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Abstract

Depression remains one of the most prevalent psychiatric disorders, with many patients not responding adequately to available treatments. Chronic or early-life stress is one of the key risk factors for depression. In addition, a growing body of data implicates chronic inflammation as a major player in depression pathogenesis. More recently, the gut microbiota has emerged as an important regulator of brain and behavior and also has been linked to depression. However, how this holy trinity of risk factors interact to maintain physiological homeostasis in the brain and body is not fully understood. In this review, we integrate the available data from animal and human studies on these three factors in the etiology and progression of depression. We also focus on the processes by which this microbiota-immune-stress matrix may influence centrally mediated events and on possible therapeutic interventions to correct imbalances in this triune.

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2020-01-04
2024-10-12
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Literature Cited

  1. Ahmetspahic D, Schwarte K, Ambree O, Burger C, Falcone V et al. 2018. Altered B cell homeostasis in patients with major depressive disorder and normalization of CD5 surface expression on regulatory B cells in treatment responders. J. Neuroimmune Pharmacol. 13:90–99
    [Google Scholar]
  2. Ait-Belgnaoui A, Colom A, Braniste V, Ramalho L, Marrot A et al. 2014. Probiotic gut effect prevents the chronic psychological stress-induced brain activity abnormality in mice. Neurogastroenterol. Motil. 26:510–20
    [Google Scholar]
  3. Ait-Belgnaoui A, Durand H, Cartier C, Chaumaz G, Eutamene H et al. 2012. Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology 37:1885–95
    [Google Scholar]
  4. Akbaraly T, Sexton C, Zsoldos E, Mahmood A, Filippini N et al. 2018. Association of long-term diet quality with hippocampal volume: longitudinal cohort study. Am. J. Med. 131:1372–81.e4
    [Google Scholar]
  5. Alcocer-Gómez E, Casas-Barquero N, Williams MR, Romero-Guillena SL, Cañadas-Lozano D et al. 2017. Antidepressants induce autophagy dependent-NLRP3-inflammasome inhibition in major depressive disorder. Pharmacol. Res. 121:114–21
    [Google Scholar]
  6. Allen AP, Dinan TG, Clarke G, Cryan JF 2017. A psychology of the human brain-gut-microbiome axis. Soc. Personal. Psychol. Compass 11:e12309
    [Google Scholar]
  7. Allen AP, Hutch W, Borre YE, Kennedy PJ, Temko A et al. 2016. Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers. Transl. Psychiatry 6:e939
    [Google Scholar]
  8. Allen AP, Kennedy PJ, Cryan JF, Dinan TG, Clarke G 2014. Biological and psychological markers of stress in humans: focus on the Trier Social Stress Test. Neurosci. Biobehav. Rev. 38:94–124
    [Google Scholar]
  9. Altman J, Das GD. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124:319–35
    [Google Scholar]
  10. Anderson SC, Cryan JF, Dinan TG 2017. The Psychobiotic Revolution: Mood, Food, and the New Science of the Gut-Brain Connection Washington, DC: Natl. Geogr.
    [Google Scholar]
  11. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M 2011. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav. Immun. 25:397–407
    [Google Scholar]
  12. Baker M. 2016. 1,500 scientists lift the lid on reproducibility: Survey sheds light on the “crisis” rocking research. Nature May 25. https://www.nature.com/news/1-500-scientists-lift-the-lid-on-reproducibility-1.19970
    [Google Scholar]
  13. Bale TL, Epperson CN. 2015. Sex differences and stress across the lifespan. Nat. Neurosci. 18:1413
    [Google Scholar]
  14. Banks WA. 2016. From blood–brain barrier to blood–brain interface: new opportunities for CNS drug delivery. Nat. Rev. Drug Discov. 15:275
    [Google Scholar]
  15. Barouei J, Moussavi M, Hodgson DM 2012. Effect of maternal probiotic intervention on HPA axis, immunity and gut microbiota in a rat model of irritable bowel syndrome. PLOS ONE 7:e46051
    [Google Scholar]
  16. Bekhbat M, Neigh GN. 2018. Sex differences in the neuro-immune consequences of stress: focus on depression and anxiety. Brain Behav. Immun. 67:1–12
    [Google Scholar]
  17. Belkaid Y, Hand TW. 2014. Role of the microbiota in immunity and inflammation. Cell 157:121–41
    [Google Scholar]
  18. Belleau EL, Treadway MT, Pizzagalli DA 2019. The impact of stress and major depressive disorder on hippocampal and medial prefrontal cortex morphology. Biol. Psychiatry 85:443–53
    [Google Scholar]
  19. Benakis C, Brea D, Caballero S, Faraco G, Moore J et al. 2016. Commensal microbiota affects ischemic stroke outcome by regulating intestinal γδ T cells. Nat. Med. 22:516
    [Google Scholar]
  20. Bercik P, Denou E, Collins J, Jackson W, Lu J et al. 2011. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141:599–609.e3
    [Google Scholar]
  21. Berer K, Gerdes LA, Cekanaviciute E, Jia X, Xiao L et al. 2017. Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. PNAS 114:10719
    [Google Scholar]
  22. Bharwani A, Mian MF, Foster JA, Surette MG, Bienenstock J, Forsythe P 2016. Structural & functional consequences of chronic psychosocial stress on the microbiome & host. Psychoneuroendocrinology 63:217–27
    [Google Scholar]
  23. Biggio F, Gorini G, Utzeri C, Olla P, Marrosu F et al. 2009. Chronic vagus nerve stimulation induces neuronal plasticity in the rat hippocampus. Int. J. Neuropsychopharmacol. 12:1209–21
    [Google Scholar]
  24. Boldrini M, Fulmore CA, Tartt AN, Simeon LR, Pavlova I et al. 2018. Human hippocampal neurogenesis persists throughout aging. Cell Stem Cell 22:589–99.e5
    [Google Scholar]
  25. Boldrini M, Hen R, Underwood MD, Rosoklija GB, Dwork AJ et al. 2012. Hippocampal angiogenesis and progenitor cell proliferation are increased with antidepressant use in major depression. Biol. Psychiatry 72:562–71
    [Google Scholar]
  26. Borsini A, Zunszain PA, Thuret S, Pariante CM 2015. The role of inflammatory cytokines as key modulators of neurogenesis. Trends Neurosci 38:145–57
    [Google Scholar]
  27. Brachman RA, Lehmann ML, Maric D, Herkenham M 2015. Lymphocytes from chronically stressed mice confer antidepressant-like effects to naive mice. J. Neurosci. 35:1530–38
    [Google Scholar]
  28. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM et al. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. PNAS 108:16050–55
    [Google Scholar]
  29. Burokas A, Arboleya S, Moloney RD, Peterson VL, Murphy K et al. 2017. Targeting the microbiota-gut-brain axis: Prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol. Psychiatry 82:472–87
    [Google Scholar]
  30. Capuron L, Miller AH. 2011. Immune system to brain signaling: neuropsychopharmacological implications. Pharmacol. Ther. 130:226–38
    [Google Scholar]
  31. Cekanaviciute E, Yoo BB, Runia TF, Debelius JW, Singh S et al. 2017. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. PNAS 114:10713
    [Google Scholar]
  32. Ceylani T, Jakubowska-Dogru E, Gurbanov R, Teker HT, Gozen AG 2018. The effects of repeated antibiotic administration to juvenile BALB/c mice on the microbiota status and animal behavior at the adult age. Heliyon 4:e00644
    [Google Scholar]
  33. Chourbaji S, Urani A, Inta I, Sanchis-Segura C, Brandwein C et al. 2006. IL-6 knockout mice exhibit resistance to stress-induced development of depression-like behaviors. Neurobiol. Dis. 23:587–94
    [Google Scholar]
  34. Clark SM, Song C, Li X, Keegan AD, Tonelli LH 2019. CD8+ T cells promote cytokine responses to stress. Cytokine 113:256–64
    [Google Scholar]
  35. Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney RD et al. 2013. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol. Psychiatry 18:666–73
    [Google Scholar]
  36. Crumeyrolle-Arias M, Jaglin M, Bruneau A, Vancassel S, Cardona A et al. 2014. Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats. Psychoneuroendocrino-logy 42:207–17
    [Google Scholar]
  37. Cryan JF. 2019. More than a gut feeling. Psychologist 32:30–35
    [Google Scholar]
  38. Cryan JF, Dinan TG. 2015a. Gut microbiota: microbiota and neuroimmune signaling—Metchnikoff to microglia. Nat. Rev. Gastroenterol. Hepatol. 12:494–96
    [Google Scholar]
  39. Cryan JF, Dinan TG. 2015b. More than a gut feeling: The microbiota regulates neurodevelopment and behavior. Neuropsychopharmacology 40:241–42
    [Google Scholar]
  40. Cryan JF, O'Riordan KJ, Cowan CS, Sandhu KV, Bastiaanssen TF et al. 2019. The microbiota-gut-brain axis. Physiol. Rev. 99:1877–2013
    [Google Scholar]
  41. Cussotto S, Clarke G, Dinan TG, Cryan JF 2019. Psychotropics and the microbiome: a chamber of secrets. Psychopharmacology 236:1411–32
    [Google Scholar]
  42. Dantzer R. 2018. Neuroimmune interactions: from the brain to the immune system and vice versa. Physiol. Rev. 98:477–504
    [Google Scholar]
  43. de Kloet ER, Joels M, Holsboer F 2005. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6:463–75
    [Google Scholar]
  44. De Palma G, Blennerhassett P, Lu J, Deng Y, Park AJ et al. 2015. Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nat. Commun. 6:7735
    [Google Scholar]
  45. De Palma G, Collins SM, Bercik P, Verdu EF 2014. The microbiota-gut-brain axis in gastrointestinal disorders: stressed bugs, stressed brain or both?. J. Physiol. 592:2989–97
    [Google Scholar]
  46. Del Grande da Silva G, Wiener CD, Barbosa LP, Goncalves Araujo JM, Molina ML et al. 2016. Pro-inflammatory cytokines and psychotherapy in depression: results from a randomized clinical trial. J. Psychiatr. Res. 75:57–64
    [Google Scholar]
  47. Derecki NC, Cardani AN, Yang CH, Quinnies KM, Crihfield A et al. 2010. Regulation of learning and memory by meningeal immunity: a key role for IL-4. J. Exp. Med. 207:1067
    [Google Scholar]
  48. Desbonnet L, Clarke G, Traplin A, O'Sullivan O, Crispie F et al. 2015. Gut microbiota depletion from early adolescence in mice: implications for brain and behaviour. Brain Behav. Immun. 48:165–73
    [Google Scholar]
  49. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG 2010. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 170:1179–88
    [Google Scholar]
  50. Dhabhar FS. 2014. Effects of stress on immune function: the good, the bad, and the beautiful. Immunol. Res. 58:193–210
    [Google Scholar]
  51. Dinan TG, Cryan JF. 2019. Gut microbes and depression: still waiting for Godot. Brain Behav. Immun. 79:1–2
    [Google Scholar]
  52. Dinu M, Abbate R, Gensini GF, Casini A, Sofi F 2017. Vegetarian, vegan diets and multiple health outcomes: a systematic review with meta-analysis of observational studies. Crit. Rev. Food Sci. Nutr. 57:3640–49
    [Google Scholar]
  53. Dong H, Zhang X, Qian Y 2014. Mast cells and neuroinflammation. Med. Sci. Monit. Basic Res. 20:200–6
    [Google Scholar]
  54. Dorrestein PC, Mazmanian SK, Knight R 2014. Finding the missing links among metabolites, microbes, and the host. Immunity 40:824–32
    [Google Scholar]
  55. Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L et al. 2010. A meta-analysis of cytokines in major depression. Biol. Psychiatry 67:446–57
    [Google Scholar]
  56. Duman RS, Aghajanian GK, Sanacora G, Krystal JH 2016. Synaptic plasticity and depression: new insights from stress and rapid-acting antidepressants. Nat. Med. 22:238–49
    [Google Scholar]
  57. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O 2003. Inflammation is detrimental for neurogenesis in adult brain. PNAS 100:13632–37
    [Google Scholar]
  58. El Aidy S, Dinan TG, Cryan JF 2015. Gut microbiota: the conductor in the orchestra of immune-neuroendocrine communication. Clin. Ther. 37:954–67
    [Google Scholar]
  59. Engelhardt B, Vajkoczy P, Weller RO 2017. The movers and shapers in immune privilege of the CNS. Nat. Immunol. 18:123–31
    [Google Scholar]
  60. Eskandari F, Webster JI, Sternberg EM 2003. Neural immune pathways and their connection to inflammatory diseases. Arthritis Res. Ther. 5:251–65
    [Google Scholar]
  61. Erny D, Hrabe de Angelis AL, Jaitin D, Wieghofer P, Staszewski O et al. 2015. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci. 18:965–77
    [Google Scholar]
  62. Esposito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC et al. 2005. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J. Neurosci. 25:10074–86
    [Google Scholar]
  63. Farrar WL, Kilian PL, Ruff MR, Hill JM, Pert CB 1987. Visualization and characterization of interleukin 1 receptors in brain. J. Immunol. 139:459–63
    [Google Scholar]
  64. Feart C, Samieri C, Barberger-Gateau P 2010. Mediterranean diet and cognitive function in older adults. Curr. Opin. Clin. Nutr. Metab. Care 13:14–18
    [Google Scholar]
  65. Firth J, Marx W, Dash S, Carney R, Teasdale SB et al. 2019. The effects of dietary improvement on symptoms of depression and anxiety: a meta-analysis of randomized controlled trials. Psychosom. Med. 81:265–80
    [Google Scholar]
  66. Fleshner M, Frank M, Maier SF 2017. Danger signals and inflammasomes: stress-evoked sterile inflammation in mood disorders. Neuropsychopharmacology 42:36–45
    [Google Scholar]
  67. Frank MG, Fonken LK, Dolzani SD, Annis JL, Siebler PH et al. 2018. Immunization with Mycobacterium vaccae induces an anti-inflammatory milieu in the CNS: attenuation of stress-induced microglial priming, alarmins and anxiety-like behavior. Brain Behav. Immun. 73:352–63
    [Google Scholar]
  68. Fülling C, Dinan TG, Cryan JF 2019. Gut microbe to brain signalling: what happens in vagus. Neuron 101:998–1002
    [Google Scholar]
  69. Georgin-Lavialle S, Moura DS, Salvador A, Chauvet-Gelinier JC, Launay JM et al. 2016. Mast cells’ involvement in inflammation pathways linked to depression: evidence in mastocytosis. Mol. Psychiatry 21:1511–16
    [Google Scholar]
  70. Gilbert JA, Blaser MJ, Caporaso JG, Jansson JK, Lynch SV, Knight R 2018. Current understanding of the human microbiome. Nat. Med. 24:392–400
    [Google Scholar]
  71. Goshen I, Kreisel T, Ben-Menachem-Zidon O, Licht T, Weidenfeld J et al. 2008. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neuro-genesis suppression. Mol. Psychiatry 13:717–28
    [Google Scholar]
  72. Green HF, Treacy E, Keohane AK, Sullivan AM, O'Keeffe GW, Nolan YM 2012. A role for interleukin-1β in determining the lineage fate of embryonic rat hippocampal neural precursor cells. Mol. Cell. Neurosci. 49:311–21
    [Google Scholar]
  73. Grosse L, Hoogenboezem T, Ambree O, Bellingrath S, Jorgens S et al. 2016. Deficiencies of the T and natural killer cell system in major depressive disorder: T regulatory cell defects are associated with inflammatory monocyte activation. Brain Behav. Immun. 54:38–44
    [Google Scholar]
  74. Hao K, Qi Q, Hao H, Wang G, Chen Y et al. 2013. The pharmacokinetic-pharmacodynamic model of azithromycin for lipopolysaccharide-induced depressive-like behavior in mice. PLOS ONE 8:e54981
    [Google Scholar]
  75. Hashioka S, Klegeris A, Monji A, Kato T, Sawada M et al. 2007. Antidepressants inhibit interferon-gamma-induced microglial production of IL-6 and nitric oxide. Exp. Neurol. 206:33–42
    [Google Scholar]
  76. Hoban AE, Moloney RD, Golubeva AV, McVey Neufeld KA, O'Sullivan O et al. 2016. Behavioural and neurochemical consequences of chronic gut microbiota depletion during adulthood in the rat. Neuroscience 339:463–77
    [Google Scholar]
  77. Hodes GE, Kana V, Menard C, Merad M, Russo SJ 2015. Neuroimmune mechanisms of depression. Nat. Neurosci. 18:1386–93
    [Google Scholar]
  78. Hodes GE, Pfau ML, Leboeuf M, Golden SA, Christoffel DJ et al. 2014. Individual differences in the peripheral immune system promote resilience versus susceptibility to social stress. PNAS 111:16136–41
    [Google Scholar]
  79. Hooper LV, Macpherson AJ. 2010. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 10:159–69
    [Google Scholar]
  80. Huang Y, Shi X, Li Z, Shen Y, Shi X et al. 2018. Possible association of Firmicutes in the gut microbiota of patients with major depressive disorder. Neuropsychiatr. Dis. Treat. 14:3329–37
    [Google Scholar]
  81. Hueston CM, O'Leary JD, Hoban AE, Kozareva DA, Pawley LC et al. 2018. Chronic interleukin-1β in the dorsal hippocampus impairs behavioural pattern separation. Brain Behav. Immun. 74:252–64
    [Google Scholar]
  82. Jacka FN, Cherbuin N, Anstey KJ, Sachdev P, Butterworth P 2015. Western diet is associated with a smaller hippocampus: a longitudinal investigation. BMC Med 13:215
    [Google Scholar]
  83. Jacka FN, O'Neil A, Opie R, Itsiopoulos C, Cotton S et al. 2017. A randomised controlled trial of dietary improvement for adults with major depression (the “SMILES” trial). BMC Med 15:23
    [Google Scholar]
  84. Jacka FN, Pasco JA, Mykletun A, Williams LJ, Hodge AM et al. 2010. Association of Western and traditional diets with depression and anxiety in women. Am. J. Psychiatry 167:305–11
    [Google Scholar]
  85. Jang H-M, Lee K-E, Lee H-J, Kim D-H 2018. Immobilization stress-induced Escherichia coli causes anxiety by inducing NF-κB activation through gut microbiota disturbance. Sci. Rep. 8:13897
    [Google Scholar]
  86. Jeon S-A, Lee E, Hwang I, Han B, Park S et al. 2017. NLRP3 inflammasome contributes to lipopolysaccharide-induced depressive-like behaviors via indoleamine 2,3-dioxygenase induction. Int. J. Neuropsychopharmacol. 20:896–906
    [Google Scholar]
  87. Jiang H, Ling Z, Zhang Y, Mao H, Ma Z et al. 2015. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav. Immun. 48:186–94
    [Google Scholar]
  88. Kanoski SE, Davidson TL. 2011. Western diet consumption and cognitive impairment: links to hippocampal dysfunction and obesity. Physiol. Behav. 103:59–68
    [Google Scholar]
  89. Kappelmann N, Lewis G, Dantzer R, Jones PB, Khandaker GM 2018. Antidepressant activity of anti-cytokine treatment: a systematic review and meta-analysis of clinical trials of chronic inflammatory conditions. Mol. Psychiatry 23:335–43
    [Google Scholar]
  90. Kaufmann FN, Costa AP, Ghisleni G, Diaz AP, Rodrigues ALS et al. 2017. NLRP3 inflammasome-driven pathways in depression: clinical and preclinical findings. Brain Behav. Immun. 64:367–83
    [Google Scholar]
  91. Kazemi A, Noorbala AA, Azam K, Eskandari MH, Djafarian K 2019. Effect of probiotic and prebiotic versus placebo on psychological outcomes in patients with major depressive disorder: a randomized clinical trial. Clin. Nutr. 38:522–28
    [Google Scholar]
  92. Kelly JR, Borre Y, O'Brien C, Patterson E, El Aidy S et al. 2016. Transferring the blues: Depression-associated gut microbiota induces neurobehavioural changes in the rat. J. Psychiatr. Res. 82:109–18
    [Google Scholar]
  93. Keohane A, Ryan S, Maloney E, Sullivan AM, Nolan YM 2010. Tumour necrosis factor-alpha impairs neuronal differentiation but not proliferation of hippocampal neural precursor cells: role of Hes1. Mol. Cell. Neurosci. 43:127–35
    [Google Scholar]
  94. Koo JW, Duman RS. 2008. IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress. PNAS 105:751–56
    [Google Scholar]
  95. Kreisel T, Frank MG, Licht T, Reshef R, Ben-Menachem-Zidon O et al. 2014. Dynamic microglial alterations underlie stress-induced depressive-like behavior and suppressed neurogenesis. Mol. Psychiatry 19:699–709
    [Google Scholar]
  96. Kunis G, Baruch K, Rosenzweig N, Kertser A, Miller O et al. 2013. IFN-γ-dependent activation of the brain's choroid plexus for CNS immune surveillance and repair. Brain 136:3427–40
    [Google Scholar]
  97. Langgartner D, Vaihinger CA, Haffner-Luntzer M, Kunze JF, Weiss AJ et al. 2018. The role of the intestinal microbiome in chronic psychosocial stress-induced pathologies in male mice. Front. Behav. Neurosci. 12:252
    [Google Scholar]
  98. Larrieu T, Sandi C. 2018. Stress-induced depression: Is social rank a predictive risk factor?. BioEssays 40:e1800012
    [Google Scholar]
  99. Lassale C, Batty GD, Baghdadli A, Jacka F, Sanchez-Villegas A et al. 2019. Healthy dietary indices and risk of depressive outcomes: a systematic review and meta-analysis of observational studies. Mol. Psychiatry 24:965–86
    [Google Scholar]
  100. Lee H, Thuret S. 2018. Adult human hippocampal neurogenesis: controversy and evidence. Trends Mol. Med. 24:521–22
    [Google Scholar]
  101. Lenz KM, Pickett LA, Wright CL, Davis KT, Joshi A, McCarthy MM 2018. Mast cells in the developing brain determine adult sexual behavior. J. Neurosci. 38:8044
    [Google Scholar]
  102. Levone BR, Cryan JF, O'Leary OF 2015. Role of adult hippocampal neurogenesis in stress resilience. Neurobiol. Stress 1:147–55
    [Google Scholar]
  103. Levy M, Thaiss Christoph A, Zeevi D, Dohnalová L, Zilberman-Schapira G et al. 2015. Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling. Cell 163:1428–43
    [Google Scholar]
  104. Lewitus GM, Cohen H, Schwartz M 2008. Reducing post-traumatic anxiety by immunization. Brain Behav. Immun. 22:1108–14
    [Google Scholar]
  105. Lewitus GM, Wilf-Yarkoni A, Ziv Y, Shabat-Simon M, Gersner R et al. 2009. Vaccination as a novel approach for treating depressive behavior. Biol. Psychiatry 65:283–88
    [Google Scholar]
  106. Li N, Wang Q, Wang Y, Sun A, Lin Y et al. 2018. Oral probiotics ameliorate the behavioral deficits induced by chronic mild stress in mice via the gut microbiota-inflammation axis. Front. Behav. Neurosci. 12:266
    [Google Scholar]
  107. Li Q, Barres BA. 2018. Microglia and macrophages in brain homeostasis and disease. Nat. Rev. Immunol. 18:225–42
    [Google Scholar]
  108. Li Z-Q, Yan Z-Y, Lan F-J, Dong Y-Q, Xiong Y 2018. Suppression of NLRP3 inflammasome attenuates stress-induced depression-like behavior in NLGN3-deficient mice. Biochem. Biophys. Res. Commun. 501:933–40
    [Google Scholar]
  109. Liang S, Wang T, Hu X, Luo J, Li W et al. 2015. Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress. Neuroscience 310:561–77
    [Google Scholar]
  110. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ et al. 2015. Structural and functional features of central nervous system lymphatic vessels. Nature 523:337–41
    [Google Scholar]
  111. Lucassen PJ, Toni N, Kempermann G, Frisen J, Gage FH, Swaab DF 2019. Limits to human neurogenesis—really?. Mol. Psychiatry. In press. https://doi.org/10.1038/s41380-018-0337-5
    [Crossref] [Google Scholar]
  112. Lurie I, Yang YX, Haynes K, Mamtani R, Boursi B 2015. Antibiotic exposure and the risk for depression, anxiety, or psychosis: a nested case-control study. J. Clin. Psychiatry 76:1522–28
    [Google Scholar]
  113. Madsen TM, Treschow A, Bengzon J, Bolwig TG, Lindvall O, Tingstrom A 2000. Increased neurogenesis in a model of electroconvulsive therapy. Biol. Psychiatry 47:1043–49
    [Google Scholar]
  114. Maes M, Lambrechts J, Bosmans E, Jacobs J, Suy E et al. 1992. Evidence for a systemic immune activation during depression: results of leukocyte enumeration by flow cytometry in conjunction with monoclonal antibody staining. Psychol. Med. 22:45–53
    [Google Scholar]
  115. Maes M, Meltzer HY, Bosmans E, Bergmans R, Vandoolaeghe E et al. 1995. Increased plasma concentrations of interleukin-6, soluble interleukin-6, soluble interleukin-2 and transferrin receptor in major depression. J. Affect. Disord. 34:301–9
    [Google Scholar]
  116. Majidi J, Kosari-Nasab M, Salari AA 2016. Developmental minocycline treatment reverses the effects of neonatal immune activation on anxiety- and depression-like behaviors, hippocampal inflammation, and HPA axis activity in adult mice. Brain Res. Bull. 120:1–13
    [Google Scholar]
  117. Malberg JE, Eisch AJ, Nestler EJ, Duman RS 2000. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20:9104–10
    [Google Scholar]
  118. Månsson KNT, Salami A, Frick A, Carlbring P, Andersson G et al. 2016. Neuroplasticity in response to cognitive behavior therapy for social anxiety disorder. Transl. Psychiatry 6:e727
    [Google Scholar]
  119. Marečková K, Mareček R, Bencurova P, Klánová J, Dušek L, Brázdil M 2018. Perinatal stress and human hippocampal volume: findings from typically developing young adults. Sci. Rep. 8:4696
    [Google Scholar]
  120. Mason L, Peters E, Williams SC, Kumari V 2017. Brain connectivity changes occurring following cognitive behavioural therapy for psychosis predict long-term recovery. Transl. Psychiatry 7:e1001
    [Google Scholar]
  121. McEwen BS. 1998. Stress, adaptation, and disease: allostasis and allostatic load. Ann. N. Y. Acad. Sci. 840:33–44
    [Google Scholar]
  122. McEwen BS, Bowles NP, Gray JD, Hill MN, Hunter RG et al. 2015. Mechanisms of stress in the brain. Nat. Neurosci. 18:1353
    [Google Scholar]
  123. McVey Neufeld KA, O'Mahony SM, Hoban AE, Waworuntu RV, Berg BM et al. 2019. Neurobehavioural effects of Lactobacillus rhamnosus GG alone and in combination with prebiotics polydextrose and galactooligosaccharide in male rats exposed to early-life stress. Nutr. Neurosci. 22:425–34
    [Google Scholar]
  124. Medina-Rodriguez EM, Lowell JA, Worthen RJ, Syed SA, Beurel E 2018. Involvement of innate and adaptive immune systems alterations in the pathophysiology and treatment of depression. Front. Neurosci. 12:547
    [Google Scholar]
  125. Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D et al. 2011. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br. J. Nutr. 105:755–64
    [Google Scholar]
  126. Miller AH, Raison CL. 2015. The role of inflammation in depression: from evolutionary imperative to modern treatment target. Nat. Rev. Immunol. 16:22–34
    [Google Scholar]
  127. Miyaoka T, Kanayama M, Wake R, Hashioka S, Hayashida M et al. 2018. Clostridium butyricum MIYAIRI 588 as adjunctive therapy for treatment-resistant major depressive disorder: a prospective open-label trial. Clin. Neuropharmacol. 41:151–55
    [Google Scholar]
  128. Möhle L, Mattei D, Heimesaat Markus M, Bereswill S, Fischer A et al. 2016. Ly6Chi monocytes provide a link between antibiotic-induced changes in gut microbiota and adult hippocampal neurogenesis. Cell Rep 15:1945–56
    [Google Scholar]
  129. Molteni R, Macchi F, Zecchillo C, Dell'agli M, Colombo E et al. 2013. Modulation of the inflammatory response in rats chronically treated with the antidepressant agomelatine. Eur. Neuropsychopharmacol. 23:1645–55
    [Google Scholar]
  130. Monje ML, Toda H, Palmer TD 2003. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760
    [Google Scholar]
  131. Morais M, Santos PA, Mateus-Pinheiro A, Patricio P, Pinto L et al. 2014. The effects of chronic stress on hippocampal adult neurogenesis and dendritic plasticity are reversed by selective MAO-A inhibition. J. Psychopharmacol. 28:1178–83
    [Google Scholar]
  132. Moreno-Jiménez EP, Flor-García M, Terreros-Roncal J, Rábano A, Cafini F et al. 2019. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer's disease. Nat. Med. 25:554–60
    [Google Scholar]
  133. Moya-Perez A, Perez-Villalba A, Benitez-Paez A, Campillo I, Sanz Y 2017. Bifidobacterium CECT 7765 modulates early stress-induced immune, neuroendocrine and behavioral alterations in mice. Brain Behav. Immun. 65:43–56
    [Google Scholar]
  134. Naseribafrouei A, Hestad K, Avershina E, Sekelja M, Linlokken A et al. 2014. Correlation between the human fecal microbiota and depression. Neurogastroenterol. Motil. 26:1155–62
    [Google Scholar]
  135. Nautiyal KM, Ribeiro AC, Pfaff DW, Silver R 2008. Brain mast cells link the immune system to anxiety-like behavior. PNAS 105:18053
    [Google Scholar]
  136. Ngwenya LB, Peters A, Rosene DL 2006. Maturational sequence of newly generated neurons in the dentate gyrus of the young adult rhesus monkey. J. Comp. Neurol. 498:204–16
    [Google Scholar]
  137. Nishida K, Sawada D, Kuwano Y, Tanaka H, Sugawara T et al. 2017. Daily administration of paraprobiotic Lactobacillus gasseri CP2305 ameliorates chronic stress-associated symptoms in Japanese medical students. J. Funct. Foods 36:112–21
    [Google Scholar]
  138. Nishino R, Mikami K, Takahashi H, Tomonaga S, Furuse M et al. 2013. Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods. Neurogastroenterol. Motil. 25:521–28
    [Google Scholar]
  139. Norris GT, Kipnis J. 2019. Immune cells and CNS physiology: microglia and beyond. J. Exp. Med. 216:60
    [Google Scholar]
  140. Ogbonnaya ES, Clarke G, Shanahan F, Dinan TG, Cryan JF, O'Leary OF 2015. Adult hippocampal neurogenesis is regulated by the microbiome. Biol. Psychiatry 78:e7–9
    [Google Scholar]
  141. O'Leary OF, Cryan JF. 2014. A ventral view on antidepressant action: roles for adult hippocampal neurogenesis along the dorsoventral axis. Trends Pharmacol. Sci. 35:675–87
    [Google Scholar]
  142. O'Leary OF, Dinan TG, Cryan JF 2015. Faster, better, stronger: towards new antidepressant therapeutic strategies. Eur. J. Pharmacol. 753:32–50
    [Google Scholar]
  143. O'Leary OF, Ogbonnaya ES, Felice D, Levone BR, Conroy LC et al. 2018. The vagus nerve modulates BDNF expression and neurogenesis in the hippocampus. Eur. Neuropsychopharmacol. 28:307–16
    [Google Scholar]
  144. O'Leime CS, Cryan JF, Nolan YM 2017. Nuclear deterrents: intrinsic regulators of IL-1β-induced effects on hippocampal neurogenesis. Brain Behav. Immun. 66:394–412
    [Google Scholar]
  145. O'Leime CS, Kozareva DA, Hoban AE, Long-Smith CM, Cryan JF, Nolan YM 2018. TLX is an intrinsic regulator of the negative effects of IL-1β on proliferating hippocampal neural progenitor cells. FASEB J 32:613–24
    [Google Scholar]
  146. O'Mahony SM, Felice VD, Nally K, Savignac HM, Claesson MJ et al. 2014. Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats. Neuroscience 277:885–901
    [Google Scholar]
  147. O'Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM et al. 2009. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol. Psychiatry 65:263–67
    [Google Scholar]
  148. Palomar MM, Maldonado Galdeano C, Perdigon G 2014. Influence of a probiotic lactobacillus strain on the intestinal ecosystem in a stress model mouse. Brain Behav. Immun. 35:77–85
    [Google Scholar]
  149. Pan Y, Chen X-Y, Zhang Q-Y, Kong L-D 2014. Microglial NLRP3 inflammasome activation mediates IL-1β-related inflammation in prefrontal cortex of depressive rats. Brain Behav. Immun. 41:90–100
    [Google Scholar]
  150. Papalini S, Michels F, Kohn N, Wegman J, van Hemert S et al. 2019. Stress matters: randomized controlled trial on the effect of probiotics on neurocognition. Neurobiol. Stress 10:100141
    [Google Scholar]
  151. Pape K, Tamouza R, Leboyer M, Zipp F 2019. Immunoneuropsychiatry—novel perspectives on brain disorders. Nat. Rev. Neurol. 15:317–28
    [Google Scholar]
  152. Patas K, Willing A, Demiralay C, Engler JB, Lupu A et al. 2018. T cell phenotype and T cell receptor repertoire in patients with major depressive disorder. Front. Immunol. 9:291
    [Google Scholar]
  153. Pavillard LE, Marin-Aguilar F, Bullon P, Cordero MD 2018. Cardiovascular diseases, NLRP3 inflammasome, and western dietary patterns. Pharmacol. Res. 131:44–50
    [Google Scholar]
  154. Pavlov VA, Tracey KJ. 2017. Neural regulation of immunity: molecular mechanisms and clinical translation. Nat. Neurosci. 20:156–66
    [Google Scholar]
  155. Perera TD, Dwork AJ, Keegan KA, Thirumangalakudi L, Lipira CM et al. 2011. Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates. PLOS ONE 6:e17600
    [Google Scholar]
  156. Pinto-Sanchez MI, Hall GB, Ghajar K, Nardelli A, Bolino C et al. 2017. Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome. Gastroenterology 153:448–59.e8
    [Google Scholar]
  157. Rajkowska G, Miguel-Hidalgo JJ. 2007. Gliogenesis and glial pathology in depression. CNS Neurol. Disord. Drug Targets 6:219–33
    [Google Scholar]
  158. Revesz D, Tjernstrom M, Ben-Menachem E, Thorlin T 2008. Effects of vagus nerve stimulation on rat hippocampal progenitor proliferation. Exp. Neurol. 214:259–65
    [Google Scholar]
  159. Rhee SH, Pothoulakis C, Mayer EA 2009. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat. Rev. Gastroenterol. Hepatol. 6:306–14
    [Google Scholar]
  160. Richards EM, Zanotti-Fregonara P, Fujita M, Newman L, Farmer C et al. 2018. PET radioligand binding to translocator protein (TSPO) is increased in unmedicated depressed subjects. EJNMMI Res 8:57
    [Google Scholar]
  161. Roque S, Oliveira TG, Nobrega C, Barreira-Silva P, Nunes-Alves C et al. 2011. Interplay between depressive-like behavior and the immune system in an animal model of prenatal dexamethasone administration. Front. Behav. Neurosci. 5:4
    [Google Scholar]
  162. Rosas-Ballina M, Tracey KJ. 2009. The neurology of the immune system: Neural reflexes regulate immunity. Neuron 64:28–32
    [Google Scholar]
  163. Rua R, McGavern DB. 2018. Advances in meningeal immunity. Trends Mol. Med. 24:542–59
    [Google Scholar]
  164. Rudzki L, Ostrowska L, Pawlak D, Malus A, Pawlak K et al. 2019. Probiotic Lactobacillus Plantarum 299v decreases kynurenine concentration and improves cognitive functions in patients with major depression: a double-blind, randomized, placebo controlled study. Psychoneuroendocrinology 100:213–22
    [Google Scholar]
  165. Ryan SM, O'Keeffe GW, O'Connor C, Keeshan K, Nolan YM 2013. Negative regulation of TLX by IL-1β correlates with an inhibition of adult hippocampal neural precursor cell proliferation. Brain Behav. Immun. 33:7–13
    [Google Scholar]
  166. Sampson TR, Debelius JW, Thron T, Janssen S, Shastri GG et al. 2016. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease. Cell 167:1469–80.e12
    [Google Scholar]
  167. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F et al. 2003. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805–9
    [Google Scholar]
  168. Sapolsky RM. 2004. Is impaired neurogenesis relevant to the affective symptoms of depression?. Biol. Psychiatry 56:137–39
    [Google Scholar]
  169. Sapolsky RM. 2015. Stress and the brain: individual variability and the inverted-U. Nat. Neurosci. 18:1344
    [Google Scholar]
  170. Sarkar A, Harty S, Lehto SM, Moeller AH, Dinan TG et al. 2018. The microbiome in psychology and cognitive neuroscience. Trends Cogn. Sci. 22:611–36
    [Google Scholar]
  171. Sarkar A, Lehto SM, Harty S, Dinan TG, Cryan JF, Burnet PWJ 2016. Psychobiotics and the manipulation of bacteria-gut-brain signals. Trends Neurosci 39:763–81
    [Google Scholar]
  172. Savignac HM, Couch Y, Stratford M, Bannerman DM, Tzortzis G et al. 2016. Prebiotic administration normalizes lipopolysaccharide (LPS)-induced anxiety and cortical 5-HT2A receptor and IL1-β levels in male mice. Brain Behav. Immun. 52:120–31
    [Google Scholar]
  173. Savignac HM, Kiely B, Dinan TG, Cryan JF 2014. Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice. Neurogastroenterol. Motil. 26:1615–27
    [Google Scholar]
  174. Scheinert RB, Haeri MH, Lehmann ML, Herkenham M 2016. Therapeutic effects of stress-programmed lymphocytes transferred to chronically stressed mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 70:1–7
    [Google Scholar]
  175. Schmidt K, Cowen PJ, Harmer CJ, Tzortzis G, Errington S, Burnet PW 2015. Prebiotic intake reduces the waking cortisol response and alters emotional bias in healthy volunteers. Psychopharmacology 232:1793–801
    [Google Scholar]
  176. Sierra A, Gottfried-Blackmore A, Milner TA, McEwen BS, Bulloch K 2008. Steroid hormone receptor expression and function in microglia. Glia 56:659–74
    [Google Scholar]
  177. Simen BB, Duman CH, Simen AA, Duman RS 2006. TNFα signaling in depression and anxiety: behavioral consequences of individual receptor targeting. Biol. Psychiatry 59:775–85
    [Google Scholar]
  178. Singh V, Sadler R, Heindl S, Llovera G, Roth S et al. 2018. The gut microbiome primes a cerebroprotective immune response after stroke. J. Cereb. Blood Flow Metab. 38:1293–98
    [Google Scholar]
  179. Sitges M, Gómez CD, Aldana BI 2014. Sertraline reduces IL-1β and TNF-α mRNA expression and overcomes their rise induced by seizures in the rat hippocampus. PLOS ONE 9:e111665
    [Google Scholar]
  180. Slykerman RF, Hood F, Wickens K, Thompson JMD, Barthow C et al. 2017. Effect of Lactobacillus rhamnosus HN001 in pregnancy on postpartum symptoms of depression and anxiety: a randomised double-blind placebo-controlled trial. EBioMedicine 24:159–65
    [Google Scholar]
  181. Smith CJ, Emge JR, Berzins K, Lung L, Khamishon R et al. 2014. Probiotics normalize the gut-brain-microbiota axis in immunodeficient mice. Am. J. Physiol. Gastrointest. Liver Physiol. 307:G793–802
    [Google Scholar]
  182. Snyder JS. 2018. Questioning human neurogenesis. Nature 555:315–16
    [Google Scholar]
  183. Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA 2011. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476:458–61
    [Google Scholar]
  184. Sofi F, Macchi C, Abbate R, Gensini GF, Casini A 2013. Mediterranean diet and health. BioFactors 39:335–42
    [Google Scholar]
  185. Sorrells SF, Paredes MF, Cebrian-Silla A, Sandoval K, Qi D et al. 2018. Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature 555:377–81
    [Google Scholar]
  186. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M et al. 2013. Dynamics of hippocampal neurogenesis in adult humans. Cell 153:1219–27
    [Google Scholar]
  187. Spranger J, Verma S, Gohring I, Bobbert T, Seifert J et al. 2006. Adiponectin does not cross the blood-brain barrier but modifies cytokine expression of brain endothelial cells. Diabetes 55:141–47
    [Google Scholar]
  188. Steenbergen L, Sellaro R, van Hemert S, Bosch JA, Colzato LS 2015. A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain Behav. Immun. 48:258–64
    [Google Scholar]
  189. Strowig T, Henao-Mejia J, Elinav E, Flavell R 2012. Inflammasomes in health and disease. Nature 481:278–86
    [Google Scholar]
  190. Su WJ, Zhang Y, Chen Y, Gong H, Lian YJ et al. 2017. NLRP3 gene knockout blocks NF-κB and MAPK signaling pathway in CUMS-induced depression mouse model. Behav. Brain Res. 322:1–8
    [Google Scholar]
  191. Sudo N. 2012. Role of microbiome in regulating the HPA axis and its relevance to allergy. Chem. Immunol. Allergy 98:163–75
    [Google Scholar]
  192. Surget A, Tanti A, Leonardo ED, Laugeray A, Rainer Q et al. 2011. Antidepressants recruit new neurons to improve stress response regulation. Mol. Psychiatry 16:1177–88
    [Google Scholar]
  193. Tang AT, Choi JP, Kotzin JJ, Yang Y, Hong CC et al. 2017. Endothelial TLR4 and the microbiome drive cerebral cavernous malformations. Nature 545:305–10
    [Google Scholar]
  194. Thion MS, Low D, Silvin A, Chen J, Grisel P et al. 2018. Microbiome influences prenatal and adult microglia in a sex-specific manner. Cell 172:500–16.e16
    [Google Scholar]
  195. Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J et al. 2013. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144:1394–401.e4
    [Google Scholar]
  196. Treadway MT, Waskom ML, Dillon DG, Holmes AJ, Park MTM et al. 2015. Illness progression, recent stress, and morphometry of hippocampal subfields and medial prefrontal cortex in major depression. Biol. Psychiatry 77:285–94
    [Google Scholar]
  197. Turrin NP, Rivest S. 2004. Unraveling the molecular details involved in the intimate link between the immune and neuroendocrine systems. Exp. Biol. Med. 229:996–1006
    [Google Scholar]
  198. Udina M, Castellvi P, Moreno-Espana J, Navines R, Valdes M et al. 2012. Interferon-induced depression in chronic hepatitis C: a systematic review and meta-analysis. J. Clin. Psychiatry 73:1128–38
    [Google Scholar]
  199. Valles-Colomer M, Falony G, Darzi Y, Tigchelaar EF, Wang J et al. 2019. The neuroactive potential of the human gut microbiota in quality of life and depression. Nat. Microbiol. 4:623–32
    [Google Scholar]
  200. van Praag H, Christie BR, Sejnowski TJ, Gage FH 1999. Running enhances neurogenesis, learning, and long-term potentiation in mice. PNAS 96:13427–31
    [Google Scholar]
  201. Vogt MA, Mallien AS, Pfeiffer N, Inta I, Gass P, Inta D 2016. Minocycline does not evoke anxiolytic and antidepressant-like effects in C57BL/6 mice. Behav. Brain Res. 301:96–101
    [Google Scholar]
  202. Wang HT, Huang FL, Hu ZL, Zhang WJ, Qiao XQ et al. 2017. Early-life social isolation-induced depressive-like behavior in rats results in microglial activation and neuronal histone methylation that are mitigated by minocycline. Neurotox. Res. 31:505–20
    [Google Scholar]
  203. Wang Q, Jie W, Liu JH, Yang JM, Gao TM 2017. An astroglial basis of major depressive disorder? An overview. Glia 65:1227–50
    [Google Scholar]
  204. Whalen KA, McCullough ML, Flanders WD, Hartman TJ, Judd S, Bostick RM 2016. Paleolithic and Mediterranean diet pattern scores are inversely associated with biomarkers of inflammation and oxidative balance in adults. J. Nutr. 146:1217–26
    [Google Scholar]
  205. Willett WC, Sacks F, Trichopoulou A, Drescher G, Ferro-Luzzi A et al. 1995. Mediterranean diet pyramid: a cultural model for healthy eating. Am. J. Clin. Nutr. 61:1402s–6s
    [Google Scholar]
  206. Williams TJ, Cervenka MC. 2017. The role for ketogenic diets in epilepsy and status epilepticus in adults. Clin. Neurophysiol. Pract. 2:154–60
    [Google Scholar]
  207. Wohleb ES. 2016. Neuron-microglia interactions in mental health disorders: “for better, and for worse.”. Front. Immunol. 7:544
    [Google Scholar]
  208. Wohleb ES, McKim DB, Shea DT, Powell ND, Tarr AJ et al. 2014. Re-establishment of anxiety in stress-sensitized mice is caused by monocyte trafficking from the spleen to the brain. Biol. Psychiatry 75:970–81
    [Google Scholar]
  209. Wohleb ES, McKim DB, Sheridan JF, Godbout JP 2015. Monocyte trafficking to the brain with stress and inflammation: a novel axis of immune-to-brain communication that influences mood and behavior. Front. Neurosci. 8:447
    [Google Scholar]
  210. Wolf SA, Steiner B, Akpinarli A, Kammertoens T, Nassenstein C et al. 2009. CD4-positive T lymphocytes provide a neuroimmunological link in the control of adult hippocampal neurogenesis. J. Immunol. 182:3979–84
    [Google Scholar]
  211. Wong ML, Inserra A, Lewis MD, Mastronardi CA, Leong L et al. 2016. Inflammasome signaling affects anxiety- and depressive-like behavior and gut microbiome composition. Mol. Psychiatry 21:797–805
    [Google Scholar]
  212. Yao Y, Chen S, Cao M, Fan X, Yang T et al. 2017. Antigen-specific CD8+ T cell feedback activates NLRP3 inflammasome in antigen-presenting cells through perforin. Nat. Commun. 8:15402
    [Google Scholar]
  213. Yue N, Huang H, Zhu X, Han Q, Wang Y et al. 2017. Activation of P2X7 receptor and NLRP3 inflammasome assembly in hippocampal glial cells mediates chronic stress-induced depressive-like behaviors. J. Neuroinflammation 14:102
    [Google Scholar]
  214. Zhang T, Tian X, Wang Q, Tong Y, Wang H et al. 2015. Surgical stress induced depressive and anxiety like behavior are improved by dapsone via modulating NADPH oxidase level. Neurosci. Lett. 585:103–8
    [Google Scholar]
  215. Zhang Y, Liu L, Liu YZ, Shen XL, Wu TY et al. 2015. NLRP3 inflammasome mediates chronic mild stress-induced depression in mice via neuroinflammation. Int. J. Neuropsychopharmacol. 18:pyv006
    [Google Scholar]
  216. Zheng P, Zeng B, Zhou C, Liu M, Fang Z et al. 2016. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host's metabolism. Mol. Psychiatry 21:786–96
    [Google Scholar]
  217. Zheng X, Ma S, Kang A, Wu M, Wang L et al. 2016. Chemical dampening of Ly6Chi monocytes in the periphery produces anti-depressant effects in mice. Sci. Rep. 6:19406
    [Google Scholar]
  218. Zhu W, Cao FS, Feng J, Chen HW, Wan JR et al. 2017. NLRP3 inflammasome activation contributes to long-term behavioral alterations in mice injected with lipopolysaccharide. Neuroscience 343:77–84
    [Google Scholar]
  219. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E et al. 2006. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 9:268–75
    [Google Scholar]
  220. Zopf Y, Reljic D, Dieterich W 2018. Dietary effects on microbiota-new trends with gluten-free or paleo diet. Med. Sci. 6:92
    [Google Scholar]
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