Effects of the intestinal microbiota on epigenetic mechanisms involved in the development of post-stress neuro-inflammation

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Abstract

A number of alleles of polymorphic genes, dysfunctions of the hypothalamic-pituitary-adrenal axis, neurotransmitter disorders, and manifestations of immune dysregulation are associated with vulnerability to stress. Post-stress states of humans and animals are accompanied by signs of neuroinflammation, the causes and mechanisms of which remain to be elucidated. The article discusses epigenetic mechanisms by which the intestinal microbiota might participate in the initiation and maintenance of post-stress inflammation.

About the authors

Irina G. Shalaginova

Immanuel Kant Baltic Federal University

Author for correspondence.
Email: shalaginova_i@mail.ru
ORCID iD: 0000-0002-0140-3077
SPIN-code: 1160-1915
Scopus Author ID: 57202052229
ResearcherId: J-3626-2018

Senior Lecturer, School of Life Science

Russian Federation, ul. Nevskogo, 14, Kaliningrad, 236041

Liudmila V. Matskova

Immanuel Kant Baltic Federal University
 

Email: liudmila.matskova@ki.se
ORCID iD: 0000-0002-3174-1560
SPIN-code: 4756-7437
Scopus Author ID: 6507748788
ResearcherId: F-3003-2016

PhD, professor-researcher, Microbiology and Biotechnology Unit of School of Life Science

Russian Federation, ul. Nevskogo, 14, Kaliningrad, 236041

Natalia M. Gunitseva

Immanuel Kant Baltic Federal University
 

Email: nat-gun@mail.ru

student in Bioengineering and bioinformatics, School of Life Science

Russian Federation, ul. Nevskogo, 14, Kaliningrad, 236041

Irina A. Vakoliuk

Immanuel Kant Baltic Federal University
 

Email: vakoluk@mail.ru
ORCID iD: 0000-0001-5480-1645
SPIN-code: 2378-7129
Scopus Author ID: 7801465798

PhD, associate professor, School of Life Science

Russian Federation, ul. Nevskogo, 14, Kaliningrad, 236041

References

  1. Jenkins T, Nguyen J, Polglaze K, Bertrand P. Influence of tryptophan and serotonin on mood and cognition with a possible role of the gut-brain axis. Nutrients. 2016;8(1). pii: E56. https://doi.org/10.3390/nu8010056.
  2. Schmidt C. Thinking from the gut. Nature. 2015; 518(7540): S12-S15. https://doi.org/10.1038/518s13a.
  3. Smith P. The tantalizing links between gut microbes and the brain. Nature. 2015;526(7573):312-314. https://doi.org/10.1038/526312a.
  4. Mayer E, Knight R, Mazmanian S, et al. Gut microbes and the brain: paradigm shift in neuroscience. J Neurosci. 2014;34(46):15490-15496. https://doi.org/10.1523/jneurosci.3299-14.2014.
  5. Diaz Heijtz R, Wang S, Anuar F, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA. 2011;108(7):3047-3052. https://doi.org/10.1073/pnas.1010529108.
  6. Wang H, Wang Y. Gut microbiota-brain axis. Chin Med J. 2016;129(19):2373-2380. https://doi.org/10.4103/ 0366-6999.190667
  7. Sudo N, Chida Y, Aiba Y, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol. 2004;558(Pt 1):263-275. https://doi.org/ 10.1113/jphysiol.2004.063388.
  8. Erny D, Hrabě de Angelis A, Jaitin D, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci. 2015;18(7):965-977. https://doi.org/10.1038/nn.4030.
  9. Deslauriers J, Powell S, Risbrough V. Immune signaling mechanisms of PTSD risk and symptom development: insights from animal models. Curr Opin Behav Sci. 2017;14:123-132. https://doi.org/10.1016/j.cobeha.2017.01.005.
  10. DiSabato DJ, Quan N, Godbout JP. Neuroinflammation: the devil is in the details. J Neurochem. 2016;139 Suppl 2:136-153. https://doi.org/10.1111/jnc.13607.
  11. Calcia MA, Bonsall DR, Bloomfield PS, et al. Stress and neuroinflammation: a systematic review of the effects of stress on microglia and the implications for mental illness. Psychopharmacology. 2016;233(9):1637-1650. https://doi.org/ 10.1007/s00213-016-4218-9.
  12. Rooks MG, Veiga P, Wardwell-Scott LH, et al. Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission. ISME J. 2014;8(7):1403-17. https://doi.org/10.1038/ismej.2014.3.
  13. Deans C, Maggert KA. What do you mean, “epigenetic”? Genetics. 2015;199(4):887-896. https://doi.org/10.1534/genetics.114.173492.
  14. Dave M, Higgins P, Middha S, Rioux K. The human gut microbiome: current knowledge, challenges, and future directions. Transl Res. 2012;160(4):246-257. https://doi.org/10.1016/j.trsl.2012.05.003.
  15. Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14(8): e1002533. https://doi.org/10.1371/journal.pbio.1002533.
  16. Eckburg P. Diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635-1638. https://doi.org/10.1126/science.1110591.
  17. Douglas-Escobar M, Elliott E, Neu J. Effect of intestinal microbial ecology on the developing brain. JAMA Pediatr. 2013;167(4):374-379. https://doi.org/10.1001/jamapediatrics.2013.497.
  18. Al-Asmakh M, Anuar F, Zadjali F, et al. Gut microbial communities modulating brain development and function. Gut Microbes. 2012;3(4):366-373. https://doi.org/10.4161/gmic.21287.
  19. Jiménez E, Fernández L, Marín M, et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol. 2005;51(4):270-274. https://doi.org/10.1007/s00284-005-0020-3.
  20. Satokari R, Grönroos T, Laitinen K, et al. Bifidobacterium and lactobacillus DNA in the human placenta. Lett Appl Microbiol. 2009;48(1):8-12. https://doi.org/10.1111/j.1472-765x.2008.02475.x.
  21. Jiménez E, Marín M, Martín R, et al. Is meconium from healthy newborns actually sterile? Res Microbiol. 2008;159(3):187-193. https://doi.org/10.1016/j.resmic.2007.12.007.
  22. Hooper L, Littman D, Macpherson A. Interactions between the microbiota and the immune system. Science. 2012;336(6086):1268-1273. https://doi.org/10.1126/science.1223490.
  23. Clarke G, O’Mahony S, Dinan T, Cryan J. Priming for health: gut microbiota acquired in early life regulates physiology, brain and behaviour. Acta Paediatr. 2014;103(8):812-819. https://doi.org/10.1111/apa.12674.
  24. Rook G, Lowry C, Raison C. Microbial “Old Friends”, immunoregulation and stress resilience. Evol Med Public Health. 2013;2013(1):46-64. https://doi.org/10.1093/emph/eot004.
  25. Puddu A, Sanguineti R, Montecucco F, Viviani G. Evidence for the gut microbiota short-chain fatty acids as key pathophysiological molecules improving diabetes. Mediators Inflamm. 2014;2014:162021. https://doi.org/10.1155/2014/162021.
  26. Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):1332-1345. https://doi.org/10.1016/j.cell.2016.05.041.
  27. Macpherson A, Harris N. Interactions between commensal intestinal bacteria and the immune system. Nature Rev Immunol. 2004;4(6):478-485. https://doi.org/10.1038/nri1373.
  28. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118(2):229-241. https://doi.org/10.1016/j.cell.2004.07.002.
  29. Petra A, Panagiotidou S, Hatziagelaki E, et al. Gut-microbiota-brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clin Ther. 2015;37(5):984-995. https://doi.org/10.1016/j.clinthera.2015.04.002.
  30. Ogilvie L, Jones B. The human gut virome: a multifaceted majority. Front Microbiol. 2015;6. https://doi.org/10.3389/fmicb.2015.00918.
  31. Molloy M, Grainger J, Bouladoux N, et al. Intraluminal containment of commensal outgrowth in the gut during infection-induced dysbiosis. Cell Host Microbe. 2013;14(3):318-328. https://doi.org/10.1016/j.chom.2013.08.003.
  32. Foster J, McVey Neufeld KА. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 2013;36(5):305-312. https://doi.org/10.1016/j.tins.2013.01.005.
  33. Rackers H, Thomas S, Williamson K, et al. Emerging literature in the microbiota-brain axis and perinatal mood and anxiety disorders. Psychoneuroendocrinology. 2018;95:86-96. https://doi.org/10.1016/j.psyneuen.2018.05.020.
  34. Marshall J, Thabane M, Garg A, et al. Eight year prognosis of postinfectious irritable bowel syndrome following waterborne bacterial dysentery. Gut. 2010;59(5):605-611. https://doi.org/10.1136/gut.2009.202234.
  35. De Angelis M, Piccolo M, Vannini L, et al. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS One. 2013;8(10): e76993. https://doi.org/10.1371/journal.pone.0076993.
  36. Abot A, Cani P, Knauf C. Impact of intestinal peptides on the enteric nervous system: novel approaches to control glucose metabolism and food intake. Front Endocrinol (Lausanne). 2018;9. https://doi.org/10.3389/fendo.2018.00328.
  37. Kaelberer MM, Buchanan KL, Klein ME, et al. A gut-brain neural circuit for nutrient sensory transduction. Science. 2018;361(6408). pii: eaat5236. https://doi.org/10.1126/science.aat5236.
  38. Schumacher S, Niemeyer H, Engel S, et al. HPA axis regulation in posttraumatic stress disorder: A meta-analysis focusing on potential moderators. Neurosci Biobehav Rev. 2019;100:35-57. https://doi.org/10.1016/j.neubiorev.2019.02.005.
  39. Desbonnet L, Garrett L, Clarke G, et al. Effects of the probiotic bifidobacterium infantis in the maternal separation model of depression. Neurosci. 2010;170(4):1179-1188. https://doi.org/10.1016/j.neuroscience.2010.08.005.
  40. O’Mahony S, Hyland N, Dinan T, Cryan J. Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology (Berl). 2010;214(1):71-88. https://doi.org/10.1007/s00213-010-2010-9.
  41. Bangsgaard Bendtsen K, Krych L, Sørensen D, et al. Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. PLoS One. 2012;7(10):e46231. https://doi.org/10.1371/journal.pone.0046231.
  42. Deng H, Yang S, Zhang Y, et al. Bacteroides fragilis prevents clostridium difficile infection in a mouse model by restoring gut barrier and microbiome regulation. Front Microbiol. 2018;9. https://doi.org/10.3389/fmicb.2018.02976.
  43. McKernan D, Dennison U, Gaszner G, et al. Enhanced peripheral toll-like receptor responses in psychosis: further evidence of a pro-inflammatory phenotype. Transl Psychiatry. 2011;1(8): e36-e36. https://doi.org/10.1038/tp.2011.37.
  44. Bourassa M, Alim I, Bultman S, Ratan R. Butyrate, neuroepigenetics and the gut microbiome: can a high fiber diet improve brain health? Neurosci Lett. 2016;625:56-63. https://doi.org/10.1016/j.neulet.2016.02.009.
  45. Usami M, Kishimoto K, Ohata A, et al. Butyrate and trichostatin a attenuate nuclear factor κB activation and tumor necrosis factor α secretion and increase prostaglandin E2 secretion in human peripheral blood mononuclear cells. Nutr Res. 2008;28(5):321-328. https://doi.org/10.1016/j.nutres.2008.02.012.
  46. Vinolo M, Rodrigues H, Nachbar R, Curi R. Regulation of inflammation by short chain fatty acids. Nutrients. 2011;3(10):858-876. https://doi.org/10.3390/nu3100858.
  47. Dalile B, van Oudenhove L, Vervliet B, Verbeke K. The role of short-chain fatty acids in microbiota-gut-brain communication. Nat Rev Gastroenterol Hepatol. 2019;16(8):461-478. https://doi.org/10.1038/s41575-019-0157-3.
  48. Erny D, Hrabě de Angelis AL, Prinz M. Communicating systems in the body: how microbiota and microglia cooperate. Immunol. 2017;150(1):7-15. https://doi.org/10.1111/imm.12645.
  49. Cryan J, Dinan T. Microbiota and neuroimmune signaling – metchnikoff to microglia. Nat Rev Gastroenterol Hepatol. 2015;12(9):494-496. https://doi.org/10.1038/nrgastro.2015.127.
  50. Fu SP, Wang JF, Xue WJ, et al. Anti-inflammatory effects of BHBA in both in vivo and in vitro Parkinson’s disease models are mediated by GPR109A-dependent mechanisms. J Neuroinflammation. 2015;12(1):9. https://doi.org/10.1186/s12974-014-0230-3.
  51. Paul B, Barnes S, Demark-Wahnefried W, et al. Influences of diet and the gut microbiome on epigenetic modulation in cancer and other diseases. Clin Epigenetics. 2015;7(1):112. https://doi.org/10.1186/s13148-015-0144-7.
  52. Hesson LB. Gut microbiota and obesity-related gastrointestinal cancer: a focus on epigenetics. Translational Gastrointestinal Cancer. 2013;2(4):204-210. https://doi.org/10.3978/j.issn.2224-4778.2013. 10.03.
  53. Eraly S, Nievergelt C, Maihofer A, et al. Assessment of plasma C-reactive protein as a biomarker of posttraumatic stress disorder risk. JAMA Psychiatry. 2014;71(4):423-431. https://doi.org/10.1001/jamapsychiatry.2013.4374.
  54. Van Zuiden M, Heijnen C, Maas M, et al. Glucocorticoid sensitivity of leukocytes predicts PTSD, depressive and fatigue symptoms after military deployment: a prospective study. Psychoneuroendocrinology. 2012;37(11):1822-1836. https://doi.org/10.1016/j.psyneuen.2012.03.018.
  55. Wohleb E, Patterson J, Sharma V, et al. Knockdown of interleukin-1 receptor type-1 on endothelial cells attenuated stress-induced neuroinflammation and prevented anxiety-like behavior. J Neurosci. 2014;34(7):2583-2591. https://doi.org/10.1523/jneurosci.3723-13.2014.
  56. Bilbo S, Levkoff L, Mahoney J, et al. Neonatal infection induces memory impairments following an immune challenge in adulthood. Behav Neurosci. 2005;119(1):293-301. https://doi.org/10.1037/0735-7044.119.1.293.
  57. Goehler L, Park S, Opitz N, et al. Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior. Brain Behav Immunol. 2008;22(3):354-366. https://doi.org/10.1016/j.bbi.2007.08.009.
  58. Malan-Muller S, Valles-Colomer M, Raes J, et al. The gut microbiome and mental health: implications for anxiety- and trauma-related disorders. OMICS. 2018;22(2):90-107. https://doi.org/10.1089/omi.2017.0077.
  59. Reber S, Slattery D. Editorial: using stress-based animal models to understand the mechanisms underlying psychiatric and somatic disorders. Front Psychiatry. 2016;7:192. https://doi.org/10.3389/fpsyt.2016.00192.
  60. Minakova E, Warner B. Maternal immune activation, central nervous system development and behavioral phenotypes. Birth Defects Res. 2018;110(20): 1539-1550. https://doi.org/10.1002/bdr2.1416.
  61. Alam R, Abdolmaleky H, Zhou J. Microbiome, inflammation, epigenetic alterations, and mental diseases. Am J Med Genet B Neuropsychiatr Genet. 2017;174(6): 651-660. https://doi.org/10.1002/ajmg.b.32567.
  62. Gur T, Shay L, Palkar A, et al. Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring. Brain Behav Immunol. 2017;64:50-58. https://doi.org/10.1016/j.bbi.2016.12.021.
  63. Дюжикова Н.А., Даев Е.В. Геном и стресс-реакция у животных и человека // Экологическая генетика. – 2018. – Т. 16. – № 1. – С. 4-26. [Dyuzhikova NA, Daev EV. Genome and stress-reaction in animals and humans. Ecological genetics. 2018;16(1):4-26. (In Russ.)]. https://doi.org/10.17816/ecogen1614-26.
  64. Cheng Y, Bernstein A, Chen D, Jin P. 5-Hydroxymethylcytosine: a new player in brain disorders? Exp Neurol. 2015;268:3-9. https://doi.org/10.1016/j.expneurol.2014.05.008.
  65. Roth S, Denu J, Allis C. Histone acetyltransferases. Annu Rev Biochem. 2001;70:81-120. https://doi.org/10.1146/annurev.biochem.70.1.81.
  66. Rusiecki J, Byrne C, Galdzicki Z, et al. PTSD and DNA methylation in select immune function gene promoter regions: a repeated measures case-control study of u. s. military service members. Front Psychiatry. 2013;4:56. https://doi.org/10.3389/fpsyt.2013. 00056.
  67. Uddin M, Aiello A, Wildman D, et al. Epigenetic and immune function profiles associated with posttraumatic stress disorder. Proc Natl Acad Sci USA. 2010;107(20):9470-9475. https://doi.org/10.1073/pnas.0910794107.
  68. Zannas A, Provençal N, Binder E. Epigenetics of posttraumatic stress disorder: current evidence, challenges, and future directions. Biol Psychiatry. 2015;78(5): 327-335. https://doi.org/10.1016/j.biopsych.2015.04.003.
  69. Niwa T, Tsukamoto T, Toyoda T, et al. Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells. Cancer Res. 2010;70(4):1430-1440. https://doi.org/10.1158/0008-5472.can-09-2755.
  70. Sepulveda A, Yao Y, Yan W, et al. CpG methylation and reduced expression of O6-methylguanine DNA methyltransferase is associated with Helicobacter pylori infection. Gastroenterology. 2010;138(5):1836-1844. https://doi.org/10.1053/j.gastro.2009.12.042.
  71. Jose L, Ramachandran R, Bhagavat R, et al. Hypothetical protein Rv3423.1 of Mycobacterium tuberculosis is a histone acetyltransferase. FEBS J. 2015;283(2): 265-281. https://doi.org/10.1111/febs.13566.
  72. Yaseen I, Kaur P, Nandicoori V, Khosla S. Mycobacteria modulate host epigenetic machinery by Rv1988 methylation of a non-tail arginine of histone H3. Nat Commun. 2015;6:8922. https://doi.org/10.1038/ncomms9922.
  73. Marjoram L, Alvers A, Deerhake M, et al. Epigenetic control of intestinal barrier function and inflammation in zebrafish. Proc Natl Acad Sci USA. 2015;112(9):2770-5. https://doi.org/10.1073/pnas.1424089112.
  74. Zhu J, Yamane H, Paul W. Differentiation of effector CD4 T cell populations. Annu Rev Immunol. 2010;28:445-489. https://doi.org/10.1146/annurev-immunol-030409-101212.
  75. Karberg S. Switching on epigenetic therapy. Cell. 2009;139(6):1029-1031. https://doi.org/10.1016/j.cell.2009.11.038.
  76. Parkes G. An overview of probiotics and prebiotics. Nurs Stand. 2007;21(20):43-47. https://doi.org/10.7748/ns2007.01.21.20.43.c4510.
  77. Sarkar A, Lehto S, Harty S, et al. Psychobiotics and the manipulation of bacteria-gut-brain signals. Trends Neurosci. 2016;39(11):763-781. https://doi.org/10.1016/j.tins.2016.09.002.
  78. Collado M, Isolauri E, Salminen S. Specific probiotic strains and their combinations counteract adhesion of Enterobacter sakazakii to intestinal mucus. FEMS Microbiol Lett. 2008;285(1):58-64. https://doi.org/10.1111/j.1574-6968.2008.01211.x.
  79. Liu Z, Shi C, Yang J, et al. Molecular regulation of the intestinal epithelial barrier: implication in human diseases. Front Biosci (Landmark Ed). 2011;16: 2903-2909. https://doi.org/10.2741/3888.
  80. Kunze W, Mao Y, Wang B, et al. Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J Cell Mol Med. 2009;13(8B):2261-2270. https://doi.org/10.1111/j.1582-4934.2009.00686.x.
  81. Rousseaux C, Thuru X, Gelot A, et al. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med. 2007;13(1):35-37. https://doi.org/10.1038/nm1521.
  82. Sanders M. Impact of probiotics on colonizing microbiota of the gut. J Clin Gastroenterol. 2011;45 Suppl: S115-9. https://doi.org/10.1097/mcg.0b013e318227414a.
  83. Linares D, Ross P, Stanton C. Beneficial microbes: the pharmacy in the gut. Bioengineered. 2016;7(1): 11-20. https://doi.org/10.1080/21655979.2015. 1126015.
  84. Suskind D, Singh N, Nielson H, Wahbeh G. Fecal microbial transplant via nasogastric tube for active pediatric ulcerative colitis. J Pediatr Gastroenterol Nutr. 2015;60(1):27-29. https://doi.org/ 10.1097/mpg.0000000000000544.
  85. Patel R, DuPont H. New approaches for bacteriotherapy: prebiotics, new-generation probiotics, and synbiotics. Clin Infect Dis. 2015;60 Suppl 2: S108-121. https://doi.org/10.1093/cid/civ177.
  86. Абдурасулова И.Н., Софонова А.Ф., Сизов В.В., и др. Действие различных пробиотиков на двигательную и ориентировочно-исследовательскую активность крыс // Здоровье — основа человеческого потенциала: проблемы и пути их решения. – 2015. – Т. 10. – № 2. – С. 1047–1050. [Abdurasulova IN, Sofonova AF, Sizov VV, et al. Effect of probiotics on locomotor and orienting-exploratory activity of rats. Zdorov’ye – osnova chelovecheskogo potentsiala: problemy i puti ikh resheniya. 2015;10(2):1047-1050. (In Russ.)]
  87. Абдурасулова И.Н., Тарасова Е.А., Мацулевич А.В., и др. Изменение качественного и количественного состава кишечной микробиоты у крыс в течение экспериментального аллергического энцефаломиелита // Российский физиологический журнал им. И.М. Сеченова. – 2015. – Т. 101. – № 11. – С. 1235–1249. [Abdurasulova IN, Tarasova EA, Matsulevich AV, et al. Changes in the qualitative and quantitative composition of gut microbiota in rats during experimental allergic encephalomyelitis. Russian journal of physiology. 2015;101(11):1235-1249. (In Russ.)]
  88. Абдурасулова И.Н., Тарасова Е.А., Ермоленко Е.И., и др. Enterococcus faecium L3 корректирует микробиотику кишечника и модулирует иммунные функции у крыс с ЭАЭ и пациентов с рассеянным склерозом // Журнал неврологии и психиатрии им. С.С. Корсакова. – 2015. – Т. 115. – № 8–2. – С. 45–45. [Abdurasulova IN, Tarasova EA, Ermolenko EI, et al. Enterococcus faecium L3 korrektiruet mikrobiotiku kishechnika i moduliruet immunnye funktsii u krys s EAE i patsientov s rassejannym sklerozom. Zhurnal nevrologii i psikhiatrii im. SS Korsakova. 2015;115(8-2):45-45. (In Russ.)]. https://doi.org/10.17116/jnevro20151158245-102.
  89. Cowan C, Callaghan B, Richardson R. The effects of a probiotic formulation (Lactobacillus rhamnosus and L. helveticus) on developmental trajectories of emotional learning in stressed Infant rats. Transl Psychiatry. 2016;6(5): e823. https://doi.org/10.1038/tp.2016.94.
  90. Foster J, Lyte M, Meyer E, Cryan J. Gut microbiota and brain function: an evolving field in neuroscience. Int J Neuropsychopharmacol. 2016;19(5). pii: pyv114. https://doi.org/10.1093/ijnp/pyv114.
  91. Tomasik J, Yolken R, Bahn S, Dickerson F. Immunomodulatory effects of probiotic supplementation in schizophrenia patients: a randomized, placebo-controlled trial. Biomark Insights. 2015;10:47-54. https://doi.org/10.4137/bmi.s22007.
  92. Severance E, Gressitt K, Stallings C, et al. Probiotic normalization of Candida albicans in schizophrenia: a randomized, placebo-controlled, longitudinal pilot study. Brain Behav Immun. 2017;62:41-45. https://doi.org/10.1016/j.bbi.2016.11.019.
  93. Pirbaglou M, Katz J, de Souza R, et al. Probiotic supplementation can positively affect anxiety and depressive symptoms: a systematic review of randomized controlled trials. Nutr Res. 2016;36(9):889-898. https://doi.org/10.1016/j.nutres.2016.06.009.
  94. McKean J, Naug H, Nikbakht E, et al. Probiotics and subclinical psychological symptoms in healthy participants: a systematic review and meta-analysis. J Altern Complement Med. 2017;23(4):249-258. https://doi.org/10.1089/acm.2016.0023.

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