecular mechanism of amyloid pore formation by Alzheimer’s β-amyloid peptide and α -synuclein, Sci. Rep., 2016, vol. 6, p. 28781. doi 10.1038/srep28781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Schwartz, K. and Boles, B.R., Microbial amyloids-functions and interactions within the host, Curr. Opin. Microbiol., 2013, vol. 16, pp. 93–99. doi 10.1016/j.mib.2012.12.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Selkrig, J., Wong, P., Zhang, X., and Pettersson, S., Metabolic tinkering by the gut microbiome: implications for brain development and function, Gut Microbes, 2014, vol. 5, no. 3, pp. 369–380. doi 10.4161/gmic.28681

    Article  PubMed  PubMed Central  Google Scholar 

  146. Sharon, G., Sampson, T.R., Geschwind, D.H., and Mazmanian, S.K., The central nervous system and the gut microbiome, Cell, 2016, vol. 167, no. 4, pp. 915–932. doi 10.1016/j.cell.2016.10.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Shenderov, B.A., Probiotic (symbiotic) bacterial languages, Anaerobe, 2011, vol. 17, pp. 490–495.

    Article  CAS  PubMed  Google Scholar 

  148. Silei, V., Fabrizi, C., Venturini, G., et al., Activation of microglial cells by PrP and beta-amyloid fragments raises intracellular calcium through L-type voltage sensitive calcium channels, Brain Res., 1999, vol. 818, no. 1, pp. 168–170.

    Article  CAS  PubMed  Google Scholar 

  149. Smith, M.Z., Wightman, F., and Lewin, S.R., HIV reservoirs and strategies for eradication, Curr. HIV/AIDS. Rep., 2012, vol. 9, no. 1, pp. 5–15. http://dx.doi.org/ 10.1007/s11904-011-0108-2.

    Article  PubMed  Google Scholar 

  150. Sobol, C.V., Mikroflora i serdechno-sosudistaya sistema v norme i pri patologii (Microflora and the Cardiovascular System in Health and Disease), Lambert Academic Publishing, 2014.

    Google Scholar 

  151. Sobol., C.V., Antineoplastic and antimutagenic effects of a new probiotic product at the cellular level and in rats with transplanted fast-growing Pliss’ lymphosarcoma, Int. J. Probiot. Prebiot., 2015, vol. 10, pp. 133–144.

    Google Scholar 

  152. Sobol., C.V., A novel complementary approach using new probiotic product for the improvement of HIV therapy, in Frontiers in Clinical Drug Research-Anti Invectives, Atta-ur-Rahman, Ed., Sharjah, United Arab Emirates: Bentham Science Publishers, 2017a, vol. 3, pp. 49–121. https:// www.dropbox.com/s/4cykdoth8iuuyiu/9781681083698R. pdf?dl=0.

  153. Sobol, C.V., A new class of pharmabiotics with unique properties, in Soft Chemistry and Food Fermentation, Grumezescu, A.M. and Holban, A.M., Eds., Elsevier, 2017b, vol. 3, pp. 79–112. https://www.sciencedirect. com/science/article/pii/B9780128114124000047.

    Google Scholar 

  154. Sobol, C.V. and Belostotskaya, G.B., Product fermented by Lactobacilli induces changes in intracellular calcium dynamics in rat brain neurons, Biochemistry (Moscow) Suppl. Series A: Membr. Cell Biol., 2016, vol. 10, no. 1, pp. 37–45.

    Google Scholar 

  155. Sobol, C.V. and Sobol, Yu.Ts., Composition and method for producing and use of a fermented hydrolyzed medium containing microorganisms and products of their metabolism, US Patent no. 6953574, 2005.

  156. Sobol., C.V., Belostotskaya, G.B., and Kenworthy, M.W., Calcium signalling in rat brain neurons and differentiation of PC-12 cells induced by application of a probiotic product, Neurophysiology (Ukraine), 2005, vol. 37, pp. 284–293.

    Article  Google Scholar 

  157. Sobol, C.V., Korotkov, S.M., Belostotskaya, G.B., and Nesterov, V.P., The influence of probiotics and probiotic product on respiration of mitochondria and intracellular calcium signal in cells of cardiovascular system, Biochemistry (Moscow) Suppl. Series A: Membr. Cell Biol., 2013, vol. 7, no. 4, pp. 294–301.

    Google Scholar 

  158. Soret, R., Chevalier, J., De Coppet, P., et al., Short-chain fatty acids regulate the enteric neurons and control gastrointestinal motility in rats, Gastroenterology, 2010, vol. 138, no. 5, pp. 1772–1782. doi 10.1053/j.gastro.2010.01.053

    Article  CAS  PubMed  Google Scholar 

  159. Soscia, S.J., Kirby, J.E., Washicosky, K.J., et al., The Alzheimer’s disease-associated amyloid β-protein is an antimicrobial peptide, PLoS One, 2010, vol. 5. e9505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Suh, J., Sinclair, E., Peterson, J., et al., Progressive increase in central nervous system immune activation in untreated primary HIV-1 infection, J. Neuroinflammation, 2014, vol. 11, p. 199. http://dx.doi.org/10.1186/s12974-014-0199-y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Tkachenko, E.I. and Uspenskii, Yu.P., Pitanie, mikrobiotsenoz i intellekt cheloveka (Nutrition, Microbiocenosis, and Human Intelligence), St. Petersburg: SpetsLit, 2006.

    Google Scholar 

  162. Torbick, N., Hession, S., Stommel, E., and Caller, T., Mapping amyotrophic lateral sclerosis lake risk factors across northern New England, Int. J. Health Geogr., 2014, vol. 13, p. 1. doi 10.1186/1476-072X-13-1

    Article  PubMed  PubMed Central  Google Scholar 

  163. Tran, L. and Greenwood-Van Meerveld, B., Age-associated remodeling of the intestinal epithelial barrier, J. Gerontol. A Biol. Sci. Med. Sci., 2013, vol. 68, pp. 1045–1056. doi 10.1093/gerona/glt106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Del Tredici, K. and Braak, H., A not entirely benign procedure: progression of Parkinson’s disease, Acta Neuropathol., 2008, vol. 115, pp. 379–384.

    Article  PubMed  Google Scholar 

  165. Udit, S. and Gautron, L., Molecular anatomy of the gut-brain axis revealed with transgenic technologies: implications in metabolic research, Front. Neurosci., 2013, vol. 7, p. 134. doi 10.3389/fnins.2013.00134

    Article  Google Scholar 

  166. Valera, E. and Masliah, E., Combination therapies: the next logical step for the treatment of synucleinopathies?, Mov. Disord., 2016, vol. 31, pp. 225–234.

    Article  PubMed  Google Scholar 

  167. Varatharaj, A. and Galea, I., The blood-brain barrier in systemic inflammation, Brain Behav. Immun, 2017, vol. 60, pp. 1–12. doi 10.1016/j.bbi.2016.03.010

  168. Verma, R., Verma, A.K., Ahuja, V., and Paul, J., Real-time analysis of mucosal flora in patients with inflammatory bowel disease in India, J. Clin. Microbiol., 2010, vol. 48, pp. 4279–4282.

    Article  PubMed  PubMed Central  Google Scholar 

  169. Voloshko, L.N. and Pinevich, A.V., Diversity of cyanobacterial toxins, Astrakhan. Vestn. Ekol. Obraz., 2014, vol. 1, no. 27, pp. 68–80.

    Google Scholar 

  170. Wall, R., Cryan, J.F., Ross, R.P., et al., Bacterial neuroactive compounds produced by psychobiotics, Adv. Exp. Med. Biol., 2014, vol. 817, pp. 221–239.

    Article  CAS  PubMed  Google Scholar 

  171. Wang, X.L., Zeng, J., Feng, J., et al., Helicobacter pylori filtrate impairs spatial learning and memory in rats and increases β-amyloid by enhancing expression of presenilin-2, Front. Aging Neurosci., 2014, vol. 6, p. 66. doi 10.3389/fnagi.2014.00066

    PubMed  PubMed Central  Google Scholar 

  172. Welling, M.M., Nabuurs, R.J., and van der Weerd, L., Potential role of antimicrobial peptides in the early onset of Alzheimer’s disease, Alzheimers Dement., 2015, vol. 11, no. 1, pp. 51–57. doi 10.1016/j.jalz.2013.12.020

    Article  PubMed  Google Scholar 

  173. Widera, M., Klein, A.N., Cinar, Y., et al., The D-amino acid peptide D3 reduces amyloid fibril boosted HIV-1 infectivity, AIDS Res. Ther., 2014, vol. 11, no. 1, p. 1. doi 10.1186/1742-6405-11-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Wozniak, M.A., Frost, A.L., Preston, C.M., and Itzhaki, R.F., Antivirals reduce the formation of key Alzheimer’s disease molecules in cell cultures acutely infected with herpes simplex virus type 1, PLoS One, vol. 6. e25152.

  175. Xie, X., Basile, M., and Mash, D.C., Cerebral uptake and protein incorporation of cyanobacterial toxin β-N-methylamino-L-alanine, Neuroreport, 2013, vol. 24, no. 14, pp. 779–784. doi 10.1097/WNR.0b013e328363fd89

    Article  CAS  PubMed  Google Scholar 

  176. Xu, J. and Ikezu, T., The comorbidity of HIV-associated neurocognitive disorders and Alzheimer’s disease: a foreseeable medical challenge in post-HAART era, J. Neuroimmune Pharmacol., 2009, vol. 4, no. 2, pp. 200–212.

    Article  CAS  PubMed  Google Scholar 

  177. Yin, H.Z., Yu, S., Hsu, C.-I., et al., Intrathecal infusion of BMAA induces selective motor neuron damage and astrogliosis in the ventral horn of the spinal cord, Exp. Neurol., 2014, vol. 261, pp. 1–9. doi 10.1016/ j.expneurol.2014.06.003

    Article  CAS  PubMed  Google Scholar 

  178. Yu, Y. and Ye, R.D., Microglial Aβ receptors in Alzheimer’s disease, Cell. Mol. Neurobiol., 2015, vol. 35, no. 1, pp. 71–83. doi 10.1007/s10571-014-0101-6

    Article  CAS  PubMed  Google Scholar 

  179. Yu, J.T., Chang, R.C., and Tan, L., Calcium dysregulation in Alzheimer’s disease: from mechanisms to therapeutic opportunities, Prog. Neurobiol., 2009, vol. 89, no. 3, pp. 240–255.

    Article  CAS  PubMed  Google Scholar 

  180. Zambrano, A., Solis, L., Salvadores, N., et al., Neuronal cytoskeletal dynamic modification and neurodegeneration induced by infection with herpes simplex virus type 1, J. Alzheimers Dis., 2008, vol. 14, no. 3, pp. 259–269.

    Article  CAS  PubMed  Google Scholar 

  181. Zhang, H., Sun, S., Wu, L., et al., Store-operated calcium channel complex in postsynaptic spines: a new therapeutic target for Alzheimer’s disease treatment, J. Neurosci., 2016, vol. 36, pp. 11837–11850.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Zhao, Y., Dua, P., and Lukiw, W.J., Microbial sources of amyloid and relevance to amyloidogenesis and Alzheimer’s disease (AD), J. Alzheimers Dis. Parkinsonism, 2015, vol. 5, no. 1, p. 177.

    CAS  PubMed  PubMed Central  Google Scholar 

  183. Zhou, Y., Blanco, L.P., Smith, D.R., and Chapman, M.R., Bacterial amyloids, Methods Mol. Biol., 2012, vol. 849, pp. 303–320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Zhou, L., Miranda-Saksena, M., and Saksena, N.K., Viruses and neurodegeneration, Virol. J., 2013, vol. 10, p. 172. doi 10.1186/1743-422X-10-172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

I am grateful to Doctor of Biology I.V. Shemarova for a number of valuable comments and additions.

The work was supported by the Federal Agency for Scientific Organizations of Russia (topic no. АААА-А18-118012290142-9).

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Sobol, C.V. Role of Microbiota in Neurodegenerative Diseases. Russ J Dev Biol 49, 297–313 (2018). https://doi.org/10.1134/S1062360418060061

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