Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice

Neurogastroenterology and Motility

Volumn 26, Issue 11, 2014, Pages 1615-1627

  Savignac, H M ^a   Kiely, B ^b   Dinan, T G ^c   Cryan, J F ^c  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b ALIMENTARY HEALTH LTD   (Ireland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Anxiety; BALB c mice; Behavior; Bifidobacteria; Corticosterone; Depression related behavior; Stress

Indexed keywords

ANTIDEPRESSANT AGENT; CITALOPRAM; PROBIOTIC AGENT;

ANIMAL; ANIMAL BEHAVIOR; ANXIETY; BAGG ALBINO MOUSE; BIFIDOBACTERIUM; DISEASE MODEL; MALE; MENTAL STRESS; MICROBIOLOGY; MOUSE;

ANIMALS; ANTIDEPRESSIVE AGENTS; ANXIETY; BEHAVIOR, ANIMAL; BIFIDOBACTERIUM; CITALOPRAM; DISEASE MODELS, ANIMAL; MALE; MICE; MICE, INBRED BALB C; PROBIOTICS; STRESS, PSYCHOLOGICAL;

EID: 84907873992     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12427     Document Type: Article

References (105)

1. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 2012; 10: 735-42.
2. Dinan TG, Cryan JF. Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology 2012; 37: 1369-78.
3. Carroll IM, Ringel-Kulka T, Keku TO, Chang YH, Packey CD, Sartor RB, Ringel Y. Molecular analysis of the luminal- and mucosal-associated intestinal microbiota in diarrhea-predominant irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 2011; 301: G799-807.
4. Jeffery IB, O'Toole PW, Ohman L, Claesson MJ, Deane J, Quigley EM, Simren M. An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota. Gut 2012; 61: 997-1006.
5. Lutgendorff F, Akkermans LM, Soderholm JD. The role of microbiota and probiotics in stress-induced gastro-intestinal damage. Curr Mol Med 2008; 8: 282-98.
6. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 2011; 25: 397-407.
7. O'Mahony SM, Savignac HM, O'Brien T, Scully P, Quigley EM, Marchesi J, O'Toole PW, Dinan TG et al. Early-life dysbiosis-induced visceral hypersensitivity in adulthood. Gastroenterology 2010; 138: S-1-S-906-Supplement 901.
8. Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney RD, Shanahan F, Dinan TG, Cryan JF. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 2013; 18: 666-73.
9. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012; 13: 701-12.
10. Neufeld KM, Kang N, Bienenstock J, Foster JA. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil 2011; 23: 255-64 e119.
11. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, Kubo C, Koga Y. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004; 558: 263-75.
12. Collins SM, Kassam Z, Bercik P. The adoptive transfer of behavioral phenotype via the intestinal microbiota: experimental evidence and clinical implications. Curr Opin Microbiol 2013; 16: 240-5.
13. Shanahan F, Dinan TG, Ross P, Hill C. Probiotics in transition. Clin Gastroenterol Hepatol 2012; 10: 1220-4.
14. Bercik P, Collins SM, Verdu EF. Microbes and the gut-brain axis. Neurogastroenterol Motil 2012; 24: 405-13.
15. Dinan TG, Stanton C, Cryan JF. Psychobiotics: a novel class of psychotropic. Biol Psychiatry 2013; 74: 720-6.
16. Gareau MG, Jury J, MacQueen G, Sherman PM, Perdue MH. Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 2007; 56: 1522-8.
17. Rao AV, Bested AC, Beaulne TM, Katzman MA, Iorio C, Berardi JM, Logan AC. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog 2009; 1: 6.
18. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A 2011; 108: 16050-5.
19. Bercik P, Park AJ, Sinclair D, Khoshdel A, Lu J, Huang X, Deng Y, Blennerhassett PA et al. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol Motil 2011a; 23: 1132-9.
20. Bercik P, Verdu EF, Foster JA, Macri J, Potter M, Huang X, Malinowski P, Jackson W et al. Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous system biochemistry in mice. Gastroenterology 2010; 139: 2102-12 e2101.
21. Ishibashi N, Yaeshima T, Hayasawa H. Bifidobacteria: their significance in human intestinal health. Mal J Nutr 1997; 3: 149-59.
22. Leahy SC, Higgins DG, Fitzgerald GF, van Sinderen D. Getting better with bifidobacteria. J Appl Microbiol 2005; 98: 1303-15.
23. Wopereis H, Oozeer R, Knipping K, Belzer C, Knol J. The first thousand days - intestinal microbiology of early life: establishing a symbiosis. Pediatr Allergy Immunol 2014; 25: 428-38.
24. O'Mahony L, McCarthy J, Kelly P, Hurley G, Luo F, Chen K, O'Sullivan GC, Kiely B et al. Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 2005; 128: 541-51.
25. McKernan DP, Fitzgerald P, Dinan TG, Cryan JF. The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat. Neurogastroenterol Motil 2010; 22(1029-1035): e1268.
26. Whorwell PJ, Altringer L, Morel J, Bond Y, Charbonneau D, O'Mahony L, Kiely B, Shanahan F et al. Efficacy of an encapsulated probiotic Bifidobacterium infantis 35624 in women with irritable bowel syndrome. Am J Gastroenterol 2006; 101: 1581-90.
27. Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG. The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res 2008; 43: 164-74.
28. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010; 170: 1179-88.
29. O'Sullivan E, Barrett E, Grenham S, Fitzgerald P, Stanton C, Ross RP, Quigley EM, Cryan JF et al. BDNF expression in the hippocampus of maternally separated rats: does Bifidobacterium breve 6330 alter BDNF levels? Benef Microbes 2011; 2: 199-207.
30. Wall R, Ross RP, Shanahan F, O'Mahony L, Kiely B, Quigley E, Dinan TG, Fitzgerald G et al. Impact of administered bifidobacterium on murine host fatty acid composition. Lipids 2010; 45: 429-36.
31. Belzung C, Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 2001; 125: 141-9.
32. Savignac HM, Hyland NP, Dinan TG, Cryan JF. The effects of repeated social interaction stress on behavioural and physiological parameters in a stress-sensitive mouse strain. Behav Brain Res 2011; 216: 576-84.
33. Dunne C, Murphy L, Flynn S, O'Mahony L, O'Halloran S, Feeney M, Morrissey D, Thornton G et al. Probiotics: from myth to reality. Demonstration of functionality in animal models of disease and in human clinical trials. Antonie Van Leeuwenhoek 1999; 76: 279-92.
34. Ji Y, Hebbring S, Zhu H, Jenkins GD, Biernacka J, Snyder K, Drews M, Fiehn O et al. Glycine and a glycine dehydrogenase (GLDC) SNP as citalopram/escitalopram response biomarkers in depression: pharmacometabolomics-informed pharmacogenomics. Clin Pharmacol Ther 2011; 89: 97-104.
35. Crawley JN. Behavioral phenotyping strategies for mutant mice. Neuron 2008; 57: 809-18.
36. Cryan JF, Kelly PH, Neijt HC, Sansig G, Flor PJ, van Der Putten H. Antidepressant and anxiolytic-like effects in mice lacking the group III metabotropic glutamate receptor mGluR7. Eur J Neurosci 2003; 17: 2409-17.
37. Jacobson LH, Bettler B, Kaupmann K, Cryan JF. Behavioral evaluation of mice deficient in GABA(B(1)) receptor isoforms in tests of unconditioned anxiety. Psychopharmacology 2007; 190: 541-53.
38. Rodgers RJ, Johnson NJ. Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacol Biochem Behav 1995; 52: 297-303.
39. Barone FC, Barton ME, White RF, Legos JJ, Kikkawa H, Shimamura M, Kuratani K, Kinoshita M. Inhibition of phosphodiesterase type 4 decreases stress-induced defecation in rats and mice. Pharmacology 2008; 81: 11-7.
40. Cryan JF, Mombereau C, Vassout A. The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci Biobehav Rev 2005; 29: 571-625.
41. Jacobson LH, Cryan JF. Feeling strained? Influence of genetic background on depression-related behavior in mice: a review. Behav Genet 2007; 37: 171-213.
42. Reber SO, Obermeier F, Straub RH, Falk W, Neumann ID. Chronic intermittent psychosocial stress (social defeat/overcrowding) in mice increases the severity of an acute DSS-induced colitis and impairs regeneration. Endocrinology 2006; 147: 4968-76.
43. Bartolomucci A, Palanza P, Sacerdote P, Panerai AE, Sgoifo A, Dantzer R, Parmigiani S. Social factors and individual vulnerability to chronic stress exposure. Neurosci Biobehav Rev 2005; 29: 67-81.
44. Engler H, Engler A, Bailey MT, Sheridan JF. Tissue-specific alterations in the glucocorticoid sensitivity of immune cells following repeated social defeat in mice. J Neuroimmunol 2005; 163: 110-9.
45. Krishnan V, Han MH, Graham DL, Berton O, Renthal W, Russo SJ, Laplant Q, Graham A et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007; 131: 391-404.
46. Reber SO, Birkeneder L, Veenema AH, Obermeier F, Falk W, Straub RH, Neumann ID. Adrenal insufficiency and colonic inflammation after a novel chronic psycho-social stress paradigm in mice: implications and mechanisms. Endocrinology 2007; 148: 670-82.
47. Dinan TG, Cryan JF. Melancholic microbes: a link between gut microbiota and depression? Neurogastroenterol Motil 2013; 25: 713-9.
48. Forsythe P, Kunze WA. Voices from within: gut microbes and the CNS. Cell Mol Life Sci 2013; 70: 55-69.
49. Rhee SH, Pothoulakis C, Mayer EA. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol 2009; 6: 306-14.
50. Gareau MG, Wine E, Rodrigues DM, Cho JH, Whary MT, Philpott DJ, Macqueen G, Sherman PM. Bacterial infection causes stress-induced memory dysfunction in mice. Gut 2011; 60: 307-17.
51. Ait-Belgnaoui A, Durand H, Cartier C, Chaumaz G, Eutamene H, Ferrier L, Houdeau E, Fioramonti J et al. Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology 2012; 37: 1885-95.
52. Arseneault-Breard J, Rondeau I, Gilbert K, Girard SA, Tompkins TA, Godbout R, Rousseau G. Combination of Lactobacillus helveticus R0052 and Bifidobacterium longum R0175 reduces post-myocardial infarction depression symptoms and restores intestinal permeability in a rat model. Br J Nutr 2012; 107: 1793-9.
53. Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejdi A, Bisson JF, Rougeot C et al. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 2011; 105: 755-64.
54. Ohland CL, Kish L, Bell H, Thiesen A, Hotte N, Pankiv E, Madsen KL. Effects of Lactobacillus helveticus on murine behavior are dependent on diet and genotype and correlate with alterations in the gut microbiome. Psychoneuroendocrinology 2013; 38: 1738-47.
55. Matthews DM, Jenks SM. Ingestion of Mycobacterium vaccae decreases anxiety-related behavior and improves learning in mice. Behav Processes 2013; 96: 27-35.
56. Ashraf R, Shah NP. Immune system stimulation by probiotic microorganisms. Crit Rev Food Sci Nutr 2014; 54: 938-56.
57. Hasnain M, Vieweg WV. Weight considerations in psychotropic drug prescribing and switching. Postgrad Med 2013; 125: 117-29.
58. Wade AG, Crawford GM, Yellowlees A. Efficacy, safety and tolerability of escitalopram in doses up to 50 mg in Major Depressive Disorder (MDD): an open-label, pilot study. BMC psychiatry 2011; 11: 42.
59. Uher R, Mors O, Hauser J, Rietschel M, Maier W, Kozel D, Henigsberg N, Souery D et al. Changes in body weight during pharmacological treatment of depression. Int J Neuropsychopharmacol 2011; 14: 367-75.
60. Unterecker S, Deckert J, Pfuhlmann B. No influence of body weight on serum levels of antidepressants. Ther Drug Monit 2011; 33: 730-4.
61. Davey KJ, Cotter PD, O'Sullivan O, Crispie F, Dinan TG, Cryan JF, O'Mahony SM. Antipsychotics and the gut microbiome: olanzapine-induced metabolic dysfunction is attenuated by antibiotic administration in the rat. Transl Psychiatry 2013; 3: e309.
62. Kang MJ, Kim HG, Kim JS, Oh do G, Um YJ, Seo CS, Han JW, Cho HJ et al. The effect of gut microbiota on drug metabolism. Expert Opin Drug Metab Toxicol 2013; 9: 1295-308.
63. Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillere R, Hannani D, Enot DP, Pfirschke C et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 2013; 342: 971-6.
64. Delzenne NM, Cani PD. Interaction between obesity and the gut microbiota: relevance in nutrition. Annu Rev Nutr 2011; 31: 15-31.
65. Million M, Angelakis E, Maraninchi M, Henry M, Giorgi R, Valero R, Vialettes B, Raoult D. Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int J Obes (Lond) 2013; 37: 1460-6.
66. Scarpellini E, Campanale M, Leone D, Purchiaroni F, Vitale G, Lauritano EC, Gasbarrini A. Gut microbiota and obesity. Intern Emerg Med 2010; 5(Suppl. 1): S53-6.
67. Angelakis E, Bastelica D, Ben Amara A, El Filali A, Dutour A, Mege JL, Alessi MC, Raoult D. An evaluation of the effects of Lactobacillus ingluviei on body weight, the intestinal microbiome and metabolism in mice. Microb Pathog 2012; 52: 61-8.
68. Delzenne NM, Neyrinck AM, Backhed F, Cani PD. Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol 2011; 7: 639-46.
69. Schellekens H, Dinan TG, Cryan JF. Ghrelin at the interface of obesity and reward. Vitam Horm 2013; 91: 285-323.
70. Diop L, Guillou S, Durand H. Probiotic food supplement reduces stress-induced gastrointestinal symptoms in volunteers: a double-blind, placebo-controlled, randomized trial. Nutr Res 2008; 28: 1-5.
71. Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B, Guyonnet D, Legrain-Raspaud S et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 2013 144: 1394-401, 1401 e1391-1394.
72. Cipriani A, Santilli C, Furukawa TA, Signoretti A, Nakagawa A, McGuire H, Churchill R, Barbui C. Escitalopram versus other antidepressive agents for depression. Cochrane Database Syst Rev 2009; (2). doi: 10.1002/14651858.CD006532.pub2.
73. Sekar S, Verhoye M, Van Audekerke J, Vanhoutte G, Lowe AS, Blamire AM, Steckler T, Van der Linden A et al. Neuroadaptive responses to citalopram in rats using pharmacological magnetic resonance imaging. Psychopharmacology 2011; 213: 521-31.
74. Cryan JF, Markou A, Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 2002; 23: 238-45.
75. Cryan JF, Slattery DA. Animal models of mood disorders: recent developments. Curr Opin Psychiatry 2007; 20: 1-7.
76. Cryan JF, Sweeney FF. The age of anxiety: role of animal models of anxiolytic action in drug discovery. Br J Pharmacol 2011; 164: 1129-61.
77. Bhagya V, Srikumar BN, Raju TR, Shankaranarayana Rao BS. Chronic escitalopram treatment restores spatial learning, monoamine levels, and hippocampal long-term potentiation in an animal model of depression. Psychopharmacology 2011; 214: 477-94.
78. Fish EW, Faccidomo S, Gupta S, Miczek KA. Anxiolytic-like effects of escitalopram, citalopram, and R-citalopram in maternally separated mouse pups. J Pharmacol Exp Ther 2004; 308: 474-80.
79. Sanchez C, Bergqvist PB, Brennum LT, Gupta S, Hogg S, Larsen A, Wiborg O. Escitalopram, the S-(+)-enantiomer of citalopram, is a selective serotonin reuptake inhibitor with potent effects in animal models predictive of antidepressant and anxiolytic activities. Psychopharmacology 2003; 167: 353-62.
80. Zomkowski AD, Engel D, Gabilan NH, Rodrigues AL. Involvement of NMDA receptors and l-arginine-nitric oxide-cyclic guanosine monophosphate pathway in the antidepressant-like effects of escitalopram in the forced swimming test. Eur Neuropsychopharmacol 2010; 20: 793-801.
81. Uys JD, Muller CJ, Marais L, Harvey BH, Stein DJ, Daniels WM. Early life trauma decreases glucocorticoid receptors in rat dentate gyrus upon adult re-stress: reversal by escitalopram. Neuroscience 2006; 137: 619-25.
82. Bhagya V, Srikumar BN, Raju TR, Shankaranarayana Rao BS. Chronic escitalopram treatment restores spatial learning, monoamine levels, and hippocampal long-term potentiation in an animal model of depression. Psychopharmacology 2010; 214(2), 477-94.
83. Fava M. Diagnosis and definition of treatment-resistant depression. Biol Psychiatry 2003; 53: 649-59.
84. Zhang X, Gainetdinov RR, Beaulieu JM, Sotnikova TD, Burch LH, Williams RB, Schwartz DA, Krishnan KR et al. Loss-of-function mutation in tryptophan hydroxylase-2 identified in unipolar major depression. Neuron 2005; 45: 11-6.
85. Browne CA, Clarke G, Dinan TG, Cryan JF. Differential stress-induced alterations in tryptophan hydroxylase activity and serotonin turnover in two inbred mouse strains. Neuropharmacology 2011; 60: 683-91.
86. Cervo L, Canetta A, Calcagno E, Burbassi S, Sacchetti G, Caccia S, Fracasso C, Albani D et al. Genotype-dependent activity of tryptophan hydroxylase-2 determines the response to citalopram in a mouse model of depression. J Neurosci 2005; 25: 8165-72.
87. Crowley JJ, Blendy JA, Lucki I. Strain-dependent antidepressant-like effects of citalopram in the mouse tail suspension test. Psychopharmacology 2005; 183: 257-64.
88. Jacobsen JP, Nielsen EO, Hummel R, Redrobe JP, Mirza N, Weikop P. Insensitivity of NMRI mice to selective serotonin reuptake inhibitors in the tail suspension test can be reversed by co-treatment with 5-hydroxytryptophan. Psychopharmacology 2008; 199: 137-50.
89. Kobayashi T, Hayashi E, Shimamura M, Kinoshita M, Murphy NP. Neurochemical responses to antidepressants in the prefrontal cortex of mice and their efficacy in preclinical models of anxiety-like and depression-like behavior: a comparative and correlational study. Psychopharmacology 2008; 197: 567-80.
90. Siesser WB, Zhang X, Jacobsen JP, Sotnikova TD, Gainetdinov RR, Caron MG. Tryptophan hydroxylase 2 genotype determines brain serotonin synthesis but not tissue content in C57Bl/6 and BALB/c congenic mice. Neurosci Lett 2010; 481: 6-11.
91. Trkulja V. Is escitalopram really relevantly superior to citalopram in treatment of major depressive disorder? A meta-analysis of head-to-head randomized trials. Croat Med J 2010; 51: 61-73.
92. Borsini F, Podhorna J, Marazziti D. Do animal models of anxiety predict anxiolytic-like effects of antidepressants? Psychopharmacology 2002; 163: 121-41.
93. Kunze WA, Mao YK, Wang B, Huizinga JD, Ma X, Forsythe P, Bienenstock J. Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J Cell Mol Med 2009; 13: 2261-70.
94. Ma X, Mao YK, Wang B, Huizinga JD, Bienenstock J, Kunze W. Lactobacillus reuteri ingestion prevents hyperexcitability of colonic DRG neurons induced by noxious stimuli. Am J Physiol Gastrointest Liver Physiol 2009; 296: G868-75.
95. Wang B, Mao YK, Diorio C, Wang L, Huizinga JD, Bienenstock J, Kunze W. Lactobacillus reuteri ingestion and IK(Ca) channel blockade have similar effects on rat colon motility and myenteric neurones. Neurogastroenterol Motil 2010; 22: 98-107 e133.
96. Tanida M, Yamano T, Maeda K, Okumura N, Fukushima Y, Nagai K. Effects of intraduodenal injection of Lactobacillus johnsonii La1 on renal sympathetic nerve activity and blood pressure in urethane-anesthetized rats. Neurosci Lett 2005; 389: 109-14.
97. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008; 9: 46-56.
98. Ng S, Hart AL, Kamm MA, Stagg AJ, Knight SC. Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis 2009; 15: 300-10.
99. O'Mahony C, Scully P, O'Mahony D, Murphy S, O'Brien F, Lyons A, Sherlock G, MacSharry J et al. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog 2008; 4: e1000112.
100. Lyons A, O'Mahony D, O'Brien F, MacSharry J, Sheil B, Ceddia M, Russell WM, Forsythe P et al. Bacterial strain-specific induction of Foxp3 + T regulatory cells is protective in murine allergy models. Clin Exp Allergy 2010; 40: 811-9.
101. Spiller R. Recent advances in understanding the role of serotonin in gastrointestinal motility in functional bowel disorders: alterations in 5-HT signalling and metabolism in human disease. Neurogastroenterol Motil 2007; 19(Suppl. 2): 25-31.
102. Kondo S, Xiao JZ, Satoh T, Odamaki T, Takahashi S, Sugahara H, Yaeshima T, Iwatsuki K et al. Antiobesity effects of Bifidobacterium breve strain B-3 supplementation in a mouse model with high-fat diet-induced obesity. Biosci Biotechnol Biochem 2010; 74: 1656-61.
103. Foster JA, McVey Neufeld KA. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 2013; 36: 305-12.
104. Moloney RD, Desbonnet L, Clarke G, Dinan TG, Cryan JF. The microbiome: stress, health and disease. Mamm Genome 2014; 25: 49-74.
105. Clarke G, O'Mahony S, Dinan TG, Cryan JF. Priming for health: gut microbiota acquired in early life regulates physiology, brain and behaviour. Acta Paediatr 2014; 103: 812-9. doi:10.1111/apa.12674.