Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress

Neuroscience

Volumn 310, Issue , 2015, Pages 561-577

  Liang, S ^a,b   Wang, T ^a   Hu, X ^a   Luo, J ^c   Li, W ^a,b   Wu, X ^a,b   Duan, Y ^a   Jin, F ^a  

^a INSTITUTE OF PSYCHOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c SICHUAN NORMAL UNIVERSITY   (China)

Author keywords

BDNF; Chronic restraint stress; Depression; Lactobacillus helveticus; Microbiota gut brain axis; Serotonin

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CITALOPRAM; CORTICOSTERONE; CORTICOTROPIN; DOPAMINE; GAMMA INTERFERON; INTERLEUKIN 10; NORADRENALIN; PROBIOTIC AGENT; SEROTONIN; TUMOR NECROSIS FACTOR ALPHA; SEROTONIN UPTAKE INHIBITOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ANXIETY DISORDER; ARTICLE; BDNF GENE; BEHAVIOR DISORDER; BIOCHEMICAL ANALYSIS; BIOCHEMISTRY; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATIONAL STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; DEPRESSION; ELEVATED PLUS MAZE TEST; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPLORATORY BEHAVIOR TEST; GENE EXPRESSION; IMMOBILIZATION STRESS; LACTOBACILLUS HELVETICUS; MALE; NONHUMAN; OBJECT PLACEMENT TEST; OBJECT RECOGNITION TEST; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SUCROSE PREFERENCE TEST; ANIMAL; ANIMAL BEHAVIOR; ANXIETY; BLOOD; BODY WEIGHT; COMPLICATION; DRUG EFFECTS; EXERCISE; HIPPOCAMPUS; MENTAL STRESS; METABOLISM; PREFRONTAL CORTEX; PREVENTION AND CONTROL; SPRAGUE DAWLEY RAT;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BODY WEIGHT; BRAIN-DERIVED NEUROTROPHIC FACTOR; CITALOPRAM; CORTICOSTERONE; DEPRESSION; DOPAMINE; HIPPOCAMPUS; INTERFERON-GAMMA; INTERLEUKIN-10; LACTOBACILLUS HELVETICUS; MALE; NOREPINEPHRINE; PREFRONTAL CORTEX; PROBIOTICS; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; SEROTONIN; SEROTONIN UPTAKE INHIBITORS; STRESS, PSYCHOLOGICAL; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84944050761     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.09.033     Document Type: Article

References (142)

1. Abelaira H.M., Reus G.Z., Quevedo J. Animal models as tools to study the pathophysiology of depression. Rev Bras Psiquiatr 2013, 35(Suppl 2):S112-S120. 10.1590/1516-4446-2013-1098.
2. Ait-Belgnaoui A., Durand H., Cartier C., Chaumaz G., Eutamene H., Ferrier L., Theodorou V. Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology 2012, 37(11):1885-1895. 10.1016/j.psyneuen.2012.03.024.
3. Ait-Belgnaoui A., Colom A., Braniste V., Ramalho L., Marrot A., Cartier C., Tompkins T. Probiotic gut effect prevents the chronic psychological stress-induced brain activity abnormality in mice. Neurogastroenterol Motil 2014, 26(4):510-520. 10.1111/nmo.12295.
4. Al-Asmakh M., Anuar F., Zadjali F., Rafter J., Pettersson S. Gut microbial communities modulating brain development and function. Gut Microbes 2012, 3(4):366-373. 10.4161/gmic.21287.
5. Alexander J.L., Dennerstein L., Woods N.F., McEwen B.S., Halbreich U., Kotz K., Richardson G. Role of stressful life events and menopausal stage in wellbeing and health. Expert Rev Neurother 2007, 7(11).
6. Arseneault-Breard J., Rondeau I., Gilbert K., Girard S.A., Tompkins T.A., 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(12):1793-1799. 10.1017/S0007114511005137.
7. Babri S., Doosti M.H., Salari A.A. Strain-dependent effects of prenatal maternal immune activation on anxiety- and depression-like behaviors in offspring. Brain Behav Immun 2014, 37:164-176. 10.1016/j.bbi.2013.12.003.
8. Bailey M.T. Influence of stressor-induced nervous system activation on the intestinal microbiota and the importance for immunomodulation. Adv Exp Med Biol 2014, 817:255-276. 10.1007/978-1-4939-0897-4_12.
9. Bailey M.T., Coe C.L. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 1999, 35(2):146-155.
10. Bailey M.T., Dowd S.E., Parry N.M.A., Galley J.D., Schauer D.B., Lyte M. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun 2010, 78(4):1509-1519. 10.1128/Iai.00862-09.
11. Bailey M.T., Dowd S.E., Galley J.D., Hufnagle A.R., Allen R.G., Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 2011, 25(3):397-407. 10.1016/j.bbi.2010.10.023.
12. Bangsgaard Bendtsen K.M., Krych L., Sorensen D.B., Pang W., Nielsen D.S., Josefsen K., Hansen A.K. Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. PLoS ONE 2012, 7(10):e46231. 10.1371/journal.pone.0046231.
13. Barden N. Implication of the hypothalamic-pituitary-adrenal axis in the physiopathology of depression. J Psychiatry Neurosci 2004, 29(3):185-193.
14. Barouei J., Adams M.C., Hodgson D.M. Prophylactic role of maternal administration of probiotics in the prevention of irritable bowel syndrome. Med Hypotheses 2009, 73(5):764-767. 10.1016/j.mehy.2009.04.023.
15. Beck K.D., Luine V.N. Sex differences in behavioral and neurochemical profiles after chronic stress role of housing conditions. Physiol Behav 2002, 75:661-673.
16. Bekkering P., Jafri I., van Overveld F.J., Rijkers G.T. The intricate association between gut microbiota and development of type 1, type 2 and type 3 diabetes. Expert Rev Clin Immunol 2013, 9(11):1031-1041. 10.1586/1744666X.2013.848793.
17. Bellani R., Luecken L.J., Conrad C.D. Peripubertal anxiety profile can predict predisposition to spatial memory impairments following chronic stress. Behav Brain Res 2006, 166(2):263-270. 10.1016/j.bbr.2005.08.006.
18. Belmaker R.H., Agam G. Major depression disorder. New Engl J Med 2008, 358(1):55-68.
19. Bercik P., Verdu E.F., Foster J.A., Macri J., Potter M., Huang X.X., Collins S.M. Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous system biochemistry in mice. Gastroenterology 2010, 139(6):U2102-U2409. 10.1053/j.gastro.2010.06.063.
20. Bercik P., Park A.J., Sinclair D., Khoshdel A., Lu J., Huang X., Verdu E.F. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol Motil 2011, 23(12):1132-1139. 10.1111/j.1365-2982.2011.01796.x.
21. Borre Y.E., Moloney R.D., Clarke G., Dinan T.G., Cryan J.F. The impact of microbiota on brain and behavior: mechanisms & therapeutic potential. Adv Exp Med Biol 2014, 817:373-403. 10.1007/978-1-4939-0897-4_17.
22. Borre Y.E., O'Keeffe G.W., Clarke G., Stanton C., Dinan T.G., Cryan J.F. Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med 2014, 20(9):509-518. 10.1016/j.molmed.2014.05.002.
23. Bowman R.E., Beck K.D., Luine V.N. Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Horm Behav 2003, 43(1):48-59. 10.1016/s0018-506x(02)00022-3.
24. Bowman R.E., Maclusky N.J., Diaz S.E., Zrull M.C., Luine V.N. Aged rats: sex differences and responses to chronic stress. Brain Res 2006, 1126:156-166. 10.1016/j.brainres.2006.07.047.
25. Bowman R.E., Micik R., Gautreaux C., Fernandez L., Luine V.N. Sex-dependent changes in anxiety, memory, and monoamines following one week of stress. Physiol Behav 2009, 97(1):21-29. 10.1016/j.physbeh.2009.01.012.
26. Bravo J.A., Forsythe P., Chew M.V., Escaravage E., Savignac H.M., Dinan T.G., Cryan J.F. 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(38):16050-16055. 10.1073/pnas.1102999108.
27. Burcelin R.M., Serino M., Chabo C., Garidou L., Pomie C., Courtney M., et al. Metagenome and metabolism the tissue microbiota hypothesis. Diabetes Obes Metab 2013, 15(3):61-70.
28. Chiba S., Numakawa T., Ninomiya M., Richards M.C., Wakabayashi C., Kunugi H. Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry 2012, 39(1):112-119. 10.1016/j.pnpbp.2012.05.018.
29. Clarke G., Grenham S., Scully P., Fitzgerald P., Moloney R.D., Shanahan F., Cryan J.F. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 2013, 18(6):666-673. 10.1038/mp.2012.77.
30. Cleck J.N., Blendy J.A. Making a bad thing worse: adverse effects of stress on drug addiction. J Clin Invest 2008, 118(2):454-461. 10.1172/JCI33946.
31. Clemente Jose C., Ursell Luke K., Parfrey Laura W., Knight R. The impact of the gut microbiota on human health: an integrative view. Cell 2012, 148(6):1258-1270. 10.1016/j.cell.2012.01.035.
32. Collins S.M., Bercik P. Gut microbiota: intestinal bacteria influence brain activity in healthy humans. Nat Rev Gastroenterol Hepatol 2013, 10(6):326-327. 10.1038/nrgastro.2013.76.
33. Critchfield J.W., van Hemert S., Ash M., Mulder L., Ashwood P. The potential role of probiotics in the management of childhood autism spectrum disorders. Gastroenterol Res Pract 2011, 2011:1-8. 10.1155/2011/161358.
34. Crumeyrolle-Arias M., Jaglin M., Bruneau A., Vancassel S., Cardona A., Dauge V., et al. Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats. Psychoneuroendocrinology 2014, 42:207-217. 10.1016/j.psyneuen.2014.01.014.
35. Cryan J.F., Dinan T.G. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012, 13(10):701-712. 10.1038/nrn3346.
36. Cryan J.F., O'Mahony S.M. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil 2011, 23(3):187-192. 10.1111/j.1365-2982.2010.01664.x.
37. Dalla C., Antoniou K., Drossopoulou G., Xagoraris M., Kokras N., Sfikakis A., Papadopoulou-Daifoti Z. Chronic mild stress impact: are females more vulnerable?. Neuroscience 2005, 135(3):703-714. 10.1016/j.neuroscience.2005.06.068.
38. Dash S., Clarke G., Berk M., Jacka F.N. The gut microbiome and diet in psychiatry: focus on depression. Curr Opin Psychiatry 2015, 28(1):1-6. 10.1097/YCO.0000000000000117.
39. Davari S., Talaei S.A., Alaei H., Salami M. Probiotics treatment improves diabetes-induced impairment of synaptic activity and cognitive function: behavioral and electrophysiological proofs for microbiome-gut-brain axis. Neuroscience 2013, 240:287-296. 10.1016/j.neuroscience.2013.02.055.
40. Desbonnet L., Garrett L., Clarke G., Bienenstock J., Dinan T.G. The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res 2008, 43(2):164-174. 10.1016/j.jpsychires.2008.03.009.
41. Desbonnet L., Garrett L., Clarke G., Kiely B., Cryan J.F., Dinan T.G. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010, 170(4):1179-1188. 10.1016/j.neuroscience.2010.08.005.
42. Desbonnet L., Clarke G., Shanahan F., Dinan T.G., Cryan J.F. Microbiota is essential for social development in the mouse. Mol Psychiatry 2014, 19(2):146-148. 10.1038/mp.2013.65.
43. Di Mauro A., Neu J., Riezzo G., Raimondi F., Martinelli D., Francavilla R., Indrio F. Gastrointestinal function development and microbiota. Ital J Pediatr 2013, 39:15. 10.1186/1824-7288-39-15.
44. Diamond B., Huerta P.T., Tracey K., Volpe B.T. It takes guts to grow a brain increasing evidence of the important role of the intestinal microflora in neuro- and immune-modulatory functions during development and adulthood. BioEssays 2011, 33:588-591. 10.1002/bies.201100042.
45. Dinan T.G., Cryan J.F. Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology 2012, 37(9):1369-1378. 10.1016/j.psyneuen.2012.03.007.
46. Dinan T.G., Stanton C., Cryan J.F. Psychobiotics: a novel class of psychotropic. Biol Psychiatry 2013, 74(10):720-726. 10.1016/j.biopsych.2013.05.001.
47. Distrutti E., O'Reilly J.A., McDonald C., Cipriani S., Renga B., Lynch M.A., Fiorucci S. Modulation of intestinal microbiota by the probiotic VSL#3 resets brain gene expression and ameliorates the age-related deficit in LTP. PLoS ONE 2014, 9(9):e106503. 10.1371/journal.pone.0106503.
48. Duman C.H., Duman R.S. Spine synapse remodeling in the pathophysiology and treatment of depression. Neurosci Lett 2015, 10.1016/j.neulet.2015.01.022.
49. Eloe-Fadrosh E.A., Rasko D.A. The human microbiome: from symbiosis to pathogenesis. Annu Rev Med 2013, 64(1):145-163. 10.1146/annurev-med-010312-133513.
50. Eutamene H., Bueno L. Role of probiotics in correcting abnormalities of colonic flora induced by stress. Gut 2007, 56(11):1495-1497. 10.1136/gut.2007.124040.
51. Evaldson G., Heimdahl A., Kager L., Nord C.E. The normal human anaerobic microflora. Scand J Infect Dis 1982, 9-15.
52. FAO, WHO (2001) Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria.
53. Farmer A.D., Randall H.A., Aziz Q. It's a gut feeling: how the gut microbiota affects the state of mind. J Physiol 2014, 592(Pt 14):2981-2988. 10.1113/jphysiol.2013.270389.
54. Ferraz A.C., Delattre A.M., Almendra R.G., Sonagli M., Borges C., Araujo P., Lima M.M.S. Chronic omega-3 fatty acids supplementation promotes beneficial effects on anxiety, cognitive and depressive-like behaviors in rats subjected to a restraint stress; protocol. Behav Brain Res 2011, 219(1):116-122. 10.1016/j.bbr.2010.12.028.
55. Fond G., Boukouaci W., Chevalier G., Regnault A., Eberl G., Hamdani N., Leboyer M. The "psychomicrobiotic": targeting microbiota in major psychiatric disorders: A systematic review. Pathol Biol (Paris) 2014, 10.1016/j.patbio.2014.10.003.
56. Forsythe P., Sudo N., Dinan T., Taylor V.H., Bienenstock J. Mood and gut feelings. Brain Behav Immun 2010, 24(1):9-16. 10.1016/j.bbi.2009.05.058.
57. Foster J.A. Gut feelings: bacteria and the brain. Cerebrum 2013, 1-14.
58. Freestone P.P.E., Sandrini S.M., Haigh R.D., Lyte M. Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol 2008, 16(2):55-64. 10.1016/j.tim.2007.11.005.
59. Galley J.D., Nelson M.C., Yu Z.T., Dowd S.E., Walter J., Kumar P.S., et al. Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiol 2014, 14. 10.1186/1471-2180-14-189.
60. Gareau M.G., Jury J., MacQueen G., Sherman P.M., Perdue M.H. Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 2007, 56(11):1522-1528. 10.1136/gut.2006.117176.
61. Gareau M.G., Wine E., Rodrigues D.M., Cho J.H., Whary M.T., Philpott D.J., et al. Bacterial infection causes stress-induced memory dysfunction in mice. Gut 2011, 60(3):307-317. 10.1136/gut.2009.202515.
62. Glavin G.B., Pare W.P., Sandbak T., Bakke H.K., Murison R. Restraint stress in biomedical-research - an update. Neurosci Biobehav Rev 1994, 18(2):223-249. 10.1016/0149-7634(94)90027-2.
63. Goehler L.E., Park S.M., Opitz N., Lyte M., Gaykema R.P.A. Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior. Brain Behav Immun 2008, 22(3):354-366. 10.1016/j.bbi.2007.08.009.
64. Gold P.W. The organization of the stress system and its dysregulation in depressive illness. Mol Psychiatry 2014, 10.1038/mp.2014.163.
65. Grenham S., Clarke G., Cryan J.F., Dinan T.G. Brain-gut-microbe communication in health and disease. Front Physiol 2011, 2:94. 10.3389/fphys.2011.00094.
66. Hammen C. Stress and depression. Annu Rev Clin Psychol 2005, 1:293-319. 10.1146/annurev.clinpsy.1.102803.143938.
67. Hamon M., Blier P. Monoamine neurocircuitry in depression and strategies for new treatments. Prog Neuropsychopharmacol Biol Psychiatry 2013, 45:54-63. 10.1016/j.pnpbp.2013.04.009.
68. Holdeman L.V., Good I.J., Moore W.E. Human fecal flora variation in bacterial composition within individuals and a possible effect of emotional stress. Appl Environ Microbiol 1976, 31(3):359-375.
69. Hörmannsperger G., Haller D. Molecular crosstalk of probiotic bacteria with the intestinal immune system: clinical relevance in the context of inflammatory bowel disease. Int J Med Microbiol 2010, 300(1):63-73. 10.1016/j.ijmm.2009.08.006.
70. Hsiao E.Y., McBride S.W., Hsien S., Sharon G., Hyde E.R., McCue T., Mazmanian S.K. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013, 155(7):1451-1463. 10.1016/j.cell.2013.11.024.
71. Human Microbiome Project, C A framework for human microbiome research. Nature 2012, 486(7402):215-221. 10.1038/nature11209.
72. Human Microbiome Project, C Structure, function and diversity of the healthy human microbiome. Nature 2012, 486(7402):207-214. 10.1038/nature11234.
73. Huynh T.N., Krigbaum A.M., Hanna J.J., Conrad C.D. Sex differences and phase of light cycle modify chronic stress effects on anxiety and depressive-like behavior. Behav Brain Res 2011, 222(1):212-222. 10.1016/j.bbr.2011.03.038.
74. Hyttel J. Citalopram - pharmacological profile of a specific serotonin uptake inhibitor with antidepressant activity. Prog Neuropsychopharmacol Biol Psychiatry 1982, 6(3):277-295.
75. Kantak P.A., Bobrow D.N., Nyby J.G. Obsessive-compulsive-like behaviors in house mice are attenuated by a probiotic (Lactobacillus rhamnosus GG). Behav Pharmacol 2014, 25(1):71-79. 10.1097/FBP.0000000000000013.
76. Kaur I.P., Kuhad A., Garg A., Chopra K. Probiotics: delineation of prophylactic and therapeutic benefits. J Med Food 2009, 12(2):219-235. 10.1089/jmf.2007.0544.
77. Kessler R.C. The effects of stressful life events on depression. Annu Rev Psychol 1997, 48:191-214. 10.1146/annurev.psych.48.1.191.
78. Le Floc'h N., Otten W., Merlot E. Tryptophan metabolism, from nutrition to potential therapeutic applications. Amino Acids 2011, 41(5):1195-1205. 10.1007/s00726-010-0752-7.
79. Ljungh A., Wadström T. Lactic acid bacteria as probiotics. Curr Issues Intest Microbiol 2006, 7(2):73-89.
80. Logan A.C., Katzman M. Major depressive disorder: probiotics may be an adjuvant therapy. Med Hypotheses 2005, 64(3):533-538. 10.1016/j.mehy.2004.08.019.
81. Lu B., Nagappan G., Lu Y. BDNF and synaptic plasticity, cognitive function, and dysfunction. Handb Exp Pharmacol 2014, 220:223-250. 10.1007/978-3-642-45106-5_9.
82. Luine V. Recognition memory tasks in neuroendocrine research. Behav Brain Res 2015, 285:158-164. 10.1016/j.bbr.2014.04.032.
83. Luo J., Wang T., Liang S., Hu X., Li W., Jin F. Ingestion of Lactobacillus strain reduces anxiety and improves cognitive function in the hyperammonemia rat. Sci China Life Sci 2014, 57(3):327-335. 10.1007/s11427-014-4615-4.
84. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 2009, 10(6):434-445. 10.1038/nrn2639.
85. Lyte M. The microbial organ in the gut as a driver of homeostasis and disease. Med Hypotheses 2010, 74(4):634-638. 10.1016/j.mehy.2009.10.025.
86. Lyte M., Li W., Opitz N., Gaykema R.P., Goehler L.E. Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia Citrobacter rodentium. Physiol Behav 2006, 89(3):350-357. 10.1016/j.physbeh.2006.06.019.
87. Maes M., Leonard B.E., Myint A.M., Kubera M., Verkerk R. The new '5-HT' hypothesis of depression: cell-mediated immune activation induces indoleamine 2,3-dioxygenase, which leads to lower plasma tryptophan and an increased synthesis of detrimental tryptophan catabolites (TRYCATs), both of which contribute to the onset of depression. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35(3):702-721. 10.1016/j.pnpbp.2010.12.017.
88. Mahar I., Bambico F.R., Mechawar N., Nobrega J.N. Stress, serotonin, and hippocampal neurogenesis in relation to depression and antidepressant effects. Neurosci Biobehav Rev 2014, 38:173-192. 10.1016/j.neubiorev.2013.11.009.
89. Malaguarnera M., Greco F., Barone G., Gargante M.P., Malaguarnera M., Toscano M.A. Bifidobacterium longum with fructo-oligosaccharide (FOS) treatment in minimal hepatic encephalopathy: a randomized, double-blind, placebo-controlled study. Dig Dis Sci 2007, 52(11):3259-3265. 10.1007/s10620-006-9687-y.
90. Malkesman O., Austin D.R., Tragon T., Henter I.D., Reed J.C., Pellecchia M., et al. Targeting the BH3-interacting domain death agonist to develop mechanistically unique antidepressants. Mol Psychiatry 2012, 17(8):770-780. 10.1038/mp.2011.77.
91. Manco M. Gut microbiota and developmental programming of the brain: from evidence in behavioral endophenotypes to novel perspective in obesity. Front Cell Infect Microbiol 2012, 2:109. 10.3389/fcimb.2012.00109.
92. Marcondes F.K., Miguel K.J., Melo L.L., Spadari-Bratfisch R.C. Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol Behav 2001, 74:435-440.
93. Marije aan het Rot M., Mathew S.J., Charney D.S. Neurobiological mechanisms in major depressive disorder. CMAJ 2009, 180(3):305-313. 10.1503/cmaj.080697.
94. Marin M.F., Lord C., Andrews J., Juster R.P., Sindi S., Arsenault-Lapierre G., Lupien S.J. Chronic stress, cognitive functioning and mental health. Neurobiol Learn Mem 2011, 96(4):583-595. 10.1016/j.nlm.2011.02.016.
95. McArthur R., Borsini F. Animal models of depression in drug discovery: a historical perspective. Pharmacol Biochem Behav 2006, 84(3):436-452. 10.1016/j.pbb.2006.06.005.
96. McLaughlin K.J., Gomez J.L., Baran S.E., Conrad C.D. The effects of chronic stress on hippocampal morphology and function: An evaluation of chronic restraint paradigms. Brain Res 2007, 1161:56-64. 10.1016/j.brainres.2007.05.042.
97. Mehrpouya S., Nahavandi A., Khojasteh F., Soleimani M., Ahmadi M., Barati M. Iron administration prevents BDNF decrease and depressive-like behavior following chronic stress. Brain Res 2014, 10.1016/j.brainres.2014.10.057.
98. Messaoudi M., Lalonde R., Violle N., Javelot H., Desor D., Nejdi A., Cazaubiel J.M. 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(5):755-764. 10.1017/S0007114510004319.
99. Moloney R.D., Desbonnet L., Clarke G., Dinan T.G., Cryan J.F. The microbiome: stress, health and disease. Mamm Genome 2014, 25(1-2):49-74. 10.1007/s00335-013-9488-5.
100. Montiel-Castro A.J., Gonzalez-Cervantes R.M., Bravo-Ruiseco G., Pacheco-Lopez G. The microbiota-gut-brain axis: neurobehavioral correlates, health and sociality. Front Integr Neurosci 2013, 7:70. 10.3389/fnint.2013.00070.
101. Morgan X.C., Segata N., Huttenhower C. Biodiversity and functional genomics in the human microbiome. Trends Genet 2013, 29(1):51-58. 10.1016/j.tig.2012.09.005.
102. Naert G., Ixart G., Maurice T., Tapia-Arancibia L., Givalois L. Brain-derived neurotrophic factor and hypothalamic-pituitary-adrenal axis adaptation processes in a depressive-like state induced by chronic restraint stress. Mol Cell Neurosci 2011, 46(1):55-66. 10.1016/j.mcn.2010.08.006.
103. Nicholson J.K., Holmes E., Kinross J., Burcelin R., Gibson G., Jia W., Pettersson S. Host-gut microbiota metabolic interactions. Science 2012, 336(6086):1262-1267. 10.1126/science.1223813.
104. O'Mahony L., McCarthy J., Kelly P., Hurley G., Luo F., Chen K., et al. Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 2005, 128(3):541-551. 10.1053/j.gastro.2004.11.050.
105. Ochoa-Reparaz J., Mielcarz D.W., Ditrio L.E., Burroughs A.R., Begum-Haque S., Dasgupta S., et al. Central nervous system demyelinating disease protection by the human commensal Bacteroides fragilis depends on polysaccharide A expression. J Immunol 2010, 185(7):4101-4108. 10.4049/jimmunol.1001443.
106. Ochoa-Reparaz J., Mielcarz D.W., Wang Y., Begum-Haque S., Dasgupta S., Kasper D.L., Kasper L.H. A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease. Mucosal Immunol 2010, 3(5):487-495. 10.1038/mi.2010.29.
107. Ogbonnaya E.S., Clarke G., Shanahan F., Dinan T.G., Cryan J.F., O'Leary O.F. Adult hippocampal neurogenesis is regulated by the microbiome. Biol Psychiatry 2015, 10.1016/j.biopsych.2014.12.023.
108. Ohland C.L., Kish L., Bell H., Thiesen A., Hotte N., Pankiv E., Madsen K.L. Effects of Lactobacillus helveticus on murine behavior are dependent on diet and genotype and correlate with alterations in the gut microbiome. Psychoneuroendocrinology 2013, 38(9):1738-1747. 10.1016/j.psyneuen.2013.02.008.
109. Ohsawa K., Uchida N., Ohki K., Nakamura Y., Yokogoshi H. Lactobacillus helveticus-fermented milk improves learning and memory in mice. Nutr Neurosci 2015, 18(5):232-240. 10.1179/1476830514Y.0000000122.
110. O'Mahony S.M., Marchesi J.R., Scully P., Codling C., Ceolho A.M., Quigley E.M., et al. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 2009, 65(3):263-267. 10.1016/j.biopsych.2008.06.026.
111. O'Mahony C.M., Clarke G., Gibney S., Dinan T.G., Cryan J.F. Strain differences in the neurochemical response to chronic restraint stress in the rat: relevance to depression. Pharmacol Biochem Behav 2011, 97(4):690-699. 10.1016/j.pbb.2010.11.012.
112. O'Mahony S.M., Clarke G., Borre Y.E., Dinan T.G., Cryan J.F. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res 2014, 10.1016/j.bbr.2014.07.027.
113. Park A.J., Collins J., Blennerhassett P.A., Ghia J.E., Verdu E.F., Bercik P., Collins S.M. Altered colonic function and microbiota profile in a mouse model of chronic depression. Neurogastroenterol Motil 2013, 25(9):e733-e775. 10.1111/nmo.12153.
114. Quigley E.M., Shanahan F. The future of probiotics for disorders of the brain-gut axis. Adv Exp Med Biol 2014, 817:417-432. 10.1007/978-1-4939-0897-4_19.
115. Radahmadi M., Alaei H., Sharifi M.R., Hosseini N. Effects of different timing of stress on corticosterone, BDNF and memory in male rats. Physiol Behav 2015, 139:459-467. 10.1016/j.physbeh.2014.12.004.
116. Rao A.V., Bested A.C., Beaulne T.M., Katzman M.A., Iorio C., Berardi J.M., Logan A.C. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathogens 2009, 1(1):6. 10.1186/1757-4749-1-6.
117. Rhee S.H., Pothoulakis C., Mayer E.A. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol 2009, 6(5):306-314. 10.1038/nrgastro.2009.35.
118. Rook G.A.W., Lowry C.A. The hygiene hypothesis and psychiatric disorders. Trends Immunol 2008, 29(4):150-158. 10.1016/J.It.2008.01.002.
119. Rook G.A.W., Raison C.L., Lowry C.A. Can we vaccinate against depression?. Drug Discovery Today 2012, 17(9-10):451-458. 10.1016/j.drudis.2012.03.018.
120. Rook G.A., Raison C.L., Lowry C.A. Microbiota, immunoregulatory old friends and psychiatric disorders. Adv Exp Med Biol 2014, 817:319-356. 10.1007/978-1-4939-0897-4_15.
121. Russo F., Linsalata M., Orlando A. Probiotics against neoplastic transformation of gastric mucosa: effects on cell proliferation and polyamine metabolism. World J Gastroenterol 2014, 20(37):13258-13272. 10.3748/wjg.v20.i37.13258.
122. Saulnier D.M., Ringel Y., Heyman M.B., Foster J.A., Bercik P., Shulman R.J., et al. The intestinal microbiome, probiotics and prebiotics in neurogastroenterology. Gut Microbes 2013, 4(1):17-27. 10.4161/gmic.22973.
123. Savignac H.M., Kiely B., Dinan T.G., Cryan J.F. Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice. Neurogastroenterol Motil 2014, 26(11):1615-1627. 10.1111/nmo.12427.
124. Savignac H.M., Tramullas M., Kiely B., Dinan T.G., Cryan J.F. Bifidobacteria modulate cognitive processes in an anxious mouse strain. Behav Brain Res 2015, 287:59-72. 10.1016/j.bbr.2015.02.044.
125. Sayin A., Derinoz O., Yuksel N., Sahin S., Bolay H. The effects of the estrus cycle and citalopram on anxiety-like behaviors and c-fos expression in rats. Pharmacol Biochem Behav 2014, 124:180-187. 10.1016/j.pbb.2014.06.002.
126. Schiepers O.J., Wichers M.C., Maes M. Cytokines and major depression. Prog Neuropsychopharmacol Biol Psychiatry 2005, 29(2):201-217. 10.1016/j.pnpbp.2004.11.003.
127. Severance E.G., Gressitt K.L., Stallings C.R., Origoni A.E., Khushalani S., Leweke F.M., et al. Discordant patterns of bacterial translocation markers and implications for innate immune imbalances in schizophrenia. Schizophr Res 2013, 148(1-3):130-137. 10.1016/j.schres.2013.05.018.
128. Sudo N. Microbiome, HPA axis and production of endocrine hormones in the gut. Adv Exp Med Biol 2014, 817:177-194. 10.1007/978-1-4939-0897-4_8.
129. Sudo N., Chida Y., Kubo C. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Psychosom Res 2005, 58(6):S60.
130. Sullivan A., Nord C.E., Evengard B. Effect of supplement with lactic-acid producing bacteria on fatigue and physical activity in patients with chronic fatigue syndrome. Nutr J 2009, 8. 10.1186/1475-2891-8-4.
131. Swaab D.F., Bao A.M., Lucassen P.J. The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev 2005, 4(2):141-194. 10.1016/j.arr.2005.03.003.
132. Takuma K., Hoshina Y., Arai S., Himeno Y., Matsuo A., Funatsu Y., Yamada K. Ginkgo biloba extract EGb 761 attenuates hippocampal neuronal loss and cognitive dysfunction resulting from chronic restraint stress in ovariectomized rats. Neuroscience 2007, 149(2):256-262. 10.1016/j.neuroscience.2007.07.042.
133. Tannock G.W., Savage D.C. Influences of dietary and environmental stress on microbial-populations in murine gastrointestinal-tract. Infect Immun 1974, 9(3):591-598.
134. Tillisch K. The effects of gut microbiota on CNS function in humans. Gut Microbes 2014, 5(3):404-410. 10.4161/gmic.29232.
135. Tillisch K., Labus J., Kilpatrick L., Jiang Z., Stains J., Ebrat B., Mayer E.A. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 2013, 144(7):1394-1401. 1401 e1391-1394. 10.1053/j.gastro.2013.02.043.
136. Vaidya V.A., Fernandes K., Jha S. Regulation of adult hippocampal neurogenesis: relevance to depression. Expert Rev Neurother 2007, 7(7):853-864.
137. Voorhees J.L., Tarr A.J., Wohleb E.S., Godbout J.P., Mo X.K., Sheridan J.F., et al. Prolonged restraint stress increases IL-6, reduces IL-10, and causes persistent depressive-like behavior that is reversed by recombinant IL-10. PLoS ONE 2013, 8(3). 10.1371/journal.pone.0058488.
138. Vyas U., Ranganathan N. Probiotics, prebiotics, and synbiotics: gut and beyond. Gastroenterol Res Pract 2012, 2012:872716. 10.1155/2012/872716.
139. Wang Y., Kasper L.H. The role of microbiome in central nervous system disorders. Brain Behav Immun 2014, 38:1-12. 10.1016/j.bbi.2013.12.015.
140. Wang Z., Klipfell E., Bennett B.J., Koeth R., Levison B.S., DuGar B., et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011, 472(7341):57-63. 10.1038/nature09922.
141. Wichers M., Maes M. The psychoneuroimmuno-pathophysiology of cytokine-induced depression in humans. Int J Neuropsychopharmacol 2002, 5(4):375-388. 10.1017/S1461145702003103.
142. Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez-Bello M.G., Contreras M., Gordon J.I. Human gut microbiome viewed across age and geography. Nature 2012, 486(7402):222-227. 10.1038/nature11053.