Differential effects of psychotropic drugs on microbiome composition and gastrointestinal function

Psychopharmacology

Volumn 236, Issue 5, 2019, Pages 1671-1685

  Cussotto, Sofia ^a,b   Strain, Conall R ^a,c   Fouhy, Fiona ^a,c   Strain, Ronan G ^a,c   Peterson, Veronica L ^a,b   Clarke, Gerard ^a,b   Stanton, Catherine ^a,b,c   Dinan, Timothy G ^a,b   Cryan, John F ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c TEAGASC FOOD RESEARCH CENTRE   (Ireland)

Author keywords

Antimicrobial; Diversity; Gut microbiota; Intestinal permeability; Psychotropics; Richness; Short chain fatty acids

Indexed keywords

ACETIC ACID; ARIPIPRAZOLE; BUTYRIC ACID; DRINKING WATER; ESCITALOPRAM; FLUOXETINE; ISOVALERIC ACID; LITHIUM SALT; PROPIONIC ACID; PSYCHOTROPIC AGENT; SODIUM CHLORIDE; VALPROIC ACID; VENLAFAXINE; ANTIINFECTIVE AGENT;

ADULT; ANIMAL EXPERIMENT; ANTIBACTERIAL ACTIVITY; ARTICLE; CECUM; CHRISTENSENELLACEAE; CLOSTRIDIUM; CONTROLLED STUDY; DRUG MECHANISM; DRUG SAFETY; ESCHERICHIA COLI; FATTY ACID ANALYSIS; GASTROINTESTINAL TRACT FUNCTION; ILEUM; IN VITRO STUDY; IN VIVO STUDY; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; INTESTINE PARAMETERS; INTESTINIBACTER; LACTOBACILLUS RHAMNOSUS; LONG TERM CARE; MALE; MICROBIAL DIVERSITY; NONHUMAN; OPEN FIELD TEST; PEPTOCLOSTRIDIUM; PRIORITY JOURNAL; RAT; SPECIES COMPOSITION; SPECIES RICHNESS; TREATMENT DURATION; ANIMAL; DOSE RESPONSE; DRUG EFFECT; GASTROINTESTINAL TRACT; HUMAN; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTI-BACTERIAL AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESCHERICHIA COLI; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; LACTOBACILLUS RHAMNOSUS; MALE; PSYCHOTROPIC DRUGS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 85053237031     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-018-5006-5     Document Type: Article

References (102)

1. Ackenheil M, Weber K (2004) Differing response to antipsychotic therapy in schizophrenia: pharmacogenomic aspects. Dialogues Clin Neurosci 6:71–77
2. Al-Harbi KS (2012) Treatment-resistant depression: therapeutic trends, challenges, and future directions. Patient Preference Adherence 6:369–388
3. Ariel L, Inbar S, Edut S, Richter-Levin G (2017) Fluoxetine treatment is effective in a rat model of childhood-induced post-traumatic stress disorder. Transl Psychiatry 7:1260
4. Ayaz M, Subhan F, Ahmed J, Khan A-u, Ullah F, Ullah I, Ali G, Syed N-i-H, Hussain S (2015a) Sertraline enhances the activity of antimicrobial agents against pathogens of clinical relevance. J Biol Res 22:4
5. Ayaz M, Subhan F, Ahmed J, Khan AU, Ullah F, Ullah I, Ali G, Syed NI, Hussain S (2015b) Sertraline enhances the activity of antimicrobial agents against pathogens of clinical relevance. J Biol Res (Thessalon) 22:4
6. Bahr SM, Tyler BC, Wooldridge N, Butcher BD, Burns TL, Teesch LM, Oltman CL, Azcarate-Peril MA, Kirby JR, Calarge CA (2015a) Use of the second-generation antipsychotic, risperidone, and secondary weight gain are associated with an altered gut microbiota in children. Transl Psychiatry 5:e652
7. Bahr SM, Weidemann BJ, Castro AN, Walsh JW, deLeon O, Burnett CML, Pearson NA, Murry DJ, Grobe JL, Kirby JR (2015b) Risperidone-induced weight gain is mediated through shifts in the gut microbiome and suppression of energy expenditure. EBioMedicine 2:1725–1734
8. Bercik P, Collins SM, Verdu EF (2012) Microbes and the gut-brain axis. Neurogastroenterology Motility 24:405–413
9. Beyazyüz M, Albayrak Y, Eğilmez OB, Albayrak N, Beyazyüz E (2013) Relationship between SSRIs and metabolic syndrome abnormalities in patients with generalized anxiety disorder: a prospective study. Psychiatry Investigation 10:148–154
10. Bischoff SC, Mailer R, Pabst O, Weier G, Sedlik W, Li Z, Chen JJ, Murphy DL, Gershon MD (2009) Role of serotonin in intestinal inflammation: knockout of serotonin reuptake transporter exacerbates 2,4,6-trinitrobenzene sulfonic acid colitis in mice. Am J Physiol Gastrointest Liver Physiol 296:G685–G695
11. Bohnert JA, Szymaniak-Vits M, Schuster S, Kern WV (2011a) Efflux inhibition by selective serotonin reuptake inhibitors in Escherichia coli. J Antimicrob Chemother 66:2057–2060
12. Bohnert JA, Szymaniak-Vits M, Schuster S, Kern WV (2011b) Efflux inhibition by selective serotonin reuptake inhibitors in Escherichia coli. J Antimicrob Chemother 66:2057–2060
13. Cani PD, Lecourt E, Dewulf EM, Sohet FM, Pachikian BD, Naslain D, De Backer F, Neyrinck AM, Delzenne NM (2009) 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 90:1236–1243
14. Caparrós-Martín JA, Lareu RR, Ramsay JP, Peplies J, Reen FJ, Headlam HA, Ward NC, Croft KD, Newsholme P, Hughes JD, O’Gara F (2017) Statin therapy causes gut dysbiosis in mice through a PXR-dependent mechanism. Microbiome 5:95
15. Chen JX, Pan H, Rothman TP, Wade PR, Gershon MD (1998) Guinea pig 5-HT transporter: cloning, expression, distribution, and function in intestinal sensory reception. Am J Phys 275:G433–G448
16. Chen JJ, Li Z, Pan H, Murphy DL, Tamir H, Koepsell H, Gershon MD (2001) Maintenance of serotonin in the intestinal mucosa and ganglia of mice that lack the high-affinity serotonin transporter: abnormal intestinal motility and the expression of cation transporters. J Neurosci 21:6348–6361
17. Chen L, Wilson JE, Koenigsknecht MJ, Chou WC, Montgomery SA, Truax AD, Brickey WJ, Packey CD, Maharshak N, Matsushima GK, Plevy SE, Young VB, Sartor RB, Ting JP (2017) NLRP12 attenuates colon inflammation by maintaining colonic microbial diversity and promoting protective commensal bacterial growth. Nat Immunol 18:541–551
18. Coates MD, Mahoney CR, Linden DR, Sampson JE, Chen J, Blaszyk H, Crowell MD, Sharkey KA, Gershon MD, Mawe GM, Moses PL (2004) Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome. Gastroenterology 126:1657–1664
19. Coban AY, Tanriverdi Cayci Y, Keles Uludag S, Durupinar B (2009) Investigation of antibacterial activity of sertralin. Mikrobiyol Bul 43:651–656
20. Collins SM, Surette M, Bercik P (2012) The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 10:735–742
21. Correll CU, Detraux J, De Lepeleire J, De Hert M (2015) Effects of antipsychotics, antidepressants and mood stabilizers on risk for physical diseases in people with schizophrenia, depression and bipolar disorder. World Psychiatry 14:119–136
22. Cryan JF, Dinan TG (2012a) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13:701–712
23. Cryan JF, Dinan TG (2012b) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13:701–712
24. Davey KJ, O’Mahony SM, Schellekens H, O’Sullivan O, Bienenstock J, Cotter PD, Dinan TG, Cryan JF (2012) Gender-dependent consequences of chronic olanzapine in the rat: effects on body weight, inflammatory, metabolic and microbiota parameters. Psychopharmacology 221:155–169
25. Davey KJ, Cotter PD, O'Sullivan O, Crispie F, Dinan TG, Cryan JF, O'Mahony SM (2013) Antipsychotics and the gut microbiome: olanzapine-induced metabolic dysfunction is attenuated by antibiotic administration in the rat. Transl Psychiatry 3:e309
26. De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A, Backhed F, Mithieux G (2014) Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 156:84–96
27. van de Wouw M, Schellekens H, Dinan TG, Cryan JF (2017) Microbiota-gut-brain axis: modulator of host metabolism and appetite. J Nutr 147:727–745
28. Dinan TG, Stanton C, Cryan JF (2013) Psychobiotics: a novel class of psychotropic. Biol Psychiatry 74:720–726
29. Dinan TG, Borre YE, Cryan JF (2014) Genomics of schizophrenia: time to consider the gut microbiome? Mol Psychiatry 19:1252–1257
30. Erny D, Hrabe de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, Keren-Shaul H, Mahlakoiv T, Jakobshagen K, Buch T, Schwierzeck V, Utermohlen O, Chun E, Garrett WS, McCoy KD, Diefenbach A, Staeheli P, Stecher B, Amit I, Prinz M (2015) Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 18:965–977
31. Evans SJ, Bassis CM, Hein R, Assari S, Flowers SA, Kelly MB, Young VB, Ellingrod VE, McInnis MG (2017) The gut microbiome composition associates with bipolar disorder and illness severity. J Psychiatr Res 87:23–29
32. Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, Faust K, Kurilshikov A, Bonder MJ, Valles-Colomer M, Vandeputte D, Tito RY, Chaffron S, Rymenans L, Verspecht C, De Sutter L, Lima-Mendez G, D'Hoe K, Jonckheere K, Homola D, Garcia R, Tigchelaar EF, Eeckhaudt L, Fu J, Henckaerts L, Zhernakova A, Wijmenga C, Raes J (2016) Population-level analysis of gut microbiome variation. Science 352:560–564
33. Flowers SA, Evans SJ, Ward KM, McInnis MG, Ellingrod VL (2017a) Interaction between atypical antipsychotics and the gut microbiome in a bipolar disease cohort. Pharmacotherapy 37:261–267
34. Flowers SA, Evans SJ, Ward KM, McInnis MG, Ellingrod VL (2017b) Interaction between atypical antipsychotics and the gut microbiome in a bipolar disease cohort. Pharmacotherapy: J Human Pharmacology Drug Therapy 37:261–267
35. Forslund K, Hildebrand F, Nielsen T, Falony G, Le Chatelier E, Sunagawa S, Prifti E, Vieira-Silva S, Gudmundsdottir V, Krogh Pedersen H, Arumugam M, Kristiansen K, Yvonne Voigt A, Vestergaard H, Hercog R, Igor Costea P, Roat Kultima J, Li J, Jørgensen T, Levenez F, Dore J, Meta HIT c, Bjørn Nielsen H, Brunak S, Raes J, Hansen T, Wang J, Dusko Ehrlich S, Bork P, Pedersen O (2015) Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528:262–266
36. Foster JA, McVey Neufeld K-A (2013) Gut–brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 36:305–312
37. Freier TA, Beitz DC, Li L, Hartman PA (1994) Characterization of Eubacterium coprostanoligenes sp. nov., a cholesterol-reducing anaerobe. Int J Syst Bacteriol 44:137–142
38. Gafoor R, Booth HP, Gulliford MC (2018) Antidepressant utilisation and incidence of weight gain during 10 years’ follow-up: population based cohort study. BMJ 361:k1951
39. Golubeva AV, Joyce SA, Moloney G, Burokas A, Sherwin E, Arboleya S, Flynn I, Khochanskiy D, Moya-Pérez A, Peterson V, Rea K, Murphy K, Makarova O, Buravkov S, Hyland NP, Stanton C, Clarke G, Gahan CGM, Dinan TG, Cryan JF (2017) Microbiota-related changes in bile acid and tryptophan metabolism are associated with gastrointestinal dysfunction in a mouse model of autism. EBioMedicine 24:166–178
40. Goodrich JK, Davenport ER, Waters JL, Clark AG, Ley RE (2016) Cross-species comparisons of host genetic associations with the microbiome. Science 352:532–535
41. Grubbs FE (1950) Sample criteria for testing outlying observations. Ann Math Stat 21:27–58
42. Hatta K, Ito H (2014) Strategies for early non-response to antipsychotic drugs in the treatment of acute-phase schizophrenia. Clinical Psychopharmacology Neuroscience 12:1–7
43. Haub S, Ritze Y, Bergheim I, Pabst O, Gershon MD, Bischoff SC (2010) Enhancement of intestinal inflammation in mice lacking interleukin 10 by deletion of the serotonin reuptake transporter. Neurogastroenterol Motil 22(826–834):e229
44. Huuskonen J, Suuronen T, Nuutinen T, Kyrylenko S, Salminen A (2004) Regulation of microglial inflammatory response by sodium butyrate and short-chain fatty acids. Br J Pharmacol 141:874–880
45. Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y, Wang W, Tang W, Tan Z, Shi J, Li L, Ruan B (2015) Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun 48:186–194
46. Kaminska K, Rogoz Z (2016) The antidepressant- and anxiolytic-like effects following co-treatment with escitalopram and risperidone in rats. J Physiol Pharmacol 67:471–480
47. Kao AC-C, Spitzer S, Anthony DC, Lennox B, Burnet PWJ (2018) Prebiotic attenuation of olanzapine-induced weight gain in rats: analysis of central and peripheral biomarkers and gut microbiota. Transl Psychiatry 8:66
48. Karl JP, Margolis LM, Madslien EH, Murphy NE, Castellani JW, Gundersen Y, Hoke AV, Levangie MW, Kumar R, Chakraborty N, Gautam A, Hammamieh R, Martini S, Montain SJ, Pasiakos SM (2017) Changes in intestinal microbiota composition and metabolism coincide with increased intestinal permeability in young adults under prolonged physiological stress. Am J Physiol Gastrointest Liver Physiol 312:G559–g571
49. Kelly JR, Borre Y, O’ Brien C, Patterson E, El Aidy S, Deane J, Kennedy PJ, Beers S, Scott K, Moloney G, Hoban AE, Scott L, Fitzgerald P, Ross P, Stanton C, Clarke G, Cryan JF, Dinan TG (2016) Transferring the blues: depression-associated gut microbiota induces neurobehavioural changes in the rat. J Psychiatr Res 82:109–118
50. Kim KA, Gu W, Lee IA, Joh EH, Kim DH (2012) High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One 7:e47713
51. Kiraly DD, Walker DM, Calipari ES, Labonte B, Issler O, Pena CJ, Ribeiro EA, Russo SJ, Nestler EJ (2016) Alterations of the host microbiome affect behavioral responses to cocaine. Sci Rep 6:35455
52. Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F (2016) From dietary Fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165:1332–1345
53. Kong F, Hua Y, Zeng B, Ning R, Li Y, Zhao J (2016) Gut microbiota signatures of longevity. Curr Biol 26:R832–R833
54. Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, De Vadder F, Arora T, Hallen A, Martens E, Björck I, Bäckhed F (2015) Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of Prevotella. Cell Metab 22:971–982
55. Li L, Buhman KK, Hartman PA, Beitz DC (1995) Hypocholesterolemic effect of Eubacterium coprostanoligenes ATCC 51222 in rabbits. Lett Appl Microbiol 20:137–140
56. Li L, Batt SM, Wannemuehler M, Dispirito A, Beitz DC (1998) Effect of feeding of a cholesterol-reducing bacterium, Eubacterium coprostanoligenes, to germ-free mice. Lab Anim Sci 48:253–255
57. Li M, Wang B, Sun X, Tang Y, Wei X, Ge B, Tang Y, Deng Y, He C, Yuan J, Li X (2017) Upregulation of intestinal barrier function in mice with DSS-induced colitis by a defined bacterial consortium is associated with expansion of IL-17A producing gamma delta T cells. Front Immunol 8:824
58. Ling Z, Li Z, Liu X, Cheng Y, Luo Y, Tong X, Yuan L, Wang Y, Sun J, Li L, Xiang C (2014) Altered fecal microbiota composition associated with food allergy in infants. Appl Environ Microbiol 80:2546–2554
59. López-Contreras BE, Morán-Ramos S, Villarruel-Vázquez R, Macías-Kauffer L, Villamil-Ramírez H, León-Mimila P, Vega-Badillo J, Sánchez-Muñoz F, Llanos-Moreno LE, Canizalez-Román A, Río-Navarro B, Ibarra-González I, Vela-Amieva M, Villarreal-Molina T, Ochoa-Leyva A, Aguilar-Salinas CA, Canizales-Quinteros S (2018) Composition of gut microbiota in obese and normal-weight Mexican school-age children and its association with metabolic traits. Pediatric Obesity 13:381–388
60. Luna RA, Foster JA (2015) Gut brain axis: diet microbiota interactions and implications for modulation of anxiety and depression. Curr Opin Biotechnol 32:35–41
61. Lyons L, ElBeltagy M, Bennett G, Wigmore P (2012) Fluoxetine counteracts the cognitive and cellular effects of 5-fluorouracil in the rat hippocampus by a mechanism of prevention rather than recovery. PLoS One 7:e30010
62. Maier L, Pruteanu M, Kuhn M, Zeller G, Telzerow A, Anderson EE, Brochado AR, Fernandez KC, Dose H, Mori H, Patil KR, Bork P, Typas A (2018) Extensive impact of non-antibiotic drugs on human gut bacteria. Nature 555:623–628
63. Mayer EA, Knight R, Mazmanian SK, Cryan JF, Tillisch K (2014) Gut microbes and the brain: paradigm shift in neuroscience. J Neurosci 34:15490–15496
64. Mayer EA, Tillisch K, Gupta A (2015) Gut/brain axis and the microbiota. J Clin Invest 125:926–938
65. Monti B, Gatta V, Piretti F, Raffaelli SS, Virgili M, Contestabile A (2010) Valproic acid is neuroprotective in the rotenone rat model of Parkinson’s disease: involvement of alpha-synuclein. Neurotox Res 17:130–141
66. Morgan AP, Crowley JJ, Nonneman RJ, Quackenbush CR, Miller CN, Ryan AK, Bogue MA, Paredes SH, Yourstone S, Carroll IM, Kawula TH, Bower MA, Sartor RB, Sullivan PF (2014) The antipsychotic olanzapine interacts with the gut microbiome to cause weight gain in mouse. PLoS One 9:e115225
67. Morrison DJ, Preston T (2016) Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7:189–200
68. Munoz-Bellido JL, Munoz-Criado S, Garcia-Rodriguez JA (1996) In-vitro activity of psychiatric drugs against Corynebacterium urealyticum (Corynebacterium group D2). J Antimicrob Chemother 37:1005–1009
69. Munoz-Bellido JL, Munoz-Criado S, Garcia-Rodriguez JA (2000) Antimicrobial activity of psychotropic drugs: selective serotonin reuptake inhibitors. Int J Antimicrob Agents 14:177–180
70. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res 54:2325–2340
71. Naseribafrouei A, Hestad K, Avershina E, Sekelja M, Linløkken A, Wilson R, Rudi K (2014) Correlation between the human fecal microbiota and depression. Neurogastroenterology Motility 26:1155–1162
72. Nelson JC (1998) Treatment of antidepressant nonresponders: augmentation or switch? J Clin Psychiatry 59(Suppl 15):35–41
73. O’Leary OF, O’Connor RM, Cryan JF (2012) Lithium-induced effects on adult hippocampal neurogenesis are topographically segregated along the dorso-ventral axis of stressed mice. Neuropharmacology 62:247–255
74. O’Mahony SM, Felice VD, Nally K, Savignac HM, Claesson MJ, Scully P, Woznicki J, Hyland NP, Shanahan F, Quigley EM, Marchesi JR, O’Toole PW, Dinan TG, Cryan JF (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
75. Olguner Eker Ö, ÖZsoy S, Eker B, DoĞAn H (2017) Metabolic effects of antidepressant treatment. Archives Neuropsychiatry 54:49–56
76. Olivares, M., Neef, A., Castillejo, G., Palma, G. D., Varea, V., Capilla, A., Palau, F., Nova, E., Marcos, A., Polanco, I., Ribes-Koninckx, C., Ortigosa, L., Izquierdo, L., Sanz, Y., 2014. The HLA-DQ2 genotype selects for early intestinal microbiota composition in infants at high risk of developing coeliac disease. Gut
77. Ott B, Skurk T, Hastreiter L, Lagkouvardos I, Fischer S, Büttner J, Kellerer T, Clavel T, Rychlik M, Haller D, Hauner H (2017) Effect of caloric restriction on gut permeability, inflammation markers, and fecal microbiota in obese women. Sci Rep 7:11955
78. Paquin-Proulx D, Ching C, Vujkovic-Cvijin I, Fadrosh D, Loh L, Huang Y, Somsouk M, Lynch SV, Hunt PW, Nixon DF, SenGupta D (2016) Bacteroides are associated with GALT iNKT cell function and reduction of microbial translocation in HIV-1 infection. Mucosal Immunol 10:69
79. Raman M, Ahmed I, Gillevet PM, Probert CS, Ratcliffe NM, Smith S, Greenwood R, Sikaroodi M, Lam V, Crotty P, Bailey J, Myers RP, Rioux KP (2013) Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clinical Gastroenterology Hepatology 11 e863:868–875
80. Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE Jr, Balish E, Taurog JD, Hammer RE, Wilson KH, Sartor RB (1996) Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J Clin Invest 98:945–953
81. Ren D, Li L, Schwabacher AW, Young JW, Beitz DC (1996) Mechanism of cholesterol reduction to coprostanol by Eubacterium coprostanoligenes ATCC 51222. Steroids 61:33–40
82. Reynolds GP, Kirk SL (2010) Metabolic side effects of antipsychotic drug treatment – pharmacological mechanisms. Pharmacol Ther 125:169–179
83. Schroeder FA, Lin CL, Crusio WE, Akbarian S (2007) Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry 62:55–64
84. Schubert AM, Rogers MA, Ring C, Mogle J, Petrosino JP, Young VB, Aronoff DM, Schloss PD (2014) Microbiome data distinguish patients with Clostridium difficile infection and non-C. difficile-associated diarrhea from healthy controls. MBio 5:e01021–e01014
85. Schwarz E, Maukonen J, Hyytiäinen T, Kieseppä T, Orešič M, Sabunciyan S, Mantere O, Saarela M, Yolken R, Suvisaari J (2017) Analysis of microbiota in first episode psychosis identifies preliminary associations with symptom severity and treatment response. Schizophr Res 192:398–403
86. Scott KA, Ida M, Peterson VL, Prenderville JA, Moloney GM, Izumo T, Murphy K, Murphy A, Ross RP, Stanton C, Dinan TG, Cryan JF (2017) Revisiting Metchnikoff: age-related alterations in microbiota-gut-brain axis in the mouse. Brain Behav Immun 65:20–32
87. Segnitz N, Schmitt A, Gebicke-Harter PJ, Zink M (2009) Differential expression of glutamate transporter genes after chronic oral treatment with aripiprazole in rats. Neurochem Int 55:619–628
88. Sogaard B, Mengel H, Rao N, Larsen F (2005) The pharmacokinetics of escitalopram after oral and intravenous administration of single and multiple doses to healthy subjects. J Clin Pharmacol 45:1400–1406
89. Thursby E, Juge N (2017) Introduction to the human gut microbiota. Biochem J 474:1823–1836
90. Torres-Fuentes C, Schellekens H, Dinan TG, Cryan JF (2017) The microbiota–gut–brain axis in obesity. Lancet Gastroenterology Hepatology 2:747–756
91. Tschoner A, Engl J, Laimer M, Kaser S, Rettenbacher M, Fleischhacker WW, Patsch JR, Ebenbichler CF (2007) Metabolic side effects of antipsychotic medication. Int J Clin Pract 61:1356–1370
92. Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC (2011) Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr 141:769–776
93. Vidal R, Valdizan E, Vilaró M, Pazos A, Castro E (2010) Reduced signal transduction by 5-HT4 receptors after long-term venlafaxine treatment in rats. Br J Pharmacol 161:695–706
94. Wade PR, Chen J, Jaffe B, Kassem IS, Blakely RD, Gershon MD (1996) Localization and function of a 5-HT transporter in crypt epithelia of the gastrointestinal tract. J Neurosci 16:2352–2364
95. Walter J (2008) Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 74:4985–4996
96. Watase K, Gatchel JR, Sun Y, Emamian E, Atkinson R, Richman R, Mizusawa H, Orr HT, Shaw C, Zoghbi HY (2007) Lithium therapy improves neurological function and hippocampal dendritic arborization in a spinocerebellar ataxia type 1 mouse model. PLoS Med 4:e182
97. World Health Organization, 2017. Depression and other common mental disorders: global health estimates. Geneva
98. Wu H, Esteve E, Tremaroli V, Khan MT, Caesar R, Mannerås-Holm L, Ståhlman M, Olsson LM, Serino M, Planas-Fèlix M, Xifra G, Mercader JM, Torrents D, Burcelin R, Ricart W, Perkins R, Fernàndez-Real JM, Bäckhed F (2017) Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat Med 23:850–858
99. Xie, Y., Zhou, G., Wang, C., Xu, X., Li, C., 2018. Temporal changes in gut microbiota and signaling molecules of the gut-brain axis in mice fed meat protein diets. bioRxiv
100. Yamada T, Inui A, Hayashi N, Fujimura M, Fujimiya M (2003) Serotonin stimulates endotoxin translocation via 5-HT3 receptors in the rat ileum. Am J Physiol Gastrointest Liver Physiol 284:G782–G788
101. Zhan G, Yang N, Li S, Huang N, Fang X, Zhang J, Zhu B, Yang L, Yang C, Luo A (2018) Abnormal gut microbiota composition contributes to cognitive dysfunction in SAMP8 mice. Aging (Albany NY) 10:1257–1267
102. Zheng P, Zeng B, Zhou C, Liu M, Fang Z, Xu X, Zeng L, Chen J, Fan S, Du X, Zhang X, Yang D, Yang Y, Meng H, Li W, Melgiri ND, Licinio J, Wei H, Xie P (2016) Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host's metabolism. Mol Psychiatry 21:786–796