Control of brain development, function, and behavior by the microbiome

Cell Host and Microbe

Volumn 17, Issue 5, 2015, Pages 565-576

  Sampson, Timothy R ^a   Mazmanian, Sarkis K ^a  

^a California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; NEUROTRANSMITTER;

AUTISM; BACTEROIDES FRAGILIS; BACTEROIDES THETAIOTAOMICRON; BEHAVIOR CONTROL; BIFIDOBACTERIUM INFANTIS; BRAIN DEVELOPMENT; BRAIN FUNCTION; CENTRAL NERVOUS SYSTEM; CLOSTRIDIUM SPOROGENES; CLOSTRIDIUM TYROBUTYRICUM; COLON MOTILITY; COMMENSALISM; ENTEROCOCCUS; ESCHERICHIA COLI; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; IMMUNE DYSREGULATION; IMMUNE SYSTEM; INTESTINE FLORA; LACTOBACILLUS BREVIS; LACTOBACILLUS DELBRUECKII SUBSP. BULGARICUS; LACTOBACILLUS RHAMNOSUS; LACTOCOCCUS LACTIS SUBSP. LACTIS; MICROBIAL COMMUNITY; MICROBIOME; MOOD; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; RUMINOCOCCUS; SOCIAL BEHAVIOR; STEREOTYPY; STREPTOCOCCUS THERMOPHILUS; ANIMAL; BEHAVIOR; BRAIN; GASTROINTESTINAL TRACT; MICROBIOLOGY; PHYSIOLOGY;

ANIMALIA;

ANIMALS; BEHAVIOR; BRAIN; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS;

EID: 84929310699     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.04.011     Document Type: Review

References (105)

1. K. Aagaard, J. Ma, K.M. Antony, R. Ganu, J. Petrosino, and J. Versalovic The placenta harbors a unique microbiome Sci. Trans. Med. 6 2014 237ra265
2. S.A. Adamo, I. Kovalko, R.H. Easy, and D. Stoltz A viral aphrodisiac in the cricket Gryllus texensis J. Exp. Biol. 217 2014 1970 1976
3. P. Ashwood, S. Wills, and J. Van de Water The immune response in autism: a new frontier for autism research J. Leukoc. Biol. 80 2006 1 15
4. E. Barrett, R.P. Ross, P.W. O'Toole, G.F. Fitzgerald, and C. Stanton γ-Aminobutyric acid production by culturable bacteria from the human intestine J. Appl. Microbiol. 113 2012 411 417
5. Y. Belkaid, and T.W. Hand Role of the microbiota in immunity and inflammation Cell 157 2014 121 141
6. P. Bercik, E. Denou, J. Collins, W. Jackson, J. Lu, J. Jury, Y. Deng, P. Blennerhassett, J. Macri, and K.D. McCoy The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice Gastroenterology 141 2011 599 609
7. M. Berger, J.A. Gray, and B.L. Roth The expanded biology of serotonin Annu. Rev. Med. 60 2009 355 366
8. D.G. Biron, L. Marché, F. Ponton, H.D. Loxdale, N. Galéotti, L. Renault, C. Joly, and F. Thomas Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach Proc. Biol. Sci. 272 2005 2117 2126
9. R.M. Bluthé, N. Castanon, F. Pousset, A. Bristow, C. Ball, J. Lestage, B. Michaud, K.W. Kelley, and R. Dantzer Central injection of IL-10 antagonizes the behavioural effects of lipopolysaccharide in rats Psychoneuroendocrinology 24 1999 301 311
10. R.M. Bluthé, K.W. Kelley, and R. Dantzer Effects of insulin-like growth factor-I on cytokine-induced sickness behavior in mice Brain Behav. Immun. 20 2006 57 63
11. Y.E. Borre, G.W. O'Keeffe, G. Clarke, C. Stanton, T.G. Dinan, and J.F. Cryan Microbiota and neurodevelopmental windows: implications for brain disorders Trends Mol. Med. 20 2014 509 518
12. V. Braniste, M. Al-Asmakh, C. Kowal, F. Anuar, A. Abbaspour, M. Toth, A. Korecka, N. Bakocevic, N.L. Guan, and P. Kundu The gut microbiota influences blood-brain barrier permeability in mice Sci. Transl. Med. 6 2014 263ra158
13. J.A. Bravo, P. Forsythe, M.V. Chew, E. Escaravage, H.M. Savignac, T.G. Dinan, J. Bienenstock, and J.F. Cryan 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 2011 16050 16055
14. C.D. Breder, C. Hazuka, T. Ghayur, C. Klug, M. Huginin, K. Yasuda, M. Teng, and C.B. Saper Regional induction of tumor necrosis factor alpha expression in the mouse brain after systemic lipopolysaccharide administration Proc. Natl. Acad. Sci. USA 91 1994 11393 11397
15. W. Cai, V.I. Khaoustov, Q. Xie, T. Pan, W. Le, and B. Yoffe Interferon-alpha-induced modulation of glucocorticoid and serotonin receptors as a mechanism of depression J. Hepatol. 42 2005 880 887
16. P.D. Cani, E. Lecourt, E.M. Dewulf, F.M. Sohet, B.D. Pachikian, D. Naslain, F. De Backer, A.M. Neyrinck, and N.M. Delzenne Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal Am. J. Clin. Nutr. 90 2009 1236 1243
17. G. Clarke, S. Grenham, P. Scully, P. Fitzgerald, R.D. Moloney, F. Shanahan, T.G. Dinan, and J.F. Cryan The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner Mol. Psychiatry 18 2013 666 673
18. A.R. Conn, D.I. Fell, and R.D. Steele Characterization of alpha-keto acid transport across blood-brain barrier in rats Am. J. Physiol. 245 1983 E253 E260
19. R. Dantzer, J.P. Konsman, R.M. Bluthe, and K.W. Kelley Neural and humoral pathways of communication from the immune system to the brain: parallel or convergent? Auton. Neurosci. 85 2000 60 65
20. R. Dantzer, J.C. O'Connor, G.G. Freund, R.W. Johnson, and K.W. Kelley From inflammation to sickness and depression: when the immune system subjugates the brain Nat. Rev. Neurosci. 9 2008 46 56
21. C.G. de Theije, H. Wopereis, M. Ramadan, T. van Eijndthoven, J. Lambert, J. Knol, J. Garssen, A.D. Kraneveld, and R. Oozeer Altered gut microbiota and activity in a murine model of autism spectrum disorders Brain Behav. Immun. 37 2014 197 206
22. L. Desbonnet, L. Garrett, G. Clarke, B. Kiely, J.F. Cryan, and T.G. Dinan Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression Neuroscience 170 2010 1179 1188
23. L. Desbonnet, G. Clarke, F. Shanahan, T.G. Dinan, and J.F. Cryan Microbiota is essential for social development in the mouse Mol. Psychiatry 19 2014 146 148
24. H.S. Deshmukh, Y. Liu, O.R. Menkiti, J. Mei, N. Dai, C.E. O'Leary, P.M. Oliver, J.K. Kolls, J.N. Weiser, and G.S. Worthen The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice Nat. Med. 20 2014 524 530
25. R. Diaz Heijtz, S. Wang, F. Anuar, Y. Qian, B. Björkholm, A. Samuelsson, M.L. Hibberd, H. Forssberg, and S. Pettersson Normal gut microbiota modulates brain development and behavior Proc. Natl. Acad. Sci. USA 108 2011 3047 3052
26. C. Driver Rabies: risk, prognosis and prevention Nurs. Times 110 2014 16 18
27. P. Forsythe, J. Bienenstock, and W.A. Kunze Vagal pathways for microbiome-brain-gut axis communication Adv. Exp. Med. Biol. 817 2014 115 133
28. J.A. Foster, and K.A. McVey Neufeld Gut-brain axis: how the microbiome influences anxiety and depression Trends Neurosci. 36 2013 305 312
29. G. Frost, M.L. Sleeth, M. Sahuri-Arisoylu, B. Lizarbe, S. Cerdan, L. Brody, J. Anastasovska, S. Ghourab, M. Hankir, and S. Zhang The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism Nat. Commun. 5 2014 10.1038/ncomms4611
30. S. Fukumoto, M. Tatewaki, T. Yamada, M. Fujimiya, C. Mantyh, M. Voss, S. Eubanks, M. Harris, T.N. Pappas, and T. Takahashi Short-chain fatty acids stimulate colonic transit via intraluminal 5-HT release in rats Am. J. Physiol. Regul. Integr. Comp. Physiol. 284 2003 R1269 R1276
31. L.J. Funkhouser, and S.R. Bordenstein Mom knows best: the universality of maternal microbial transmission PLoS Biol. 11 2013 e1001631
32. M.D. Gershon 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract Curr. Opin. Endocrinol. Diabetes Obes. 20 2013 14 21
33. L.E. Goehler, R.P. Gaykema, N. Opitz, R. Reddaway, N. Badr, and M. Lyte Activation in vagal afferents and central autonomic pathways: early responses to intestinal infection with Campylobacter jejuni Brain Behav. Immun. 19 2005 334 344
34. J.I. Gordon, K.G. Dewey, D.A. Mills, and R.M. Medzhitov The human gut microbiota and undernutrition Sci. Transl. Med. 4 2012 137ps112
35. L.V. Hooper, D.R. Littman, and A.J. Macpherson Interactions between the microbiota and the immune system Science 336 2012 1268 1273
36. P.K. House, A. Vyas, and R. Sapolsky Predator cat odors activate sexual arousal pathways in brains of Toxoplasma gondii infected rats PLoS ONE 6 2011 e23277
37. E.Y. Hsiao Immune dysregulation in autism spectrum disorder Int. Rev. Neurobiol. 113 2013 269 302
38. E.Y. Hsiao, S.W. McBride, J. Chow, S.K. Mazmanian, and P.H. Patterson Modeling an autism risk factor in mice leads to permanent immune dysregulation Proc. Natl. Acad. Sci. USA 109 2012 12776 12781
39. E.Y. Hsiao, S.W. McBride, S. Hsien, G. Sharon, E.R. Hyde, T. McCue, J.A. Codelli, J. Chow, S.E. Reisman, and J.F. Petrosino Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders Cell 155 2013 1451 1463
40. D.P. Hughes Parasitic manipulation: a social context Behav. Processes 68 2005 263 266
41. N.P. Hyland, and J.F. Cryan A Gut Feeling about GABA: Focus on GABA(B) Receptors Front. Pharmacol. 1 2010 124
42. E. Jiménez, M.L. Marín, R. Martín, J.M. Odriozola, M. Olivares, J. Xaus, L. Fernández, and J.M. Rodríguez Is meconium from healthy newborns actually sterile? Res. Microbiol. 159 2008 187 193
43. D.W. Kang, J.G. Park, Z.E. Ilhan, G. Wallstrom, J. Labaer, J.B. Adams, and R. Krajmalnik-Brown Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children PLoS ONE 8 2013 e68322
44. W. Li, S.E. Dowd, B. Scurlock, V. Acosta-Martinez, and M. Lyte Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria Physiol. Behav. 96 2009 557 567
45. Y. Li, Y.Y. Xiang, W.Y. Lu, C. Liu, and J. Li A novel role of intestine epithelial GABAergic signaling in regulating intestinal fluid secretion Am. J. Physiol. Gastrointest. Liver Physiol. 303 2012 G453 G460
46. B. Lu, G. Nagappan, X. Guan, P.J. Nathan, and P. Wren BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases Nat. Rev. Neurosci. 14 2013 401 416
47. P. Lucas, J. Landete, M. Coton, E. Coton, and A. Lonvaud-Funel The tyrosine decarboxylase operon of Lactobacillus brevis IOEB 9809: characterization and conservation in tyramine-producing bacteria FEMS Microbiol. Lett. 229 2003 65 71
48. M. Lyte Microbial endocrinology in the microbiome-gut-brain axis: how bacterial production and utilization of neurochemicals influence behavior PLoS Pathog. 9 2013 e1003726
49. M. Lyte Microbial endocrinology and the microbiota-gut-brain axis Adv. Exp. Med. Biol. 817 2014 3 24
50. V. Macnab, and I. Barber Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences Glob. Change Biol. 18 2012 1540 1548
51. D.P. Maitland A parasitic fungus infecting yellow dungflies manipulates host perching behavior P. Roy. Soc. B.-Biol. Sci. 258 1994 187 193
52. A. Marcobal, P.C. Kashyap, T.A. Nelson, P.A. Aronov, M.S. Donia, A. Spormann, M.A. Fischbach, and J.L. Sonnenburg A metabolomic view of how the human gut microbiota impacts the host metabolome using humanized and gnotobiotic mice ISME J. 7 2013 1933 1943
53. M. Matsumoto, R. Kibe, T. Ooga, Y. Aiba, S. Kurihara, E. Sawaki, Y. Koga, and Y. Benno Impact of intestinal microbiota on intestinal luminal metabolome Sci. Rep. 2 2012 10.1038/srep00233
54. E.A. Mayer, R. Knight, S.K. Mazmanian, J.F. Cryan, and K. Tillisch Gut microbes and the brain: paradigm shift in neuroscience J. Neurosci. 34 2014 15490 15496
55. E.A. Mayer, K. Tillisch, and A. Gupta Gut/brain axis and the microbiota J. Clin. Invest. 125 2015 926 938
56. S.K. Mazmanian, J.L. Round, and D.L. Kasper A microbial symbiosis factor prevents intestinal inflammatory disease Nature 453 2008 620 625
57. N.P. McNulty, T. Yatsunenko, A. Hsiao, J.J. Faith, B.D. Muegge, A.L. Goodman, B. Henrissat, R. Oozeer, S. Cools-Portier, and G. Gobert The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins Sci. Transl. Med. 3 2011 10.1126/scitranslmed.3002701
58. J. Mead, and P. Ashwood Evidence supporting an altered immune response in ASD Immunol. Lett. 163 2015 49 55
59. M. Messaoudi, R. Lalonde, N. Violle, H. Javelot, D. Desor, A. Nejdi, J.F. Bisson, C. Rougeot, M. Pichelin, M. Cazaubiel, and J.M. Cazaubiel 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 2011 755 764
60. K. Meuer, C. Pitzer, P. Teismann, C. Krüger, B. Göricke, R. Laage, P. Lingor, K. Peters, J.C. Schlachetzki, and K. Kobayashi Granulocyte-colony stimulating factor is neuroprotective in a model of Parkinson's disease J. Neurochem. 97 2006 675 686
61. T.L. Miller, and M.J. Wolin Fermentations by saccharolytic intestinal bacteria Am. J. Clin. Nutr. 32 1979 164 172
62. G.Y. Minuk Gamma-aminobutyric acid (GABA) production by eight common bacterial pathogens Scand. J. Infect. Dis. 18 1986 465 467
63. R.W. Mitchell, N.H. On, M.R. Del Bigio, D.W. Miller, and G.M. Hatch Fatty acid transport protein expression in human brain and potential role in fatty acid transport across human brain microvessel endothelial cells J. Neurochem. 117 2011 735 746
64. Montiel-Castro, J. Augusto, Báez-Yáñez, G. Mario, and G. Pacheco-López Social neuroeconomics: the influence of microbiota in partner-choice and sociality Curr. Pharm. Des. 20 2014 4774 4783
65. J.G. Mulle, W.G. Sharp, and J.F. Cubells The gut microbiome: a new frontier in autism research Curr. Psychiatry Rep. 15 2013 337
66. K.M. Neufeld, N. Kang, J. Bienenstock, and J.A. Foster Reduced anxiety-like behavior and central neurochemical change in germ-free mice Neurogastroenterol. Motil. 23 2011 255 264
67. S.M. O'Mahony, G. Clarke, Y.E. Borre, T.G. Dinan, and J.F. Cryan Serotonin, tryptophan metabolism and the brain-gut-microbiome axis Behav. Brain Res. 277 2015 32 48
68. J. Ochoa-Repáraz, D.W. Mielcarz, L.E. Ditrio, A.R. Burroughs, S. Begum-Haque, S. Dasgupta, D.L. Kasper, and L.H. Kasper Central nervous system demyelinating disease protection by the human commensal Bacteroides fragilis depends on polysaccharide A expression J. Immunol. 185 2010 4101 4108
69. F. Ozogul, E. Kuley, Y. Ozogul, and I. Ozogul The Function of Lactic Acid Bacteria on Biogenic Amines Production by Food-Borne Pathogens in Arginine Decarboxylase Broth Food Sci. Technol. Res. 18 2012 795 804
70. R.G. Paredes, and A. Agmo GABA and behavior: the role of receptor subtypes Neurosci. Biobehav. Rev. 16 1992 145 170
71. M. PrabhuDas, E. Bonney, K. Caron, S. Dey, A. Erlebacher, A. Fazleabas, S. Fisher, T. Golos, M. Matzuk, and J.M. McCune Immune mechanisms at the maternal-fetal interface: perspectives and challenges Nat. Immunol. 16 2015 328 334
72. A. Prakash, B. Medhi, and K. Chopra Granulocyte colony stimulating factor (GCSF) improves memory and neurobehavior in an amyloid-β induced experimental model of Alzheimer's disease Pharmacol. Biochem. Behav. 110 2013 46 57
73. B. Pyndt Jørgensen, J.T. Hansen, L. Krych, C. Larsen, A.B. Klein, D.S. Nielsen, K. Josefsen, A.K. Hansen, and D.B. Sørensen A possible link between food and mood: dietary impact on gut microbiota and behavior in BALB/c mice PLoS ONE 9 2014 e103398
74. C.L. Raison, L. Capuron, and A.H. Miller Cytokines sing the blues: inflammation and the pathogenesis of depression Trends Immunol. 27 2006 24 31
75. C.S. Reigstad, C.E. Salmonson, J.F. Rainey 3rd, J.H. Szurszewski, D.R. Linden, J.L. Sonnenburg, G. Farrugia, and P.C. Kashyap Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells FASEB J. 29 2014 1395 1403
76. E. Rosenberg, G. Sharon, I. Atad, and I. Zilber-Rosenberg The evolution of animals and plants via symbiosis with microorganisms Environ. Microbiol. Rep. 2 2010 500 506
77. C.S. Rosenfeld Microbiome Disturbances and Autism Spectrum Disorders Drug Metab. Dispos. 2015 10.1124/dmd.115.063826 in press
78. J.L. Round, and S.K. Mazmanian The gut microbiota shapes intestinal immune responses during health and disease Nat. Rev. Immunol. 9 2009 313 323
79. J.L. Round, and S.K. Mazmanian Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota Proc. Natl. Acad. Sci. USA 107 2010 12204 12209
80. H.M. Savignac, B. Kiely, T.G. Dinan, and J.F. Cryan Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice Neurogastroenterol. Motil. 26 2014 1615 1627
81. H.M. Savignac, M. Tramullas, B. Kiely, T.G. Dinan, and J.F. Cryan Bifidobacteria modulate cognitive processes in an anxious mouse strain Behav. Brain Res. 287 2015 59 72
82. J. Selkrig, P. Wong, X. Zhang, and S. Pettersson Metabolic tinkering by the gut microbiome: Implications for brain development and function Gut Microbes 5 2014 369 380
83. G. Sharon, D. Segal, J.M. Ringo, A. Hefetz, I. Zilber-Rosenberg, and E. Rosenberg Commensal bacteria play a role in mating preference of Drosophila melanogaster Proc. Natl. Acad. Sci. USA 107 2010 20051 20056
84. G. Sharon, N. Garg, J. Debelius, R. Knight, P.C. Dorrestein, and S.K. Mazmanian Specialized metabolites from the microbiome in health and disease Cell Metab. 20 2014 719 730
85. W.C. Shyu, S.Z. Lin, H.I. Yang, Y.S. Tzeng, C.Y. Pang, P.S. Yen, and H. Li Functional recovery of stroke rats induced by granulocyte colony-stimulating factor-stimulated stem cells Circulation 110 2004 1847 1854
86. C. Sobrino Crespo, A. Perianes Cachero, L. Puebla Jimenez, V. Barrios, and E. Arilla Ferreiro Peptides and food intake Front. Endocrinol. (Lausanne) 5 2014 58
87. L. Steenbergen, R. Sellaro, S. van Hemert, J.A. Bosch, and L.S. Colzato A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood Brain Behav. Immun. 2015 10.1016/j.bbi.2015.04.003 in press
88. R.M. Stilling, S.R. Bordenstein, T.G. Dinan, and J.F. Cryan Friends with social benefits: host-microbe interactions as a driver of brain evolution and development? Front. Cell. Infect. Microbiol. 4 2014 147
89. R.M. Stilling, T.G. Dinan, and J.F. Cryan Microbial genes, brain & behaviour - epigenetic regulation of the gut-brain axis Genes Brain Behav. 13 2014 69 86
90. N. Sudo, Y. Chida, Y. Aiba, J. Sonoda, N. Oyama, X.N. Yu, C. Kubo, and Y. Koga Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice J. Physiol. 558 2004 263 275
91. K.R. Theis, T.M. Schmidt, and K.E. Holekamp Evidence for a bacterial mechanism for group-specific social odors among hyenas Sci. Rep. 2 2012 615
92. K.R. Theis, A. Venkataraman, J.A. Dycus, K.D. Koonter, E.N. Schmitt-Matzen, A.P. Wagner, K.E. Holekamp, and T.M. Schmidt Symbiotic bacteria appear to mediate hyena social odors Proc. Natl. Acad. Sci. USA 110 2013 19832 19837
93. K. Tillisch, J. Labus, L. Kilpatrick, Z. Jiang, J. Stains, B. Ebrat, D. Guyonnet, S. Legrain-Raspaud, B. Trotin, and B. Naliboff Consumption of fermented milk product with probiotic modulates brain activity Gastroenterology 144 2013 1394 1401
94. A.M. van Dam, M. Brouns, S. Louisse, and F. Berkenbosch 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 1992 291 296
95. P.O. Vandvik, I. Wilhelmsen, C. Ihlebaek, and P.G. Farup Comorbidity of irritable bowel syndrome in general practice: a striking feature with clinical implications Aliment. Pharmacol. Ther. 20 2004 1195 1203
96. V.R. Velagapudi, R. Hezaveh, C.S. Reigstad, P. Gopalacharyulu, L. Yetukuri, S. Islam, J. Felin, R. Perkins, J. Borén, M. Oresic, and F. Bäckhed The gut microbiota modulates host energy and lipid metabolism in mice J. Lipid Res. 51 2010 1101 1112
97. J. Vetulani Early maternal separation: a rodent model of depression and a prevailing human condition Pharmacol. Rep. 65 2013 1451 1461
98. M. Vijay-Kumar, J.D. Aitken, F.A. Carvalho, T.C. Cullender, S. Mwangi, S. Srinivasan, S.V. Sitaraman, R. Knight, R.E. Ley, and A.T. Gewirtz Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5 Science 328 2010 228 231
99. R. Wall, J.F. Cryan, R.P. Ross, G.F. Fitzgerald, T.G. Dinan, and C. Stanton Bacterial neuroactive compounds produced by psychobiotics Adv. Exp. Med. Biol. 817 2014 221 239
100. W.R. Wikoff, A.T. Anfora, J. Liu, P.G. Schultz, S.A. Lesley, E.C. Peters, and G. Siuzdak Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites Proc. Natl. Acad. Sci. USA 106 2009 3698 3703
101. B.B. Williams, A.H. Van Benschoten, P. Cimermancic, M.S. Donia, M. Zimmermann, M. Taketani, A. Ishihara, P.C. Kashyap, J.S. Fraser, and M.A. Fischbach Discovery and characterization of gut microbiota decarboxylases that can produce the neurotransmitter tryptamine Cell Host Microbe 16 2014 495 503
102. J.M. Yano, K. Yu, G.P. Donaldson, G.G. Shastri, P. Ann, L. Ma, C.R. Nagler, R.F. Ismagilov, S.K. Mazmanian, and E.Y. Hsiao Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis Cell 161 2015 264 276
103. L.R. Zhao, Y. Navalitloha, S. Singhal, J. Mehta, C.S. Piao, W.P. Guo, J.A. Kessler, and D.R. Groothuis Hematopoietic growth factors pass through the blood-brain barrier in intact rats Exp. Neurol. 204 2007 569 573
104. C.B. Zhu, R.D. Blakely, and W.A. Hewlett The proinflammatory cytokines interleukin-1beta and tumor necrosis factor-alpha activate serotonin transporters Neuropsychopharmacology 31 2006 2121 2131
105. R. Zucchi, G. Chiellini, T.S. Scanlan, and D.K. Grandy Trace amine-associated receptors and their ligands Br. J. Pharmacol. 149 2006 967 978