Targeting Gut Dysbiosis and Microbiome Metabolites for the Development of Therapeutic Modalities for Neurological Disorders

  • Authors: Wiefels M.1, Furar E.2, Eshraghi R.3, Mittal J.4, Memis I.4, Moosa M.5, Mittal R.6, Eshraghi A.7
  • Affiliations:
    1. Hearing Research and Communication Disorders Laboratory, Department of Otolaryngolog, Miller School of Medicine, University of Miami
    2. Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology, Miller School of Medicine,, Miller School of Medicine, University of Miami,
    3. Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology, Miller School of Medicine, Miller School of Medicine, University of Miami
    4. Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology,, Miller School of Medicine, University of Miami
    5. Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology,, Miller School of Medicine, University of Miami,
    6. Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology, Miller School of Medicine, University of Miami
    7. Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology, Miller School of Medicine, University of Miami,
  • Issue: Vol 22, No 1 (2024)
  • Pages: 123-139
  • Section: Neurology
  • URL: https://rjraap.com/1570-159X/article/view/644248
  • DOI: https://doi.org/10.2174/1570159X20666221003085508
  • ID: 644248

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Full Text

Abstract

The gut microbiota, composed of numerous species of microbes, works in synergy with the various organ systems in the body to bolster our overall health and well-being. The most well-known function of the gut microbiome is to facilitate the metabolism and absorption of crucial nutrients, such as complex carbohydrates, while also generating vitamins. In addition, the gut microbiome plays a crucial role in regulating the functioning of the central nervous system (CNS). Host genetics, including specific genes and single nucleotide polymorphisms (SNPs), have been implicated in the pathophysiology of neurological disorders, including Parkinson’s disease (PD), Alzheimer’s disease (AD), and autism spectrum disorder (ASD). The gut microbiome dysbiosis also plays a role in the pathogenesis of these neurodegenerative disorders, thus perturbing the gut-brain axis. Overproduction of certain metabolites synthesized by the gut microbiome, such as short-chain fatty acids (SCFAs) and p-cresyl sulfate, are known to interfere with microglial function and trigger misfolding of alpha-synuclein protein, which can build up inside neurons and cause damage. By determining the association of the gut microbiome and its metabolites with various diseases, such as neurological disorders, future research will pave the way for the development of effective preventive and treatment modalities.

About the authors

Matthew Wiefels

Hearing Research and Communication Disorders Laboratory, Department of Otolaryngolog, Miller School of Medicine, University of Miami

Email: info@benthamscience.net

Emily Furar

Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology, Miller School of Medicine,, Miller School of Medicine, University of Miami,

Email: info@benthamscience.net

Rebecca Eshraghi

Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology, Miller School of Medicine, Miller School of Medicine, University of Miami

Email: info@benthamscience.net

Jeenu Mittal

Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology,, Miller School of Medicine, University of Miami

Email: info@benthamscience.net

Idil Memis

Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology,, Miller School of Medicine, University of Miami

Email: info@benthamscience.net

Moeed Moosa

Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology,, Miller School of Medicine, University of Miami,

Email: info@benthamscience.net

Rahul Mittal

Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology, Miller School of Medicine, University of Miami

Email: info@benthamscience.net

Adrien Eshraghi

Hearing Research and Communication Disorders Laboratory, Department of Otolaryngology, Miller School of Medicine, University of Miami,

Author for correspondence.
Email: info@benthamscience.net

References

  1. Verhaar, B.J.H.; Hendriksen, H.M.A.; de Leeuw, F.A.; Doorduijn, A.S.; van Leeuwenstijn, M.; Teunissen, C.E.; Barkhof, F.; Scheltens, P.; Kraaij, R.; van Duijn, C.M.; Nieuwdorp, M.; Muller, M.; van der Flier, W.M. Gut microbiota composition is related to AD pathology. Front. Immunol., 2022, 12, 794519. doi: 10.3389/fimmu.2021.794519 PMID: 35173707
  2. Konopelski, P.; Mogilnicka, I. Biological effects of indole-3-propionic acid, a gut microbiota-derived metabolite, and its precursor tryptophan in mammals’ health and disease. Int. J. Mol. Sci., 2022, 23(3), 1222. doi: 10.3390/ijms23031222 PMID: 35163143
  3. Eshraghi, R.S.; Davies, C.; Iyengar, R.; Perez, L.; Mittal, R.; Eshraghi, A.A. Gut-induced inflammation during development may compromise the blood-brain barrier and predispose to autism spectrum disorder. J. Clin. Med., 2020, 10(1), 27. doi: 10.3390/jcm10010027 PMID: 33374296
  4. Eshraghi, R.S.; Deth, R.C.; Mittal, R.; Aranke, M.; Kay, S.I.S.; Moshiree, B.; Eshraghi, A.A. Early disruption of the microbiome leading to decreased antioxidant capacity and epigenetic changes: Implications for the rise in autism. Front. Cell. Neurosci., 2018, 12, 256. doi: 10.3389/fncel.2018.00256 PMID: 30158857
  5. Kim, C.H.; Jung, J.; Lee, Y.; Kim, K.; Kang, S.; Kang, G.; Chu, H.; Kim, S.Y.; Lee, S. Comparison of metabolites and gut microbes between patients with Parkinson’s disease and healthy individuals – a pilot clinical observational study (STROBE compliant). Healthcare (Basel), 2022, 10(2), 302. doi: 10.3390/healthcare10020302 PMID: 35206916
  6. Chen, S.J.; Chen, C.C.; Liao, H.Y.; Lin, Y.T.; Wu, Y.W.; Liou, J.M.; Wu, M.S.; Kuo, C.H.; Lin, C.H. Association of fecal and plasma levels of short-chain fatty acids with gut microbiota and clinical severity in patients with Parkinson disease. Neurology, 2022, 98(8), e848-e858. doi: 10.1212/WNL.0000000000013225 PMID: 34996879
  7. Sampson, T.R.; Debelius, J.W.; Thron, T.; Janssen, S.; Shastri, G.G.; Ilhan, Z.E.; Challis, C.; Schretter, C.E.; Rocha, S.; Gradinaru, V.; Chesselet, M.F.; Keshavarzian, A.; Shannon, K.M.; Krajmalnik-Brown, R.; Wittung-Stafshede, P.; Knight, R.; Mazmanian, S.K. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson’s disease. Cell, 2016, 167(6), 1469-1480.e12. doi: 10.1016/j.cell.2016.11.018 PMID: 27912057
  8. Brody, H. The gut microbiome. Nature, 2020, 577(7792), S5. doi: 10.1038/d41586-020-00194-2 PMID: 31996824
  9. Cresci, G.A.; Bawden, E. Gut microbiome. Nutr. Clin. Pract., 2015, 30(6), 734-746. doi: 10.1177/0884533615609899 PMID: 26449893
  10. Lozupone, C.A.; Stombaugh, J.I.; Gordon, J.I.; Jansson, J.K.; Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature, 2012, 489(7415), 220-230. doi: 10.1038/nature11550 PMID: 22972295
  11. Shreiner, A.B.; Kao, J.Y.; Young, V.B. The gut microbiome in health and in disease. Curr. Opin. Gastroenterol., 2015, 31(1), 69-75. doi: 10.1097/MOG.0000000000000139 PMID: 25394236
  12. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature, 2012, 486(7402), 207-214. doi: 10.1038/nature11234 PMID: 22699609
  13. Manor, O.; Dai, C.L.; Kornilov, S.A.; Smith, B.; Price, N.D.; Lovejoy, J.C.; Gibbons, S.M.; Magis, A.T. Health and disease markers correlate with gut microbiome composition across thousands of people. Nat. Commun., 2020, 11(1), 5206. doi: 10.1038/s41467-020-18871-1 PMID: 33060586
  14. Wu, Y.T.; Shen, S.J.; Liao, K.F.; Huang, C.Y. Dietary plant and animal protein sources oppositely modulate fecal Bilophila and Lachnoclostridium in vegetarians and omnivores. Microbiol. Spectr., 2022, 10(2), e02047-e21. doi: 10.1128/spectrum.02047-21 PMID: 35285706
  15. Tanes, C.; Bittinger, K.; Gao, Y.; Friedman, E.S.; Nessel, L.; Paladhi, U.R.; Chau, L.; Panfen, E.; Fischbach, M.A.; Braun, J.; Xavier, R.J.; Clish, C.B.; Li, H.; Bushman, F.D.; Lewis, J.D.; Wu, G.D. Role of dietary fiber in the recovery of the human gut microbiome and its metabolome. Cell Host Microbe, 2021, 29(3), 394-407.e5. doi: 10.1016/j.chom.2020.12.012 PMID: 33440171
  16. Cahana, I.; Iraqi, F.A. Impact of host genetics on gut microbiome: Take‐home lessons from human and mouse studies. Animal Model. Exp. Med., 2020, 3(3), 229-236. doi: 10.1002/ame2.12134 PMID: 33024944
  17. Kurilshikov, A.; Medina-Gomez, C.; Bacigalupe, R.; Radjabzadeh, D.; Wang, J.; Demirkan, A.; Le Roy, C.I.; Raygoza Garay, J.A.; Finnicum, C.T.; Liu, X.; Zhernakova, D.V.; Bonder, M.J.; Hansen, T.H.; Frost, F.; Rühlemann, M.C.; Turpin, W.; Moon, J.Y.; Kim, H.N.; Lüll, K.; Barkan, E.; Shah, S.A.; Fornage, M.; Szopinska-Tokov, J.; Wallen, Z.D.; Borisevich, D.; Agreus, L.; Andreasson, A.; Bang, C.; Bedrani, L.; Bell, J.T.; Bisgaard, H.; Boehnke, M.; Boomsma, D.I.; Burk, R.D.; Claringbould, A.; Croitoru, K.; Davies, G.E.; van Duijn, C.M.; Duijts, L.; Falony, G.; Fu, J.; van der Graaf, A.; Hansen, T.; Homuth, G.; Hughes, D.A.; Ijzerman, R.G.; Jackson, M.A.; Jaddoe, V.W.V.; Joossens, M.; Jørgensen, T.; Keszthelyi, D.; Knight, R.; Laakso, M.; Laudes, M.; Launer, L.J.; Lieb, W.; Lusis, A.J.; Masclee, A.A.M.; Moll, H.A.; Mujagic, Z.; Qibin, Q.; Rothschild, D.; Shin, H.; Sørensen, S.J.; Steves, C.J.; Thorsen, J.; Timpson, N.J.; Tito, R.Y.; Vieira-Silva, S.; Völker, U.; Völzke, H.; Võsa, U.; Wade, K.H.; Walter, S.; Watanabe, K.; Weiss, S.; Weiss, F.U.; Weissbrod, O.; Westra, H.J.; Willemsen, G.; Payami, H.; Jonkers, D.M.A.E.; Arias Vasquez, A.; de Geus, E.J.C.; Meyer, K.A.; Stokholm, J.; Segal, E.; Org, E.; Wijmenga, C.; Kim, H.L.; Kaplan, R.C.; Spector, T.D.; Uitterlinden, A.G.; Rivadeneira, F.; Franke, A.; Lerch, M.M.; Franke, L.; Sanna, S.; D’Amato, M.; Pedersen, O.; Paterson, A.D.; Kraaij, R.; Raes, J.; Zhernakova, A. Large-scale association analyses identify host factors influencing human gut microbiome composition. Nat. Genet., 2021, 53(2), 156-165. doi: 10.1038/s41588-020-00763-1 PMID: 33462485
  18. Schmidt, V.; Enav, H.; Spector, T.D.; Youngblut, N.D.; Ley, R.E. Strain-level analysis of Bifidobacterium spp. from gut microbiomes of adults with differing lactase persistence genotypes. mSystems, 2020, 5(5), e00911-e00920. doi: 10.1128/mSystems.00911-20 PMID: 32994293
  19. Kolde, R.; Franzosa, E.A.; Rahnavard, G.; Hall, A.B.; Vlamakis, H.; Stevens, C.; Daly, M.J.; Xavier, R.J.; Huttenhower, C. Host genetic variation and its microbiome interactions within the Human Microbiome Project. Genome Med., 2018, 10(1), 6. doi: 10.1186/s13073-018-0515-8 PMID: 29378630
  20. Lim, M.Y.; You, H.J.; Yoon, H.S.; Kwon, B.; Lee, J.Y.; Lee, S.; Song, Y.M.; Lee, K.; Sung, J.; Ko, G. The effect of heritability and host genetics on the gut microbiota and metabolic syndrome. Gut, 2017, 66(6), 1031-1038. doi: 10.1136/gutjnl-2015-311326 PMID: 27053630
  21. Montgomery, T.L.; Künstner, A.; Kennedy, J.J.; Fang, Q.; Asarian, L.; Culp-Hill, R.; D’Alessandro, A.; Teuscher, C.; Busch, H.; Krementsov, D.N. Interactions between host genetics and gut microbiota determine susceptibility to CNS autoimmunity. Proc. Natl. Acad. Sci. USA, 2020, 117(44), 27516-27527. doi: 10.1073/pnas.2002817117 PMID: 33077601
  22. Turpin, W.; Espin-Garcia, O.; Xu, W.; Silverberg, M.S.; Kevans, D.; Smith, M.I.; Guttman, D.S.; Griffiths, A.; Panaccione, R.; Otley, A.; Xu, L.; Shestopaloff, K.; Moreno-Hagelsieb, G.; Paterson, A.D.; Croitoru, K. Association of host genome with intestinal microbial composition in a large healthy cohort. Nat. Genet., 2016, 48(11), 1413-1417. doi: 10.1038/ng.3693 PMID: 27694960
  23. Bubier, J.A.; Chesler, E.J.; Weinstock, G.M. Host genetic control of gut microbiome composition. Mamm. Genome, 2021, 32(4), 263-281. doi: 10.1007/s00335-021-09884-2 PMID: 34159422
  24. Tang, J.; Wu, X.; Mou, M.; Wang, C.; Wang, L.; Li, F.; Guo, M.; Yin, J.; Xie, W.; Wang, X.; Wang, Y.; Ding, Y.; Xue, W.; Zhu, F. GIMICA: Host genetic and immune factors shaping human microbiota. Nucleic Acids Res., 2021, 49(D1), D715-D722. doi: 10.1093/nar/gkaa851 PMID: 33045729
  25. Silva, Y.P.; Bernardi, A.; Frozza, R.L. The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front. Endocrinol. (Lausanne), 2020, 11, 25. doi: 10.3389/fendo.2020.00025 PMID: 32082260
  26. Mitchell, R.W.; On, N.H.; Del Bigio, M.R.; Miller, D.W.; Hatch, G.M. Fatty acid transport protein expression in human brain and potential role in fatty acid transport across human brain microvessel endothelial cells. J. Neurochem., 2011, 117(4), no. doi: 10.1111/j.1471-4159.2011.07245.x PMID: 21395585
  27. Lee, J.; Venna, V.R.; Durgan, D.J.; Shi, H.; Hudobenko, J.; Putluri, N.; Petrosino, J.; McCullough, L.D.; Bryan, R.M. Young versus aged microbiota transplants to germ-free mice: Increased short-chain fatty acids and improved cognitive performance. Gut Microbes, 2020, 12(1), 1814107. doi: 10.1080/19490976.2020.1814107 PMID: 32897773
  28. Unger, M.M.; Spiegel, J.; Dillmann, K.U.; Grundmann, D.; Philippeit, H.; Bürmann, J.; Faßbender, K.; Schwiertz, A.; Schäfer, K.H. Short chain fatty acids and gut microbiota differ between patients with Parkinson’s disease and age-matched controls. Parkinsonism Relat. Disord., 2016, 32, 66-72. doi: 10.1016/j.parkreldis.2016.08.019 PMID: 27591074
  29. Thomas, R.H.; Meeking, M.M.; Mepham, J.R.; Tichenoff, L.; Possmayer, F.; Liu, S.; MacFabe, D.F. The enteric bacterial metabolite propionic acid alters brain and plasma phospholipid molecular species: Further development of a rodent model of autism spectrum disorders. J. Neuroinflammation, 2012, 9(1), 695. doi: 10.1186/1742-2094-9-153 PMID: 22747852
  30. Thomas, R.H.; Foley, K.A.; Mepham, J.R.; Tichenoff, L.J.; Possmayer, F.; MacFabe, D.F. Altered brain phospholipid and acylcarnitine profiles in propionic acid infused rodents: Further development of a potential model of autism spectrum disorders. J. Neurochem., 2010, 113(2), 515-529. doi: 10.1111/j.1471-4159.2010.06614.x PMID: 20405543
  31. MacFabe, D.F.; Cain, N.E.; Boon, F.; Ossenkopp, K.P.; Cain, D.P. 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, 217(1), 47-54. doi: 10.1016/j.bbr.2010.10.005 PMID: 20937326
  32. Shultz, S.R.; MacFabe, D.F.; Martin, S.; Jackson, J.; Taylor, R.; Boon, F.; Ossenkopp, K.P.; Cain, D.P. Intracerebroventricular injections of the enteric bacterial metabolic product propionic acid impair cognition and sensorimotor ability in the Long–Evans rat: Further development of a rodent model of autism. Behav. Brain Res., 2009, 200(1), 33-41. doi: 10.1016/j.bbr.2008.12.023 PMID: 19154758
  33. Shultz, S.R.; MacFabe, D.F.; Ossenkopp, K.P.; Scratch, S.; Whelan, J.; Taylor, R.; Cain, D.P. Intracerebroventricular injection of propionic acid, an enteric bacterial metabolic end-product, impairs social behavior in the rat: Implications for an animal model of autism. Neuropharmacology, 2008, 54(6), 901-911. doi: 10.1016/j.neuropharm.2008.01.013 PMID: 18395759
  34. Zheng, W.; He, R.; Yan, Z.; Huang, Y.; Huang, W.; Cai, Z.; Su, Y.; Liu, S.; Deng, Y.; Wang, Q.; Xie, H. Regulation of immune-driven pathogenesis in Parkinson’s disease by gut microbiota. Brain Behav. Immun., 2020, 87, 890-897. doi: 10.1016/j.bbi.2020.01.009 PMID: 31931152
  35. Sharon, G.; Cruz, N.J.; Kang, D.W.; Gandal, M.J.; Wang, B.; Kim, Y.M.; Zink, E.M.; Casey, C.P.; Taylor, B.C.; Lane, C.J.; Bramer, L.M.; Isern, N.G.; Hoyt, D.W.; Noecker, C.; Sweredoski, M.J.; Moradian, A.; Borenstein, E.; Jansson, J.K.; Knight, R.; Metz, T.O.; Lois, C.; Geschwind, D.H.; Krajmalnik-Brown, R.; Mazmanian, S.K.; Mazmanian, S.K. Human gut microbiota from autism spectrum disorder promote behavioral symptoms in mice. Cell, 2019, 177(6), 1600-1618.e17. doi: 10.1016/j.cell.2019.05.004 PMID: 31150625
  36. Mersman, B.; Zaidi, W.; Syed, N.I.; Xu, F. Taurine promotes neurite outgrowth and synapse development of both vertebrate and invertebrate central neurons. Front. Synaptic Neurosci., 2020, 12, 29. doi: 10.3389/fnsyn.2020.00029 PMID: 32792935
  37. Kaelberer, M.M.; Buchanan, K.L.; Klein, M.E.; Barth, B.B.; Montoya, M.M.; Shen, X.; Bohórquez, D.V. A gut-brain neural circuit for nutrient sensory transduction. Science, 2018, 361(6408), eaat5236. doi: 10.1126/science.aat5236 PMID: 30237325
  38. Needham, B.D.; Kaddurah-Daouk, R.; Mazmanian, S.K. Gut microbial molecules in behavioural and neurodegenerative conditions. Nat. Rev. Neurosci., 2020, 21(12), 717-731. doi: 10.1038/s41583-020-00381-0 PMID: 33067567
  39. Bermudez-Martin, P.; Becker, J.A.J.; Caramello, N.; Fernandez, S.P.; Costa-Campos, R.; Canaguier, J.; Barbosa, S.; Martinez-Gili, L.; Myridakis, A.; Dumas, M.E.; Bruneau, A.; Cherbuy, C.; Langella, P.; Callebert, J.; Launay, J.M.; Chabry, J.; Barik, J.; Le Merrer, J.; Glaichenhaus, N.; Davidovic, L. The microbial metabolite p-Cresol induces autistic-like behaviors in mice by remodeling the gut microbiota. Microbiome, 2021, 9(1), 157. doi: 10.1186/s40168-021-01103-z PMID: 34238386
  40. Needham, B.D.; Adame, M.D.; Serena, G.; Rose, D.R.; Preston, G.M.; Conrad, M.C.; Campbell, A.S.; Donabedian, D.H.; Fasano, A.; Ashwood, P.; Mazmanian, S.K. Plasma and fecal metabolite profiles in autism spectrum disorder. Biol. Psychiatry, 2021, 89(5), 451-462. doi: 10.1016/j.biopsych.2020.09.025 PMID: 33342544
  41. Hsiao, E.Y.; McBride, S.W.; Hsien, S.; Sharon, G.; Hyde, E.R.; McCue, T.; Codelli, J.A.; Chow, J.; Reisman, S.E.; Petrosino, J.F.; Patterson, P.H.; Mazmanian, S.K. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell, 2013, 155(7), 1451-1463. doi: 10.1016/j.cell.2013.11.024 PMID: 24315484
  42. Gabriele, S.; Sacco, R.; Cerullo, S.; Neri, C.; Urbani, A.; Tripi, G.; Malvy, J.; Barthelemy, C.; Bonnet-Brihault, F.; Persico, A.M. Urinary p -cresol is elevated in young French children with autism spectrum disorder: A replication study. Biomarkers, 2014, 19(6), 463-470. doi: 10.3109/1354750X.2014.936911 PMID: 25010144
  43. Gacias, M.; Gaspari, S.; Santos, P.M.G.; Tamburini, S.; Andrade, M.; Zhang, F.; Shen, N.; Tolstikov, V.; Kiebish, M.A.; Dupree, J.L.; Zachariou, V.; Clemente, J.C.; Casaccia, P. Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior. eLife, 2016, 5, e13442. doi: 10.7554/eLife.13442 PMID: 27097105
  44. Guzmán-Salas, S.; Weber, A.; Malci, A.; Lin, X.; Herrera-Molina, R.; Cerpa, W.; Dorador, C.; Signorelli, J.; Zamorano, P. The metaboliteP ‐cresol impairs dendritic development, synaptogenesis, and synapse function in hippocampal neurons: Implications for autism spectrum disorder. J. Neurochem., 2022, 161(4), 335-349. doi: 10.1111/jnc.15604 PMID: 35257373
  45. Daneberga, Z.; Nakazawa-Miklasevica, M.; Berga-Svitina, E.; Murmane, D.; Isarova, D.; Cupane, L.; Masinska, M.; Nartisa, I.; Lazdane, A.; Miklasevics, E. Urinary organic acids spectra in children with altered gut microbiota composition and autistic spectrum disorder. Nord. J. Psychiatry, 2021, 1-7. doi: 10.1080/08039488.2021.2014954 PMID: 34935590
  46. Kang, D.W.; Adams, J.B.; Vargason, T.; Santiago, M.; Hahn, J.; Krajmalnik-Brown, R. Distinct fecal and plasma metabolites in children with autism spectrum disorders and their modulation after microbiota transfer therapy. MSphere, 2020, 5(5), e00314-e00320. doi: 10.1128/mSphere.00314-20 PMID: 33087514
  47. Gevi, F.; Belardo, A.; Zolla, L. A metabolomics approach to investigate urine levels of neurotransmitters and related metabolites in autistic children. Biochim. Biophys. Acta Mol. Basis Dis., 2020, 1866(10), 165859. doi: 10.1016/j.bbadis.2020.165859 PMID: 32512190
  48. Kang, D.W.; Ilhan, Z.E.; Isern, N.G.; Hoyt, D.W.; Howsmon, D.P.; Shaffer, M.; Lozupone, C.A.; Hahn, J.; Adams, J.B.; Krajmalnik-Brown, R. Differences in fecal microbial metabolites and microbiota of children with autism spectrum disorders. Anaerobe, 2018, 49, 121-131. doi: 10.1016/j.anaerobe.2017.12.007 PMID: 29274915
  49. Altieri, L.; Neri, C.; Sacco, R.; Curatolo, P.; Benvenuto, A.; Muratori, F.; Santocchi, E.; Bravaccio, C.; Lenti, C.; Saccani, M.; Rigardetto, R.; Gandione, M.; Urbani, A.; Persico, A.M. Urinary p -cresol is elevated in small children with severe autism spectrum disorder. Biomarkers, 2011, 16(3), 252-260. doi: 10.3109/1354750X.2010.548010 PMID: 21329489
  50. Velasquez, M.; Ramezani, A.; Manal, A.; Raj, D. Trimethylamine N-oxide: The good, the bad and the unknown. Toxins (Basel), 2016, 8(11), 326. doi: 10.3390/toxins8110326 PMID: 27834801
  51. Hoyles, L.; Pontifex, M.G.; Rodriguez-Ramiro, I.; Anis-Alavi, M.A.; Jelane, K.S.; Snelling, T.; Solito, E.; Fonseca, S.; Carvalho, A.L.; Carding, S.R.; Müller, M.; Glen, R.C.; Vauzour, D.; McArthur, S. Regulation of blood–brain barrier integrity by microbiome-associated methylamines and cognition by trimethylamine N-oxide. Microbiome, 2021, 9(1), 235. doi: 10.1186/s40168-021-01181-z PMID: 34836554
  52. Gobbetti, T.; Cooray, S.N. Annexin A1 and resolution of inflammation: Tissue repairing properties and signalling signature. Biol. Chem., 2016, 397(10), 981-993. doi: 10.1515/hsz-2016-0200 PMID: 27447237
  53. Cristante, E.; McArthur, S.; Mauro, C.; Maggioli, E.; Romero, I.A.; Wylezinska-Arridge, M.; Couraud, P.O.; Lopez-Tremoleda, J.; Christian, H.C.; Weksler, B.B.; Malaspina, A.; Solito, E. Identification of an essential endogenous regulator of blood–brain barrier integrity, and its pathological and therapeutic implications. Proc. Natl. Acad. Sci. USA, 2013, 110(3), 832-841. doi: 10.1073/pnas.1209362110 PMID: 23277546
  54. Matheoud, D.; Cannon, T.; Voisin, A.; Penttinen, A.M.; Ramet, L.; Fahmy, A.M.; Ducrot, C.; Laplante, A.; Bourque, M.J.; Zhu, L.; Cayrol, R.; Le Campion, A.; McBride, H.M.; Gruenheid, S.; Trudeau, L.E.; Desjardins, M. Intestinal infection triggers Parkinson’s disease-like symptoms in Pink1−/− mice. Nature, 2019, 571(7766), 565-569. doi: 10.1038/s41586-019-1405-y PMID: 31316206
  55. Wei, G.Z.; Martin, K.A.; Xing, P.Y.; Agrawal, R.; Whiley, L.; Wood, T.K.; Hejndorf, S.; Ng, Y.Z.; Low, J.Z.Y.; Rossant, J.; Nechanitzky, R.; Holmes, E.; Nicholson, J.K.; Tan, E.K.; Matthews, P.M.; Pettersson, S. Tryptophan-metabolizing gut microbes regulate adult neurogenesis via the aryl hydrocarbon receptor. Proc. Natl. Acad. Sci. USA, 2021, 118(27), e2021091118. doi: 10.1073/pnas.2021091118 PMID: 34210797
  56. Agirman, G.; Yu, K.B.; Hsiao, E.Y. Signaling inflammation across the gut-brain axis. Science, 2021, 374(6571), 1087-1092. doi: 10.1126/science.abi6087 PMID: 34822299
  57. Campos-Acuña, J.; Elgueta, D.; Pacheco, R. T-cell-driven inflammation as a mediator of the gut-brain axis involved in Parkinson’s disease. Front. Immunol., 2019, 10, 239. doi: 10.3389/fimmu.2019.00239 PMID: 30828335
  58. Singh, V.; Roth, S.; Llovera, G.; Sadler, R.; Garzetti, D.; Stecher, B.; Dichgans, M.; Liesz, A. Microbiota dysbiosis controls the neuroinflammatory response after stroke. J. Neurosci., 2016, 36(28), 7428-7440. doi: 10.1523/JNEUROSCI.1114-16.2016 PMID: 27413153
  59. Rothhammer, V.; Mascanfroni, I.D.; Bunse, L.; Takenaka, M.C.; Kenison, J.E.; Mayo, L.; Chao, C.C.; Patel, B.; Yan, R.; Blain, M.; Alvarez, J.I.; Kébir, H.; Anandasabapathy, N.; Izquierdo, G.; Jung, S.; Obholzer, N.; Pochet, N.; Clish, C.B.; Prinz, M.; Prat, A.; Antel, J.; Quintana, F.J. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat. Med., 2016, 22(6), 586-597. doi: 10.1038/nm.4106 PMID: 27158906
  60. Wolf, S.A.; Boddeke, H.W.G.M.; Kettenmann, H. Microglia in physiology and disease. Annu. Rev. Physiol., 2017, 79(1), 619-643. doi: 10.1146/annurev-physiol-022516-034406 PMID: 27959620
  61. Erny, D.; Hrabě de Angelis, A.L.; Jaitin, D.; Wieghofer, P.; Staszewski, O.; David, E.; Keren-Shaul, H.; Mahlakoiv, T.; Jakobshagen, K.; Buch, T.; Schwierzeck, V.; Utermöhlen, O.; Chun, E.; Garrett, W.S.; McCoy, K.D.; Diefenbach, A.; Staeheli, P.; Stecher, B.; Amit, I.; Prinz, M. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci., 2015, 18(7), 965-977. doi: 10.1038/nn.4030 PMID: 26030851
  62. Martins-Silva, T.; Salatino-Oliveira, A.; Genro, J.P.; Meyer, F.D.T.; Li, Y.; Rohde, L.A.; Hutz, M.H.; Tovo-Rodrigues, L. Host genetics influences the relationship between the gut microbiome and psychiatric disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2021, 106, 110153. doi: 10.1016/j.pnpbp.2020.110153 PMID: 33130294
  63. Santos, S.F.; de Oliveira, H.L.; Yamada, E.S.; Neves, B.C.; Pereira, A., Jr The gut and Parkinson’s disease—a bidirectional pathway. Front. Neurol., 2019, 10, 574. doi: 10.3389/fneur.2019.00574 PMID: 31214110
  64. Perez Visñuk, D.; Savoy de Giori, G.; LeBlanc, J.G.; de Moreno de LeBlanc, A. Neuroprotective effects associated with immune modulation by selected lactic acid bacteria in a Parkinson’s disease model. Nutrition, 2020, 79-80, 110995. doi: 10.1016/j.nut.2020.110995 PMID: 32977125
  65. Cheng, L.H.; Liu, Y.W.; Wu, C.C.; Wang, S.; Tsai, Y.C. Psychobiotics in mental health, neurodegenerative and neurodevelopmental disorders. Yao Wu Shi Pin Fen Xi, 2019, 27(3), 632-648. PMID: 31324280
  66. Cerdó, T.; Ruíz, A.; Suárez, A.; Campoy, C. Probiotic, prebiotic, and brain development. Nutrients, 2017, 9(11), 1247. doi: 10.3390/nu9111247 PMID: 29135961
  67. Tahami Monfared, A.A.; Byrnes, M.J.; White, L.A.; Zhang, Q. Alzheimer’s disease: Epidemiology and clinical progression. Neurol. Ther., 2022, 11(2), 553-569. doi: 10.1007/s40120-022-00338-8 PMID: 35286590
  68. Fisher, R.A.; Miners, J.S.; Love, S. Pathological changes within the cerebral vasculature in Alzheimer’s disease: New perspectives. Brain Pathol., 2022, e13061. doi: 10.1111/bpa.13061 PMID: 35289012
  69. Scheltens, P.; De Strooper, B.; Kivipelto, M.; Holstege, H.; Chételat, G.; Teunissen, C.E.; Cummings, J.; van der Flier, W.M. Alzheimer’s disease. Lancet, 2021, 397(10284), 1577-1590. doi: 10.1016/S0140-6736(20)32205-4 PMID: 33667416
  70. Rezaei, A.Z.; Sepehri, G.; Salami, M. Probiotic treatment improves the impaired spatial cognitive performance and restores synaptic plasticity in an animal model of Alzheimer’s disease. Behav. Brain Res., 2019, 376, 112183. doi: 10.1016/j.bbr.2019.112183 PMID: 31472194
  71. Babür, E.; Tan, B.; Delibaş, S.; Yousef, M.; Dursun, N.; Süer, C. Depotentiation of long-term potentiation is associated with epitope-specific tau hyper-/hypophosphorylation in the hippocampus of adult rats. J. Mol. Neurosci., 2019, 67(2), 193-203. doi: 10.1007/s12031-018-1224-x PMID: 30498986
  72. Athari, N.A.S.; Djazayeri, A.; Safa, M.; Azami, K.; Djalali, M.; Sharifzadeh, M.; Vafa, M. Probiotics improve insulin resistance status in an experimental model of Alzheimer’s disease. Med. J. Islam. Repub. Iran, 2017, 31(1), 699-704. doi: 10.14196/mjiri.31.103 PMID: 29951404
  73. Yamin, G. NMDA receptor-dependent signaling pathways that underlie amyloid β-protein disruption of LTP in the hippocampus. J. Neurosci. Res., 2009, 87(8), 1729-1736. doi: 10.1002/jnr.21998 PMID: 19170166
  74. Wiatrak, B.; Jawień, P.; Matuszewska, A.; Szeląg, A.; Kubis-Kubiak, A. Effect of amyloid-β on the redox system activity in SH-SY5Y cells preincubated with lipopolysaccharide or co-cultured with microglia cells. Biomed. Pharmacother., 2022, 149, 112880. doi: 10.1016/j.biopha.2022.112880 PMID: 35367762
  75. Hemert, S.V.; Ormel, G. Influence of the multispecies probiotic Ecologic® BARRIER on parameters of intestinal barrier function. Food Nutr. Sci., 2014, 5(18), 1739-1745. doi: 10.4236/fns.2014.518187
  76. Romo-Araiza, A.; Gutiérrez-Salmeán, G.; Galván, E.J.; Hernández-Frausto, M.; Herrera-López, G.; Romo-Parra, H.; García-Contreras, V.; Fernández-Presas, A.M.; Jasso-Chávez, R.; Borlongan, C.V.; Ibarra, A. Probiotics and prebiotics as a therapeutic strategy to improve memory in a model of middle-aged rats. Front. Aging Neurosci., 2018, 10, 416. doi: 10.3389/fnagi.2018.00416 PMID: 30618722
  77. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 5th ed; ATA: Washington, USA, 2013.
  78. Gao, J.; Wang, X.; Sun, H.; Cao, Y.; Liang, S.; Wang, H.; Wang, Y.; Yang, F.; Zhang, F.; Wu, L. Neuroprotective effects of docosahexaenoic acid on hippocampal cell death and learning and memory impairments in a valproic acid‐induced rat autism model. Int. J. Dev. Neurosci., 2016, 49(1), 67-78. doi: 10.1016/j.ijdevneu.2015.11.006 PMID: 26639559
  79. Dan, Z.; Mao, X.; Liu, Q.; Guo, M.; Zhuang, Y.; Liu, Z.; Chen, K.; Chen, J.; Xu, R.; Tang, J.; Qin, L.; Gu, B.; Liu, K.; Su, C.; Zhang, F.; Xia, Y.; Hu, Z.; Liu, X. Altered gut microbial profile is associated with abnormal metabolism activity of Autism Spectrum Disorder. Gut Microbes, 2020, 11(5), 1246-1267. doi: 10.1080/19490976.2020.1747329 PMID: 32312186
  80. Golubeva, A.V.; Joyce, S.A.; Moloney, G.; Burokas, A.; Sherwin, E.; Arboleya, S.; Flynn, I.; Khochanskiy, D.; Moya-Pérez, A.; Peterson, V.; Rea, K.; Murphy, K.; Makarova, O.; Buravkov, S.; Hyland, N.P.; Stanton, C.; Clarke, G.; Gahan, C.G.M.; Dinan, T.G.; Cryan, J.F. Microbiota-related changes in bile acid & tryptophan metabolism are associated with gastrointestinal dysfunction in a mouse model of autism. EBioMedicine, 2017, 24, 166-178. doi: 10.1016/j.ebiom.2017.09.020 PMID: 28965876
  81. Liu, Z.; Mao, X.; Dan, Z.; Pei, Y.; Xu, R.; Guo, M.; Liu, K.; Zhang, F.; Chen, J.; Su, C.; Zhuang, Y.; Tang, J.; Xia, Y.; Qin, L.; Hu, Z.; Liu, X. Gene variations in Autism Spectrum Disorder are associated with alternation of gut microbiota, metabolites and cytokines. Gut Microbes, 2021, 13(1), 1854967. doi: 10.1080/19490976.2020.1854967 PMID: 33412999
  82. Sabit, H.; Tombuloglu, H.; Rehman, S.; Almandil, N.B.; Cevik, E.; Abdel-Ghany, S.; Rashwan, S.; Abasiyanik, M.F.; Yee Waye, M.M. Gut microbiota metabolites in autistic children: An epigenetic perspective. Heliyon, 2021, 7(1), e06105. doi: 10.1016/j.heliyon.2021.e06105 PMID: 33553761
  83. Jyonouchi, H.; Sun, S.; Itokazu, N. Innate immunity associated with inflammatory responses and cytokine production against common dietary proteins in patients with autism spectrum disorder. Neuropsychobiology, 2002, 46(2), 76-84. doi: 10.1159/000065416 PMID: 12378124
  84. MacFabe, D.; Cain, D.; Rodriguezcapote, K.; Franklin, A.; Hoffman, J.; Boon, F.; Taylor, A.; Kavaliers, M.; Ossenkopp, K. 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, 176(1), 149-169. doi: 10.1016/j.bbr.2006.07.025 PMID: 16950524
  85. De Angelis, M.; Piccolo, M.; Vannini, L.; Siragusa, S.; De Giacomo, A.; Serrazzanetti, D.I.; Cristofori, F.; Guerzoni, M.E.; Gobbetti, M.; Francavilla, R. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS One, 2013, 8(10), e76993. doi: 10.1371/journal.pone.0076993 PMID: 24130822
  86. D’Eufemia, P.; Celli, M.; Finocchiaro, R.; Pacifico, L.; Viozzi, L.; Zaccagnini, M.; Cardi, E.; Giardini, O. Abnormal intestinal permeability in children with autism. Acta Paediatr., 1996, 85(9), 1076-1079. doi: 10.1111/j.1651-2227.1996.tb14220.x PMID: 8888921
  87. Kang, D.W.; Park, J.G.; Ilhan, Z.E.; Wallstrom, G.; LaBaer, J.; Adams, J.B.; Krajmalnik-Brown, R. Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children. PLoS One, 2013, 8(7), e68322. doi: 10.1371/journal.pone.0068322 PMID: 23844187
  88. Luna, R.A.; Oezguen, N.; Balderas, M.; Venkatachalam, A.; Runge, J.K.; Versalovic, J.; Veenstra-VanderWeele, J.; Anderson, G.M.; Savidge, T.; Williams, K.C. Distinct microbiome-neuroimmune signatures correlate with functional abdominal pain in children with autism spectrum disorder. Cell. Mol. Gastroenterol. Hepatol., 2017, 3(2), 218-230. doi: 10.1016/j.jcmgh.2016.11.008 PMID: 28275689
  89. McElhanon, B.O.; McCracken, C.; Karpen, S.; Sharp, W.G. Gastrointestinal symptoms in autism spectrum disorder: A meta-analysis. Pediatrics, 2014, 133(5), 872-883. doi: 10.1542/peds.2013-3995 PMID: 24777214
  90. Tomova, A.; Husarova, V.; Lakatosova, S.; Bakos, J.; Vlkova, B.; Babinska, K.; Ostatnikova, D. Gastrointestinal microbiota in children with autism in Slovakia. Physiol. Behav., 2015, 138, 179-187. doi: 10.1016/j.physbeh.2014.10.033 PMID: 25446201
  91. Peralta-Marzal, L.N.; Prince, N.; Bajic, D.; Roussin, L.; Naudon, L.; Rabot, S.; Garssen, J.; Kraneveld, A.D.; Perez-Pardo, P. The impact of gut microbiota-derived metabolites in autism spectrum disorders. Int. J. Mol. Sci., 2021, 22(18), 10052. doi: 10.3390/ijms221810052 PMID: 34576216
  92. Kociszewska, D.; Vlajkovic, S.M. The association of inflammatory gut diseases with neuroinflammatory and auditory disorders. Front. Biosci. (Elite Ed.), 2022, 14(2), 8. doi: 10.31083/j.fbe1402008 PMID: 35730449
  93. Frost, G.; Sleeth, M.L.; Sahuri-Arisoylu, M.; Lizarbe, B.; Cerdan, S.; Brody, L.; Anastasovska, J.; Ghourab, S.; Hankir, M.; Zhang, S.; Carling, D.; Swann, J.R.; Gibson, G.; Viardot, A.; Morrison, D.; Louise, T.E.; Bell, J.D. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat. Commun., 2014, 5(1), 3611. doi: 10.1038/ncomms4611 PMID: 24781306
  94. Morimoto, M.; Hashimoto, T.; Tsuda, Y.; Nakatsu, T.; Kitaoka, T.; Kyotani, S. Assessment of oxidative stress in autism spectrum disorder using reactive oxygen metabolites and biological antioxidant potential. PLoS One, 2020, 15(5), e0233550. doi: 10.1371/journal.pone.0233550 PMID: 32442231
  95. Greene, W.C.; Chen, L.F. Regulation of NF-kappaB action by reversible acetylation. Novartis Found. Symp., 2004, 259, 208-217. PMID: 15171256
  96. Nankova, B.B.; Agarwal, R.; MacFabe, D.F.; La Gamma, E.F. Enteric bacterial metabolites propionic and butyric acid modulate gene expression, including CREB-dependent catecholaminergic neurotransmission, in PC12 cells-possible relevance to autism spectrum disorders. PLoS One, 2014, 9(8), e103740. doi: 10.1371/journal.pone.0103740 PMID: 25170769
  97. Al-Lahham, S.H.; Peppelenbosch, M.P.; Roelofsen, H.; Vonk, R.J.; Venema, K. Biological effects of propionic acid in humans; metabolism, potential applications and underlying mechanisms. Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 2010, 1801(11), 1175-1183. doi: 10.1016/j.bbalip.2010.07.007 PMID: 20691280
  98. Chelakkot, C.; Ghim, J.; Ryu, S.H. Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp. Mol. Med., 2018, 50(8), 1-9. doi: 10.1038/s12276-018-0126-x PMID: 30115904
  99. Günzel, D.; Yu, A.S.L. Claudins and the modulation of tight junction permeability. Physiol. Rev., 2013, 93(2), 525-569. doi: 10.1152/physrev.00019.2012 PMID: 23589827
  100. Beatch, M.; Jesaitis, L.A.; Gallin, W.J.; Goodenough, D.A.; Stevenson, B.R. The tight junction protein ZO-2 contains three PDZ (PSD-95/Discs-Large/ZO-1) domains and an alternatively spliced region. J. Biol. Chem., 1996, 271(42), 25723-25726. doi: 10.1074/jbc.271.42.25723 PMID: 8824195
  101. Itoh, M.; Furuse, M.; Morita, K.; Kubota, K.; Saitou, M.; Tsukita, S. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J. Cell Biol., 1999, 147(6), 1351-1363. doi: 10.1083/jcb.147.6.1351 PMID: 10601346
  102. Feldman, G.; Mullin, J.; Ryan, M. Occludin: Structure, function and regulation. Adv. Drug Deliv. Rev., 2005, 57(6), 883-917. doi: 10.1016/j.addr.2005.01.009 PMID: 15820558
  103. Allam-Ndoul, B.; Castonguay-Paradis, S.; Veilleux, A. Gut microbiota and intestinal trans-epithelial permeability. Int. J. Mol. Sci., 2020, 21(17), 6402. doi: 10.3390/ijms21176402 PMID: 32899147
  104. Han, X.; Lee, A.; Huang, S.; Gao, J.; Spence, J.R.; Owyang, C. Lactobacillus rhamnosus GG prevents epithelial barrier dysfunction induced by interferon-gamma and fecal supernatants from irritable bowel syndrome patients in human intestinal enteroids and colonoids. Gut Microbes, 2019, 10(1), 59-76. doi: 10.1080/19490976.2018.1479625 PMID: 30040527
  105. Yoshida, N.; Emoto, T.; Yamashita, T.; Watanabe, H.; Hayashi, T.; Tabata, T.; Hoshi, N.; Hatano, N.; Ozawa, G.; Sasaki, N.; Mizoguchi, T.; Amin, H.Z.; Hirota, Y.; Ogawa, W.; Yamada, T.; Hirata, K. Bacteroides vulgatus and Bacteroides dorei reduce gut microbial lipopolysaccharide production and inhibit atherosclerosis. Circulation, 2018, 138(22), 2486-2498. doi: 10.1161/CIRCULATIONAHA.118.033714 PMID: 30571343
  106. Chelakkot, C.; Choi, Y.; Kim, D.K.; Park, H.T.; Ghim, J.; Kwon, Y.; Jeon, J.; Kim, M.S.; Jee, Y.K.; Gho, Y.S.; Park, H.S.; Kim, Y.K.; Ryu, S.H. Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions. Exp. Mol. Med., 2018, 50(2), e450. doi: 10.1038/emm.2017.282 PMID: 29472701
  107. Anderson, R.C.; Cookson, A.L.; McNabb, W.C.; Park, Z.; McCann, M.J.; Kelly, W.J.; Roy, N.C. Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation. BMC Microbiol., 2010, 10(1), 316. doi: 10.1186/1471-2180-10-316 PMID: 21143932
  108. Bhattarai, Y. Microbiota-gut-brain axis: Interaction of gut microbes and their metabolites with host epithelial barriers. Neurogastroenterol. Motil., 2018, 30(6), e13366. doi: 10.1111/nmo.13366 PMID: 29878576
  109. Ma, X.; Fan, P.X.; Li, L.S.; Qiao, S.Y.; Zhang, G.L.; Li, D.F. Butyrate promotes the recovering of intestinal wound healing through its positive effect on the tight junctions. J. Anim. Sci., 2012, 90(Suppl. 4), 266-268. doi: 10.2527/jas.50965 PMID: 23365351
  110. Pradhan, S.; Karve, S.S.; Weiss, A.A.; Hawkins, J.; Poling, H.M.; Helmrath, M.A.; Wells, J.M.; McCauley, H.A. Tissue responses to Shiga toxin in human intestinal organoids. Cell. Mol. Gastroenterol. Hepatol., 2020, 10(1), 171-190. doi: 10.1016/j.jcmgh.2020.02.006 PMID: 32145469
  111. Shi, H.; Yu, Y.; Lin, D.; Zheng, P.; Zhang, P.; Hu, M.; Wang, Q.; Pan, W.; Yang, X.; Hu, T.; Li, Q.; Tang, R.; Zhou, F.; Zheng, K.; Huang, X.F. β-glucan attenuates cognitive impairment via the gut-brain axis in diet-induced obese mice. Microbiome, 2020, 8(1), 143. doi: 10.1186/s40168-020-00920-y PMID: 33008466
  112. Tulyeu, J.; Kumagai, H.; Jimbo, E.; Watanabe, S.; Yokoyama, K.; Cui, L.; Osaka, H.; Mieno, M.; Yamagata, T. Probiotics prevents sensitization to oral antigen and subsequent increases in intestinal tight junction permeability in juvenile-young adult rats. Microorganisms, 2019, 7(10), 463. doi: 10.3390/microorganisms7100463 PMID: 31623229
  113. Davenport, E.R.; Sanders, J.G.; Song, S.J.; Amato, K.R.; Clark, A.G.; Knight, R. The human microbiome in evolution. BMC Biol., 2017, 15(1), 127. doi: 10.1186/s12915-017-0454-7 PMID: 29282061
  114. Wang, X.; Zhang, A.; Miao, J.; Sun, H.; Yan, G.; Wu, F.; Wang, X. Gut microbiota as important modulator of metabolism in health and disease. RSC Advances, 2018, 8(74), 42380-42389. doi: 10.1039/C8RA08094A PMID: 35558413
  115. Gagliardi, A.; Totino, V.; Cacciotti, F.; Iebba, V.; Neroni, B.; Bonfiglio, G.; Trancassini, M.; Passariello, C.; Pantanella, F.; Schippa, S. Rebuilding the gut microbiota ecosystem. Int. J. Environ. Res. Public Health, 2018, 15(8), 1679. doi: 10.3390/ijerph15081679 PMID: 30087270
  116. Manzoor, S.; Wani, S.M.; Ahmad Mir, S.; Rizwan, D. Role of probiotics and prebiotics in mitigation of different diseases. Nutrition, 2022, 96, 111602. doi: 10.1016/j.nut.2022.111602 PMID: 35182833
  117. Chen, M.; Liu, C.; Dai, M.; Wang, Q.; Li, C.; Hung, W. Bifidobacterium lactis BL-99 modulates intestinal inflammation and functions in zebrafish models. PLoS One, 2022, 17(2), e0262942. doi: 10.1371/journal.pone.0262942 PMID: 35171916
  118. Lu, J.; Lu, L.; Yu, Y.; Baranowski, J.; Claud, E.C. Maternal administration of probiotics promotes brain development and protects offspring’s brain from postnatal inflammatory insults in C57/BL6J mice. Sci. Rep., 2020, 10(1), 8178. doi: 10.1038/s41598-020-65180-0 PMID: 32424168
  119. Tamtaji, O.R.; Taghizadeh, M.; Daneshvar Kakhaki, R.; Kouchaki, E.; Bahmani, F.; Borzabadi, S.; Oryan, S.; Mafi, A.; Asemi, Z. Clinical and metabolic response to probiotic administration in people with Parkinson’s disease: A randomized, double-blind, placebo-controlled trial. Clin. Nutr., 2019, 38(3), 1031-1035. doi: 10.1016/j.clnu.2018.05.018 PMID: 29891223
  120. Chudzik, A.; Orzyłowska, A.; Rola, R.; Stanisz, G.J. Probiotics, prebiotics and postbiotics on mitigation of depression symptoms: Modulation of the brain-gut-microbiome axis. Biomolecules, 2021, 11(7), 1000. doi: 10.3390/biom11071000 PMID: 34356624
  121. Żółkiewicz, J.; Marzec, A.; Ruszczyński, M.; Feleszko, W. Postbiotics— a step beyond pre- and probiotics. Nutrients, 2020, 12(8), 2189. doi: 10.3390/nu12082189 PMID: 32717965
  122. Gu, Z.; Meng, S.; Wang, Y.; Lyu, B.; Li, P.; Shang, N. A novel bioactive postbiotics: From microbiota-derived extracellular nanoparticles to health promoting. Crit. Rev. Food Sci. Nutr., 2022, 1-15. Advance online publication doi: 10.1080/10408398.2022.2039897 PMID: 35179102
  123. Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; Calder, P.C.; Sanders, M.E. The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol., 2014, 11(8), 506-514. doi: 10.1038/nrgastro.2014.66 PMID: 24912386
  124. Vallianou, N.; Stratigou, T.; Christodoulatos, G.S.; Tsigalou, C.; Dalamaga, M. Probiotics, prebiotics, synbiotics, postbiotics, and obesity: Current evidence, controversies, and perspectives. Curr. Obes. Rep., 2020, 9(3), 179-192. doi: 10.1007/s13679-020-00379-w PMID: 32472285
  125. Li, H.Y.; Zhou, D.D.; Gan, R.Y.; Huang, S.Y.; Zhao, C.N.; Shang, A.; Xu, X.Y.; Li, H.B. Effects and mechanisms of probiotics, prebiotics, synbiotics, and postbiotics on metabolic diseases targeting gut microbiota: A narrative review. Nutrients, 2021, 13(9), 3211. doi: 10.3390/nu13093211 PMID: 34579087
  126. Garrett, W.S.; Lord, G.M.; Punit, S.; Lugo-Villarino, G.; Mazmanian, S.K.; Ito, S.; Glickman, J.N.; Glimcher, L.H. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell, 2007, 131(1), 33-45. doi: 10.1016/j.cell.2007.08.017 PMID: 17923086
  127. Richards, J.L.; Yap, Y.A.; McLeod, K.H.; Mackay, C.R.; Mariño, E. Dietary metabolites and the gut microbiota: An alternative approach to control inflammatory and autoimmune diseases. Clin. Transl. Immunology, 2016, 5(5), e82. doi: 10.1038/cti.2016.29 PMID: 27350881
  128. Sonnenburg, E.D.; Smits, S.A.; Tikhonov, M.; Higginbottom, S.K.; Wingreen, N.S.; Sonnenburg, J.L. Diet-induced extinctions in the gut microbiota compound over generations. Nature, 2016, 529(7585), 212-215. doi: 10.1038/nature16504 PMID: 26762459
  129. Hua, X.; Zhu, J.; Yang, T.; Guo, M.; Li, Q.; Chen, J.; Li, T. The gut microbiota and associated metabolites are altered in sleep disorder of children with autism spectrum disorders. Front. Psychiatry, 2020, 11, 855. doi: 10.3389/fpsyt.2020.00855 PMID: 32982808
  130. Agus, A.; Planchais, J.; Sokol, H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host Microbe, 2018, 23(6), 716-724. doi: 10.1016/j.chom.2018.05.003 PMID: 29902437
  131. Ossenkopp, K.P.; Foley, K.A.; Gibson, J.; Fudge, M.A.; Kavaliers, M.; Cain, D.P.; MacFabe, D.F. Systemic treatment with the enteric bacterial fermentation product, propionic acid, produces both conditioned taste avoidance and conditioned place avoidance in rats. Behav. Brain Res., 2012, 227(1), 134-141. doi: 10.1016/j.bbr.2011.10.045 PMID: 22085877
  132. Hou, Y.; Li, X.; Liu, C.; Zhang, M.; Zhang, X.; Ge, S.; Zhao, L. Neuroprotective effects of short-chain fatty acids in MPTP induced mice model of Parkinson’s disease. Exp. Gerontol., 2021, 150, 111376. doi: 10.1016/j.exger.2021.111376 PMID: 33905875
  133. Page, M.J.; Pretorius, E. Platelet behavior contributes to neuropathologies: A focus on Alzheimer’s and Parkinson’s disease. Semin. Thromb. Hemost., 2022, 48(3), 382-404. doi: 10.1055/s-0041-1733960 PMID: 34624913
  134. Abdel-Rahman, E.A.; Zaky, E.A.; Aboulsaoud, M.; Elhossiny, R.M.; Youssef, W.Y.; Mahmoud, A.M.; Ali, S.S. Autism spectrum disorder (ASD)-associated mitochondrial deficits are revealed in children’s platelets but unimproved by hyperbaric oxygen therapy. Free Radic. Res., 2021, 55(1), 26-40. doi: 10.1080/10715762.2020.1856376 PMID: 33402007
  135. Xie, Z.; Liu, X.; Huang, X.; Liu, Q.; Yang, M.; Huang, D.; Zhao, P.; Tian, J.; Wang, X.; Hou, J. Remodelling of gut microbiota by Berberine attenuates trimethylamine N-oxide-induced platelet hyperreaction and thrombus formation. Eur. J. Pharmacol., 2021, 911, 174526. doi: 10.1016/j.ejphar.2021.174526 PMID: 34599914
  136. Anderson, G.; Rodriguez, M.; Reiter, R.J. Multiple sclerosis: Melatonin, orexin, and ceramide interact with platelet activation coagulation factors and gut-microbiome-derived butyrate in the circadian dysregulation of mitochondria in glia and immune cells. Int. J. Mol. Sci., 2019, 20(21), 5500. doi: 10.3390/ijms20215500 PMID: 31694154
  137. Chen, Z.; Liu, C.; Jiang, Y.; Liu, H.; Shao, L.; Zhang, K.; Cheng, D.; Zhou, Y.; Chong, W. HDAC inhibitor attenuated NETs formation induced by activated platelets in vitro, partially through downregulating platelet secretion. Shock, 2020, 54(3), 321-329. doi: 10.1097/SHK.0000000000001518 PMID: 32044829
  138. Anderson, G.; Maes, M. Gut dysbiosis dysregulates central and systemic homeostasis via suboptimal mitochondrial function: Assessment, treatment and classification implications. Curr. Top. Med. Chem., 2020, 20(7), 524-539. doi: 10.2174/1568026620666200131094445 PMID: 32003689
  139. Ghafouri-Fard, S.; Namvar, A.; Arsang-Jang, S.; Komaki, A.; Taheri, M. Expression analysis of BDNF, BACE1, and their natural occurring antisenses in autistic patients. J. Mol. Neurosci., 2020, 70(2), 194-200. doi: 10.1007/s12031-019-01432-7 PMID: 31760580

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