Neurological and cognitive significance of probiotics: a holy grail deciding individual personality

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1. Rieder R, Wisniewski PJ, Alderman BL, Campbell SC. Microbes and mental health: a review. Brain Behav. Immun. 66, 9–17 (2017).
  Medline CASGoogle Scholar
• 2. Khan AA, Khurshid M, Khan S, Alshamsan A. Gut microbiota and probiotics: current status and their role in cancer therapeutics. Drug Develop. Res. 74(6), 365–375 (2013).
  CASGoogle Scholar
• 3. Khurshid M, Aslam B, Nisar MA et al. Bacterial munch for infants: potential pediatric therapeutic interventions of probiotics. Future Microbiol. 10(11), 1881–1895 (2015).
  CASGoogle Scholar
• 4. Khan AA, Shrivastava A, Khurshid M. Normal to cancer microbiome transformation and its implication in cancer diagnosis. Biochim. Biophys. Acta Rev. Cancer. 1826(2), 331–337 (2012).
  Medline CASGoogle Scholar
• 5. Lankelma JM, Nieuwdorp M, de Vos WM, Wiersinga WJ. The gut microbiota in internal medicine: implications for health and disease. Neth. J. Med. 73(2), 61–68 (2015).
  Medline CASGoogle Scholar
• 6. Bermon S, Petriz B, Kajeniene A, Prestes J, Castell L, Franco OL. The microbiota: an exercise immunology perspective. Exerc. Immunol. Rev. 21, 70–79 (2015).
  MedlineGoogle Scholar
• 7. Tillisch K. The effects of gut microbiota on CNS function in humans. Gut Microbes 5(3), 404–410 (2014).
  MedlineGoogle Scholar
• 8. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J. Clin. Invest. 125(3), 926–938 (2015).
  MedlineGoogle Scholar
• 9. Bauer KC, Huus KE, Finlay BB. Microbes and the mind: emerging hallmarks of the gut microbiota-brain axis. Cell. Microbiol. 18(5), 632–644 (2016).
  Medline CASGoogle Scholar
• 10. Li Q, Zhou JM. The microbiota–gut–brain axis and its potential therapeutic role in autism spectrum disorder. Neuroscience. 324, 131–139 (2016).
  Medline CASGoogle Scholar
• 11. Forsythe P, Bienenstock J, Kunze WA. Vagal pathways for microbiome–brain–gut axis communication. Adv. Exp. Med. Biol. 817, 115–133 (2014).
  MedlineGoogle Scholar
• 12. O'Toole PW, Marchesi JR, Hill C. Next-generation probiotics: the spectrum from probiotics to live biotherapeutics. Nat. Microbiol. 2, 17057 (2017).
  MedlineGoogle Scholar
• 13. Umbrello G, Esposito S. Microbiota and neurologic diseases: potential effects of probiotics. J. Transl. Med. 14(1), 298 (2016).
  MedlineGoogle Scholar
• 14. Mazhar SF, Afzal M, Almatroudi A et al. The prospects for the therapeutic implications of genetically engineered probiotics. J. Food Qual. 2020, 9676452 (2020).
  Google Scholar
• 15. Kristensen NB, Bryrup T, Allin KH, Nielsen T, Hansen TH, Pedersen O. Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials. Genome Med. 8(1), 52 (2016).
  MedlineGoogle Scholar
• 16. Bakirtzi K, Law IK, Xue X, Iliopoulos D, Shah YM, Pothoulakis C. Neurotensin promotes the development of colitis and intestinal angiogenesis via Hif-1alpha-miR-210 signaling. J. Immunol. 196(10), 4311–4321 (2016).
  Medline CASGoogle Scholar
• 17. Shahid M, Hussain B, Riaz D, Khurshid M, Ismail M, Tariq M. Identification and partial characterization of potential probiotic lactic acid bacteria in freshwater Labeo rohita and Cirrhinus mrigala. Aquac. Res. 48(4), 1688–1698 (2017).
  CASGoogle Scholar
• 18. Sornplang P, Piyadeatsoontorn S. Probiotic isolates from unconventional sources: a review. J. Anim. Sci. Technol. 58, 26 (2016).
  MedlineGoogle Scholar
• 19. Rajoka MSR, Mehwish HM, Zhang H et al. Antibacterial and antioxidant activity of exopolysaccharide mediated silver nanoparticle synthesized by Lactobacillus brevis isolated from Chinese koumiss. Colloids Surf. B Biointerfaces. 186, 110734 (2020).
  MedlineGoogle Scholar
• 20. Rajoka MSR, Mehwish HM, Fang H et al. Characterization and anti-tumor activity of exopolysaccharide produced by Lactobacillus kefiri isolated from Chinese kefir grains. J. Funct. Foods. 63, 103588 (2019).
  Google Scholar
• 21. George Kerry R, Patra JK, Gouda S, Park Y, Shin HS, Das G. Benefaction of probiotics for human health: s review. J. Food Drug Anal. 26(3), 927–939 (2018).
  MedlineGoogle Scholar
• 22. Guarner F, Khan AG, Garisch J et al. World Gastroenterology Organisation practice guideline: probiotics and prebiotics - May 2008. S. Afr. Gastroenterol. Rev. 6(2), 14–25 (2008).
  Google Scholar
• 23. Khurshid M, Akash MS. Probiotic preparations for infantile gastroenteritis: the clinical and economic perspective. Future Microbiol. doi: https://doi.org/10.2217/fmb-2019-0111 (2020) (Epub ahead of print).
  Google Scholar
• 24. Hempel S, Newberry SJ, Maher AR et al. Probiotics for the prevention and treatment of antibiotic-associated diarrhea: a systematic review and meta-analysis. JAMA. 307(18), 1959–1969 (2012).
  Medline CASGoogle Scholar
• 25. Guarino A, Albano F, Ashkenazi S et al. European Society for Paediatric Gastroenterology, Hepatology, and Nutrition/European Society for Paediatric Infectious Diseases evidence-based guidelines for the management of acute gastroenteritis in children in Europe. J. Pediatr. Gastroenterol. Nutr. 46(Suppl. 2), S81–122 (2008).
  MedlineGoogle Scholar
• 26. Rafter J. Lactic acid bacteria and cancer: mechanistic perspective. Br. J. Nutr. 88(Suppl. 1), S89–94 (2002).
  Medline CASGoogle Scholar
• 27. Legesse Bedada T, Feto TK, Awoke KS, Garedew AD, Yifat FT, Birri DJ. Probiotics for cancer alternative prevention and treatment. Biomed. Pharmacother. 129, 110409 (2020).
  MedlineGoogle Scholar
• 28. Olivares M, Laparra M, Sanz Y. Bifidobacterium longumInfluence of CECT 7347 and gliadin peptides on intestinal epithelial cell proteome. J. Agric. Food Chem. 59(14), 7666–7671 (2011).
  Medline CASGoogle Scholar
• 29. Laparra JM, Olivares M, Gallina O, Sanz Y. Bifidobacterium longum CECT 7347 modulates immune responses in a gliadin-induced enteropathy animal model. PLoS ONE 7(2), e30744 (2012).
  Medline CASGoogle Scholar
• 30. Fallani M, Young D, Scott J et al. Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics. J. Pediatr. Gastroenterol. Nutr. 51(1), 77–84 (2010).
  MedlineGoogle Scholar
• 31. Wright G, Chattree A, Jalan R. Management of hepatic encephalopathy. Int. J. Hepatol. 2011, 841407 (2011).
  Medline CASGoogle Scholar
• 32. Holte K, Krag A, Gluud LL. Systematic review and meta-analysis of randomized trials on probiotics for hepatic encephalopathy. Hepatol. Res. 42(10), 1008–1015 (2012).
  MedlineGoogle Scholar
• 33. Liu L, Li P, Liu Y, Zhang Y. Efficacy of probiotics and synbiotics in patients with nonalcoholic fatty liver disease: a meta-analysis. Dig. Dis. Sci. 64(12), 3402–3412 (2019).
  MedlineGoogle Scholar
• 34. Waigankar SS, Patel V. Role of probiotics in urogenital healthcare. J. Midlife Health. 2(1), 5–10 (2011).
  MedlineGoogle Scholar
• 35. Shen ZH, Zhu CX, Quan YS et al. Relationship between intestinal microbiota and ulcerative colitis: Mechanisms and clinical application of probiotics and fecal microbiota transplantation. World J. Gastroenterol. 24(1), 5–14 (2018).
  Medline CASGoogle Scholar
• 36. Shen J, Zuo ZX, Mao AP. Effect of probiotics on inducing remission and maintaining therapy in ulcerative colitis, Crohn's disease, and pouchitis: meta-analysis of randomized controlled trials. Inflamm. Bowel Dis. 20(1), 21–35 (2014).
  MedlineGoogle Scholar
• 37. Cain AM, Karpa KD. Clinical utility of probiotics in inflammatory bowel disease. Altern. Ther. Health Med. 17(1), 72–79 (2011).
  MedlineGoogle Scholar
• 38. Penders J, Stobberingh EE, Thijs C et al. Molecular fingerprinting of the intestinal microbiota of infants in whom atopic eczema was or was not developing. Clin. Exp. Allergy. 36(12), 1602–1608 (2006).
  Medline CASGoogle Scholar
• 39. Michail S. The role of probiotics in allergic diseases. Allergy Asthma Clin. Immunol. 5(1), 5 (2009).
  MedlineGoogle Scholar
• 40. Kiousi DE, Karapetsas A, Karolidou K, Panayiotidis MI, Pappa A, Galanis A. Probiotics in extraintestinal diseases: current trends and new directions. Nutrients. 11(4), 788 (2019).
  CASGoogle Scholar
• 41. Yoosuf S, Makharia GK. Evolving therapy for celiac disease. Front. Pediatr. 7, 193 (2019).
  MedlineGoogle Scholar
• 42. Tabrizi R, Ostadmohammadi V, Akbari M et al. The Effects of Probiotic Supplementation on Clinical Symptom, Weight Loss, Glycemic Control, Lipid and Hormonal Profiles, Biomarkers of Inflammation, and Oxidative Stress in Women with Polycystic Ovary Syndrome: a Systematic Review and Meta-analysis of Randomized Controlled Trials. Probiotics Antimicrob. Proteins. doi: https://doi.org/10.1007/s12602-019-09559-0 (2019) (Epub ahead of print).
  MedlineGoogle Scholar
• 43. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13(10), 701–712 (2012).
  Medline CASGoogle Scholar
• 44. Yatsunenko T, Rey FE, Manary MJ et al. Human gut microbiome viewed across age and geography. Nature. 486(7402), 222–227 (2012).
  Medline CASGoogle Scholar
• 45. Pacheco AR, Barile D, Underwood MA, Mills DA. The impact of the milk glycobiome on the neonate gut microbiota. Annu. Rev. Anim. Biosci. 3, 419–445 (2015).
  Medline CASGoogle Scholar
• 46. Hunt KM, Foster JA, Forney LJ et al. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS One 6(6), e21313 (2011).
  Medline CASGoogle Scholar
• 47. Rinninella E, Raoul P, Cintoni M et al. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms. 7(1), 14 (2019).
  Medline CASGoogle Scholar
• 48. Montiel-Castro AJ, Gonzalez-Cervantes RM, Bravo-Ruiseco G, Pacheco-Lopez G. The microbiota–gut–brain axis: neurobehavioral correlates, health and sociality. Front. Integr. Neurosci. 7, 70 (2013).
  Medline CASGoogle Scholar
• 49. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat. Rev. Microbiol. 10(11), 735–742 (2012).
  Medline CASGoogle Scholar
• 50. Braniste V, Al-Asmakh M, Kowal C et al. The gut microbiota influences blood–brain barrier permeability in mice. Sci. Transl. Med. 6(263), 263ra158 (2014).
  MedlineGoogle Scholar
• 51. Williams BB, Van Benschoten AH, Cimermancic P et al. Discovery and characterization of gut microbiota decarboxylases that can produce the neurotransmitter tryptamine. Cell Host Microbe. 16(4), 495–503 (2014).
  Medline CASGoogle Scholar
• 52. Sudo N. Role of microbiome in regulating the HPA axis and its relevance to allergy. Chem. Immunol. Allergy. 98, 163–175 (2012).
  Medline CASGoogle Scholar
• 53. Holmes E, Li JV, Athanasiou T, Ashrafian H, Nicholson JK. Understanding the role of gut microbiome-host metabolic signal disruption in health and disease. Trends Microbiol. 19(7), 349–359 (2011).
  Medline CASGoogle Scholar
• 54. Barrett E, Ross RP, O'Toole PW, Fitzgerald GF, Stanton C. Gamma-aminobutyric acid production by culturable bacteria from the human intestine. J. Appl. Microbiol. 113(2), 411–417 (2012).
  Medline CASGoogle Scholar
• 55. Lyte M. Probiotics function mechanistically as delivery vehicles for neuroactive compounds: Microbial endocrinology in the design and use of probiotics. Bioessays. 33(8), 574–581 (2011).
  Medline CASGoogle Scholar
• 56. Mazzoli R, Pessione E. The Neuro-endocrinological role of microbial glutamate and GABA signaling. Front. Microbiol. 7, 1934 (2016).
  MedlineGoogle Scholar
• 57. Kimura I, Inoue D, Maeda T et al. Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41). Proc. Natl Acad. Sci. USA 108(19), 8030–8035 (2011).
  Medline CASGoogle Scholar
• 58. Vecsey CG, Hawk JD, Lattal KM et al. Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J. Neurosci. 27(23), 6128–6140 (2007).
  Medline CASGoogle Scholar
• 59. Alexander KS, Pocivavsek A, Wu HQ, Pershing ML, Schwarcz R, Bruno JP. Early developmental elevations of brain kynurenic acid impair cognitive flexibility in adults: reversal with galantamine. Neuroscience 238, 19–28 (2013).
  Medline CASGoogle Scholar
• 60. Sudo N, Chida Y, Aiba Y et al. Postnatal microbial colonization programs the hypothalamic–pituitary–adrenal system for stress response in mice. J. Physiol. 558(Pt 1), 263–275 (2004).
  Medline CASGoogle Scholar
• 61. Lu B, Nagappan G, Guan X, Nathan PJ, Wren P. BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases. Nat. Rev. Neurosci. 14(6), 401–416 (2013).
  Medline CASGoogle Scholar
• 62. Clarke G, Grenham S, Scully P et al. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol. Psychiatry 18(6), 666–673 (2013).
  Medline CASGoogle Scholar
• 63. Selkrig J, Wong P, Zhang X, Pettersson S. Metabolic tinkering by the gut microbiome: implications for brain development and function. Gut Microbes 5(3), 369–380 (2014).
  MedlineGoogle Scholar
• 64. Bercik P, Denou E, Collins J et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141(2), 599–609 609.e591–593 (2011).
  Medline CASGoogle Scholar
• 65. Bravo JA, Forsythe P, Chew MV 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. USA 108(38), 16050–16055 (2011).
  Medline CASGoogle Scholar
• 66. Savignac HM, Kiely B, Dinan TG, Cryan JF. Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice. Neurogastroenterol. Motil. 26(11), 1615–1627 (2014).
  Medline CASGoogle Scholar
• 67. Messaoudi M, Lalonde R, Violle N et al. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br. J. Nutr. 105(5), 755–764 (2011).
  Medline CASGoogle Scholar
• 68. Savignac HM, Tramullas M, Kiely B, Dinan TG, Cryan JF. Bifidobacteria modulate cognitive processes in an anxious mouse strain. Behav. Brain Res. 287, 59–72 (2015).
  Medline CASGoogle Scholar
• 69. Pyndt Jorgensen B, Hansen JT, Krych L et al. A possible link between food and mood: dietary impact on gut microbiota and behavior in BALB/c mice. PLoS ONE 9(8), e103398 (2014).
  MedlineGoogle Scholar
• 70. Tillisch K, Labus J, Kilpatrick L et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144(7), 1394–1401 1401.e1391–1394 (2013).
  Medline CASGoogle Scholar
• 71. Steenbergen L, Sellaro R, van Hemert S, Bosch JA, Colzato LS. A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain Behav. Immun. 48, 258–264 (2015).
  MedlineGoogle Scholar
• 72. Stilling RM, Bordenstein SR, Dinan TG, Cryan JF. Friends with social benefits: host-microbe interactions as a driver of brain evolution and development? Front. Cell. Infect. Microbiol. 4, 147 (2014).
  MedlineGoogle Scholar
• 73. Desbonnet L, Clarke G, Shanahan F, Dinan TG, Cryan JF. Microbiota is essential for social development in the mouse. Mol. Psychiatry 19(2), 146–148 (2014).
  Medline CASGoogle Scholar
• 74. Theis KR, Venkataraman A, Dycus JA et al. Symbiotic bacteria appear to mediate hyena social odors. Proc. Natl Acad. Sci. USA 110(49), 19832–19837 (2013).
  Medline CASGoogle Scholar
• 75. Venu I, Durisko Z, Xu J, Dukas R. Social attraction mediated by fruit flies' microbiome. J. Exp. Biol. 217(Pt 8), 1346–1352 (2014).
  MedlineGoogle Scholar
• 76. Kang DW, Park JG, Ilhan ZE et al. Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children. PLoS One 8(7), e68322 (2013).
  Medline CASGoogle Scholar
• 77. Hsiao EY, McBride SW, Hsien S et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155(7), 1451–1463 (2013). •• As the findings support the connection between the gut microbiome and brain in the autism spectrum disorder mouse model and reported a potential probiotic for the therapeutic management of human neurodevelopmental disorders.
  Medline CASGoogle Scholar
• 78. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl Acad. Sci. USA 107(27), 12204–12209 (2010).
  Medline CASGoogle Scholar
• 79. de Theije CG, Wopereis H, Ramadan M et al. Altered gut microbiota and activity in a murine model of autism spectrum disorders. Brain Behav. Immun. 37, 197–206 (2014).
  Medline CASGoogle Scholar
• 80. Yano JM, Yu K, Donaldson GP et al. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161(2), 264–276 (2015).
  Medline CASGoogle Scholar
• 81. Marcobal A, Kashyap PC, Nelson TA et al. A metabolomic view of how the human gut microbiota impacts the host metabolome using humanized and gnotobiotic mice. ISME J. 7(10), 1933–1943 (2013).
  Medline CASGoogle Scholar
• 82. Gershon MD. 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract. Curr. Opin. Endocrinol. Diabetes Obes. 20(1), 14–21 (2013).
  Medline CASGoogle Scholar
• 83. Fukumoto S, Tatewaki M, Yamada T et al. Short-chain fatty acids stimulate colonic transit via intraluminal 5-HT release in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284(5), R1269–1276 (2003).
  Medline CASGoogle Scholar
• 84. O'Mahony SM, Clarke G, Borre YE, Dinan TG, Cryan JF. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav. Brain Res. 277, 32–48 (2015).
  MedlineGoogle Scholar
• 85. Wall R, Cryan JF, Ross RP, Fitzgerald GF, Dinan TG, Stanton C. Bacterial neuroactive compounds produced by psychobiotics. Adv. Exp. Med. Biol. 817, 221–239 (2014).
  Medline CASGoogle Scholar
• 86. Lucas P, Landete J, Coton M, Coton E, Lonvaud-Funel A. The tyrosine decarboxylase operon of Lactobacillus brevis IOEB 9809: characterization and conservation in tyramine-producing bacteria. FEMS Microbiol. Lett. 229(1), 65–71 (2003).
  Medline CASGoogle Scholar
• 87. Kuley E, Ozogul F, Balikci E, Durmus M, Ayas D. The influences of fish infusion broth on the biogenic amines formation by lactic acid bacteria. Braz. J. Microbiol. 44(2), 407–415 (2013).
  MedlineGoogle Scholar
• 88. Hyland NP, Cryan JF. A gut feeling about GABA: focus on GABA(B) Receptors. Front. Pharmacol. 1, 124 (2010).
  MedlineGoogle Scholar
• 89. Li Y, Xiang YY, Lu WY, Liu C, Li J. A novel role of intestine epithelial GABAergic signaling in regulating intestinal fluid secretion. Am. J. Physiol. Gastrointest. Liver Physiol. 303(4), G453–460 (2012).
  Medline CASGoogle Scholar
• 90. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9(1), 46–56 (2008). • Interesting review describing the role of Inflammation in the major depressive episodes.
  Medline CASGoogle Scholar
• 91. Dantzer R, Konsman JP, Bluthe RM, Kelley KW. Neural and humoral pathways of communication from the immune system to the brain: parallel or convergent? Auton. Neurosci. 85(1–3), 60–65 (2000).
  Medline CASGoogle Scholar
• 92. van Dam AM, Brouns M, Louisse S, Berkenbosch F. Appearance of interleukin-1 in macrophages and in ramified microglia in the brain of endotoxin-treated rats: a pathway for the induction of non-specific symptoms of sickness? Brain Res. 588(2), 291–296 (1992).
  Medline CASGoogle Scholar
• 93. Bluthe RM, Kelley KW, Dantzer R. Effects of insulin-like growth factor-I on cytokine-induced sickness behavior in mice. Brain Behav. Immun. 20(1), 57–63 (2006).
  Medline CASGoogle Scholar
• 94. Raison CL, Capuron L, Miller AH. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol. 27(1), 24–31 (2006).
  Medline CASGoogle Scholar
• 95. Ghaisas S, Maher J, Kanthasamy A. Gut microbiome in health and disease: Linking the microbiome-gut-brain axis and environmental factors in the pathogenesis of systemic and neurodegenerative diseases. Pharmacol. Ther. 158, 52–62 (2016).
  Medline CASGoogle Scholar
• 96. Dinan TG, Cryan JF. The impact of gut microbiota on brain and behaviour: implications for psychiatry. Curr. Opin. Clin. Nutr. Metab. Care. 18(6), 552–558 (2015).
  MedlineGoogle Scholar
• 97. Yarandi SS, Peterson DA, Treisman GJ, Moran TH, Pasricha PJ. Modulatory effects of gut microbiota on the central nervous system: how gut could play a role in neuropsychiatric health and diseases. J Neurogastroenterol. Motil. 22(2), 201–212 (2016).
  MedlineGoogle Scholar
• 98. Diamanti AP, Manuela Rosado M, Lagana B, D'Amelio R. Microbiota and chronic inflammatory arthritis: an interwoven link. J. Transl. Med. 14(1), 233 (2016).
  MedlineGoogle Scholar
• 99. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl Acad. Sci. USA 108(Suppl. 1), 4615–4622 (2011).
  Medline CASGoogle Scholar
• 100. Berer K, Mues M, Koutrolos M et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 479(7374), 538–541 (2011).
  Medline CASGoogle Scholar
• 101. Scheperjans F, Aho V, Pereira PA et al. Gut microbiota are related to Parkinson's disease and clinical phenotype. Mov. Disord. 30(3), 350–358 (2015).
  MedlineGoogle Scholar
• 102. Cassani E, Barichella M, Cancello R et al. Increased urinary indoxyl sulfate (indican): new insights into gut dysbiosis in Parkinson's disease. Parkinsonism Relat. Disord. 21(4), 389–393 (2015).
  MedlineGoogle Scholar
• 103. Wu S, Yi J, Zhang YG, Zhou J, Sun J. Leaky intestine and impaired microbiome in an amyotrophic lateral sclerosis mouse model. Physiol. Rep. 3(4), e12356 (2015).
  MedlineGoogle Scholar
• 104. Tremlett H, Fadrosh DW, Faruqi AA et al. Gut microbiota composition and relapse risk in pediatric MS: A pilot study. J. Neurol. Sci. 363, 153–157 (2016).
  MedlineGoogle Scholar
• 105. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience. 170(4), 1179–1188 (2010). •• Describing the role for Bifidobacteria in neural function.
  Medline CASGoogle Scholar
• 106. Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG. The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J. Psychiatr. Res. 43(2), 164–174 (2008).
  MedlineGoogle Scholar
• 107. Janik R, Thomason LAM, Stanisz AM, Forsythe P, Bienenstock J, Stanisz GJ. Magnetic resonance spectroscopy reveals oral Lactobacillus promotion of increases in brain GABA, N-acetyl aspartate and glutamate. Neuroimage. 125, 988–995 (2016).
  Medline CASGoogle Scholar
• 108. O'Mahony SM, Marchesi JR, Scully P et al. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol. Psychiatry. 65(3), 263–267 (2009).
  MedlineGoogle Scholar
• 109. Donato KA, Gareau MG, Wang YJ, Sherman PM. Lactobacillus rhamnosus GG attenuates interferon-{gamma} and tumour necrosis factor-alpha-induced barrier dysfunction and pro-inflammatory signalling. Microbiology 156(Pt 11), 3288–3297 (2010).
  Medline CASGoogle Scholar
• 110. Felger JC, Lotrich FE. Inflammatory cytokines in depression: neurobiological mechanisms and therapeutic implications. Neuroscience 246, 199–229 (2013).
  Medline CASGoogle Scholar
• 111. Miller AH, Haroon E, Raison CL, Felger JC. Cytokine targets in the brain: impact on neurotransmitters and neurocircuits. Depress Anxiety 30(4), 297–306 (2013).
  Medline CASGoogle Scholar
• 112. Kato-Kataoka A, Nishida K, Takada M et al. Fermented milk containing lactobacillus casei strain shirota preserves the diversity of the gut microbiota and relieves abdominal dysfunction in healthy medical students exposed to academic stress. Appl. Environ. Microbiol. 82(12), 3649–3658 (2016).
  Medline CASGoogle Scholar
• 113. Benton D, Williams C, Brown A. Impact of consuming a milk drink containing a probiotic on mood and cognition. Eur. J. Clin. Nutr. 61(3), 355–361 (2007).
  Medline CASGoogle Scholar
• 114. Akkasheh G, Kashani-Poor Z, Tajabadi-Ebrahimi M et al. Clinical and metabolic response to probiotic administration in patients with major depressive disorder: a randomized, double-blind, placebo-controlled trial. Nutrition 32(3), 315–320 (2016).
  Medline CASGoogle Scholar
• 115. Allen AP, Hutch W, Borre YE et al. Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers. Transl. Psychiatry 6(11), e939 (2016).
  Medline CASGoogle Scholar
• 116. Rao AV, Bested AC, Beaulne TM et al. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog. 1(1), 6 (2009).
  MedlineGoogle Scholar
• 117. Takada M, Nishida K, Gondo Y et al. Beneficial effects of Lactobacillus casei strain Shirota on academic stress-induced sleep disturbance in healthy adults: a double-blind, randomised, placebo-controlled trial. Benef. Microbes. 8(2), 153–162 (2017).
  Medline CASGoogle Scholar
• 118. Kaluzna-Czaplinska J, Blaszczyk S. The level of arabinitol in autistic children after probiotic therapy. Nutrition 28(2), 124–126 (2012).
  Medline CASGoogle Scholar
• 119. Akbari E, Asemi Z, Daneshvar Kakhaki R et al. Effect of probiotic supplementation on cognitive function and metabolic status in Alzheimer's disease: a randomized, double-blind and controlled trial. Front. Aging Neurosci. 8, 256 (2016).
  MedlineGoogle Scholar
• 120. Bharwani A, Mian MF, Surette MG, Bienenstock J, Forsythe P. Oral treatment with Lactobacillus rhamnosus attenuates behavioural deficits and immune changes in chronic social stress. BMC Med. 15(1), 7 (2017).
  MedlineGoogle Scholar
• 121. Davari S, Talaei SA, Alaei H, Salami M. Probiotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: behavioral and electrophysiological proofs for microbiome–gut–brain axis. Neuroscience. 240, 287–296 (2013).
  Medline CASGoogle Scholar
• 122. Kouchaki E, Tamtaji OR, Salami M et al. Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: a randomized, double-blind, placebo-controlled trial. Clin. Nutr. 36(5), 1245–1249 (2017).
  Medline CASGoogle Scholar
• 123. Liang S, Wang T, Hu X et al. Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress. Neuroscience. 310, 561–577 (2015).
  Medline CASGoogle Scholar
• 124. Aziz Q, Dore J, Emmanuel A, Guarner F, Quigley EM. Gut microbiota and gastrointestinal health: current concepts and future directions. Neurogastroenterol. Motil. 25(1), 4–15 (2013).
  Medline CASGoogle Scholar
• 125. Mitew S, Kirkcaldie MT, Dickson TC, Vickers JC. Altered synapses and gliotransmission in Alzheimer's disease and AD model mice. Neurobiol. Aging. 34(10), 2341–2351 (2013).
  Medline CASGoogle Scholar
• 126. Talaei SA, Azami A, Salami M. Postnatal development and sensory experience synergistically underlie the excitatory/inhibitory features of hippocampal neural circuits: glutamatergic and GABAergic neurotransmission. Neuroscience 318, 230–243 (2016).
  Medline CASGoogle Scholar