Antidepressant-like activities of live and heat-killed Lactobacillus paracasei PS23 in chronic corticosterone-treated mice and possible mechanisms

Brain Research

Volumn 1711, Issue , 2019, Pages 202-213

  Wei, Chia Li ^a   Wang, Sabrina ^b   Yen, Jui Ting ^b   Cheng, Yun Fang ^c   Liao, Chia Li ^b   Hsu, Chih Chieh ^c   Wu, Chien Chen ^c   Tsai, Ying Chieh ^b  

^a NATIONAL CHIAYI UNIVERSITY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c Bened Biomedicals Co   (Taiwan)

Author keywords

Corticosterone; Depression; Fluoxetine; Gut brain axis; Mice; Psychobiotics

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; DOPAMINE; FLUOXETINE; GLUCOCORTICOID RECEPTOR; MINERALOCORTICOID RECEPTOR; PROBIOTIC AGENT; SEROTONIN; ANTIDEPRESSANT AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ANXIETY; ARTICLE; BEHAVIOR CHANGE; BODY WEIGHT; BRAIN TISSUE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; CORPUS STRIATUM; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DOPAMINE BRAIN LEVEL; FORCED SWIM TEST; HIPPOCAMPUS; INTESTINE FLORA; LACTOBACILLUS PARACASEI; LOCOMOTION; MALE; MOUSE; NONHUMAN; OPEN FIELD TEST; PREFRONTAL CORTEX; PRIORITY JOURNAL; SEROTONIN BRAIN LEVEL; SUCROSE PREFERENCE TEST; TOTAL DISTANCE TRAVELED; TRANQUILIZING ACTIVITY; ANIMAL; ANIMAL BEHAVIOR; ANXIETY DISORDER; BLOOD; BRAIN; C57BL MOUSE; DISEASE MODEL; DRUG EFFECT; MENTAL STRESS; METABOLISM;

ANIMALS; ANTIDEPRESSIVE AGENTS; ANXIETY; ANXIETY DISORDERS; BEHAVIOR, ANIMAL; BRAIN; CORTICOSTERONE; DEPRESSION; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; FLUOXETINE; HIPPOCAMPUS; LACTOBACILLUS PARACASEI; MALE; MICE; MICE, INBRED C57BL; PREFRONTAL CORTEX; PROBIOTICS; RECEPTORS, GLUCOCORTICOID; STRESS, PSYCHOLOGICAL;

EID: 85060849210     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2019.01.025     Document Type: Article

References (99)

1. Adams, C.A., The probiotic paradox: live and dead cells are biological response modifiers. Nutr. Res. Rev. 23 (2010), 37–46.
2. Agusti, A., Moya-Pérez, A., Campillo, I., Montserrat-de la Paz, S., Cerrudo, V., Perez-Villalba, A., Sanz, Y., Bifidobacterium pseudocatenulatum CECT 7765 ameliorates neuroendocrine alterations associated with an exaggerated stress response and anhedonia in obese mice. Mol. Neurobiol. 55 (2018), 5337–5352.
3. Ait-Belgnaoui, A., Durand, H., Cartier, C., Chaumaz, G., Eutamene, H., Ferrier, L., Houdeau, E., Fioramonti, J., Bueno, L., Theodorou, V., Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology 37 (2012), 1885–1895.
4. Ait-Belgnaoui, A., Colom, A., Braniste, V., Ramalho, L., Marrot, A., Cartier, C., Houdeau, E., Theodorou, V., Tompkins, T., Probiotic gut effect prevents the chronic psychological stress-induced brain activity abnormality in mice. Neurogastroenterol. Motil. 26 (2014), 510–520.
5. Allen, A.P., Hutch, W., Borre, Y.E., Kennedy, P.J., Temko, A., Boylan, G., Murphy, E., Cryan, J.F., Dinan, T.G., Clarke, G., Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers. Transl. Psychiatry, 6, 2016, e939.
6. Andersson, H., Tullberg, C., Ahrné S., Hamberg, K., Lazou Ahrén, I., Molin, G., Sonesson, M., Håkansson, Å., Oral administration of Lactobacillus plantarum 299v reduces cortisol levels in human saliva during examination induced stress: a randomized, Double-Blind Controlled Trial. Int. J. Microbiol., 2016, 2016, 8469018.
7. American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders (DSM-5). 2013, American Psychiatric Association, Washington, DC.
8. 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. 25 (2011), 397–407.
9. Barouei, J., Moussavi, M., Hodgson, D.M., Effect of maternal probiotic intervention on HPA axis, immunity and gut microbiota in a rat model of irritable bowel syndrome. PLoS One, 7, 2012, e46051.
10. Benton, D., Williams, C., Brown, A., Impact of consuming a milk drink containing a probiotic on mood and cognition. Eur. J. Clin. Nutr. 61 (2007), 355–361.
11. Berton, O., Nestler, E.J., New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 7 (2006), 137–151.
12. Bharwani, A., Mian, M.F., Surette, M.G., Bienenstock, J., Forsythe, P., Oral treatment with Lactobacillus rhamnosus attenuates behavioural deficits and immune changes in chronic social stress. BMC Med., 15, 2017, 7.
13. Blier, P., Pharmacology of rapid-onset antidepressant treatment strategies. J. Clin. Psychiatry 62:Suppl. 15 (2001), 12–17.
14. 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. 817 (2014), 373–403.
15. Brambilla, P., Cipriani, A., Hotopf, M., Barbui, C., Side-effect profile of fluoxetine in comparison with other SSRIs, tricyclic and newer antidepressants: a meta-analysis of clinical trial data. Pharmacopsychiatry 38 (2005), 69–77.
16. Bravo, J.A., Forsythe, P., Chew, M.V., Escaravage, E., Savignac, H.M., Dinan, T.G., Bienenstock, J., 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. 108 (2011), 16050–16055.
17. Burke, H.M., Davis, M.C., Otte, C., Mohr, D.C., Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology 30 (2005), 846–856.
18. Burokas, A., Arboleya, S., Moloney, R.D., Peterson, V.L., Murphy, K., Clarke, G., Stanton, C., Dinan, T.G., Cryan, J.F., Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol. Psychiatry 82 (2017), 472–487.
19. Castro, S.L., Zigmond, M.J., Stress-induced increase in extracellular dopamine in striatum: Role of glutamatergic action via N-methyl-d-aspartate receptors in substantia nigra. Brain Res. 901 (2001), 47–54.
20. Caudal, D., Jay, T.M., Godsil, B.P., Behavioral stress induces regionally-distinct shifts of brain mineralocorticoid and glucocorticoid receptor levels. Front. Behav. Neurosci., 8, 2014, 19.
21. Chaouloff, F., Berton, O., Mormede, P., Serotonin and stress. Neuropsychopharmacology 21 (1999), 28S–32S.
22. Checkley, S., The neuroendocrinology of depression and chronic stress. Br. Med. Bull. 52 (1996), 597–617.
23. Conway-Campbell, B.L., McKenna, M.A., Wiles, C.C., Atkinson, H.C., de Kloet, E.R., Lightman, S.L., Proteasome-dependent down-regulation of activated nuclear hippocampal glucocorticoid receptors determines dynamic responses to corticosterone. Endocrinology 148 (2007), 5470–5477.
24. Coplan, J.D., Gopinath, S., Abdallah, C.G., Berry, B., A neurobiological hypothesis of treatment-resistant depression – mechanisms for selective serotonin reuptake inhibitor non-efficacy. Front. Behav. Neurosci., 8, 2014, 189.
25. Crupi, R., Mazzon, E., Marino, A., La Spada, G., Bramanti, P., Cuzzocrea, S., Spina, E., Melatonin treatment mimics the antidepressant action in chronic corticosterone-treated mice. J. Pineal Res. 49 (2010), 123–129.
26. Cussotto, S., Strain, C.R., Fouhy, F., Strain, R.G., Peterson, V.L., Clarke, G., Stanton, C., Dinan, T.G., Cryan, J.F., Differential effects of psychotropic drugs on microbiome composition and gastrointestinal function. Psychopharmacology, 2018.
27. Dang, H., Chen, Y., Liu, X., Wang, Q., Wang, L., Jia, W., Wang, Y., Antidepressant effects of ginseng total saponins in the forced swimming test and chronic mild stress models of depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 33 (2009), 1417–1424.
28. David, D.J., Samuels, B.A., Rainer, Q., Wang, J.-W., Marsteller, D., Mendez, I., Drew, M., Craig, D.A., Guiard, B.P., Guilloux, J.-P., Artymyshyn, R.P., Gardier, A.M., Gerald, C., Antonijevic, I.A., Leonardo, E.D., Hen, R., Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62 (2009), 479–493.
29. de Kloet, E.R., Joëls, M., Holsboer, F., Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6 (2005), 463–475.
30. de Wouw, M., Boehme, M., Lyte, J.M., Wiley, N., Strain, C., O'Sullivan, O., Clarke, G., Stanton, C., Dinan, T.G., Cryan, J.F., Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain–gut axis alterations. J. Physiol. 596 (2018), 4923–4944.
31. Demuyser, T., Bentea, E., Deneyer, L., Albertini, G., Massie, A., Smolders, I., Disruption of the HPA-axis through corticosterone-release pellets induces robust depressive-like behavior and reduced BDNF levels in mice. Neurosci. Lett. 626 (2016), 119–125.
32. 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. 43 (2009), 164–174.
33. Deshpande, G., Athalye-Jape, G., Patole, S., Para-probiotics for preterm neonates-the next frontier. Nutrients, 2018, 10.
34. Dinan, T.G., Stanton, C., Cryan, J.F., Psychobiotics: a novel class of psychotropic. Biol. Psychiatry 74 (2013), 720–726.
35. Dinan, T.G., Stilling, R.M., Stanton, C., Cryan, J.F., Collective unconscious: how gut microbes shape human behavior. J. Psychiatr. Res. 63 (2015), 1–9.
36. Ding, H., Cui, X.-Y., Cui, S.-Y., Ye, H., Hu, X., Zhao, H.-L., Liu, Y.-T., Zhang, Y.-H., Depression-like behaviors induced by chronic corticosterone exposure via drinking water: time-course analysis. Neurosci. Lett. 687 (2018), 202–206.
37. Duman, R.S., Monteggia, L.M., A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 59 (2006), 1116–1127.
38. Dunphy-Doherty, F., O'Mahony, S.M., Peterson, V.L., O'Sullivan, O., Crispie, F., Cotter, P.D., Wigmore, P., King, M.V., Cryan, J.F., Fone, K.C.F., Post-weaning social isolation of rats leads to long-term disruption of the gut microbiota-immune-brain axis. Brain Behav. Immun. 68 (2018), 261–273.
39. Farzi, A., Fröhlich, E.E., Holzer, P., Gut microbiota and the neuroendocrine system. Neurotherapeutics 15 (2018), 5–22.
40. Ferguson, J.M., SSRI antidepressant medications: adverse effects and tolerability. Prim. Care Companion J. Clin. Psychiatry 3 (2001), 22–27.
41. Ferrari, A.J., Charlson, F.J., Norman, R.E., Patten, S.B., Freedman, G., Murray, C.J., Vos, T., Whiteford, H.A., Burden of depressive disorders by country, sex, age, and year: findings from the Global Burden of Disease Study 2010. PLOS Med., 10, 2013, e1001547.
42. Flowers, S.A., Evans, S.J., Ward, K.M., McInnis, M.G., Ellingrod, V.L., Interaction between atypical antipsychotics and the gut microbiome in a bipolar disease cohort. Pharmacotherapy 37 (2017), 261–267.
43. Freitas, A., Egea, J., Buendia, I., Gómez-Rangel, V., Parada, E., Navarro, E., Casas, A., Wojnicz, A., Ortiz, J., Cuadrado, A., Ruiz-Nuño, A., Rodrigues, A., Lopez, M., Agmatine, by improving neuroplasticity markers and inducing Nrf2, prevents corticosterone-induced depressive-like behavior in mice. Mol. Neurobiol. 53 (2016), 3030–3045.
44. Galland, L., The gut microbiome and the brain. J. Med. Food 17 (2014), 1261–1272.
45. Galley, J.D., Mackos, A.R., Varaljay, V.A., Bailey, M.T., Stressor exposure has prolonged effects on colonic microbial community structure in Citrobacter rodentium-challenged mice. Sci. Rep., 7, 2017, 45012.
46. Hao, C.-W., Lai, W.-S., Ho, C.-T., Sheen, L.-Y., Antidepressant-like effect of lemon essential oil is through a modulation in the levels of norepinephrine, dopamine, and serotonin in mice: use of the tail suspension test. J. Funct. Food. 5 (2013), 370–379.
47. Hecimovic, H., Neurobiological aspects of depression: How do they affect neurologic disorders?. Kanner, A.M., (eds.) Depression in Neurologic Disorders: Diagnosis and Management, 2012, Wiley-Blackwell Inc, Oxford, UK, 10–27.
48. Herman, J.P., Cullinan, W.E., Neurocircuitry of stress: central control of the hypothalamo–pituitary–adrenocortical axis. Trends Neurosci. 20 (1997), 78–84.
49. Hodes, G.E., Brookshire, B.R., Hill-Smith, T.E., Teegarden, S.L., Berton, O., Lucki, I., Strain differences in the effects of chronic corticosterone exposure in the hippocampus. Neuroscience 222 (2012), 269–280.
50. Huang, S.-Y., Chen, L.-H., Wang, M.-F., Hsu, C.-C., Chan, C.-H., Li, J.-X., Huang, H.-Y., Lactobacillus paracasei PS23 delays progression of age-related cognitive decline in senescence accelerated mouse prone 8 (SAMP8) mice. Nutrients, 10, 2018, 894.
51. Johnson, S.A., Fournier, N.M., Kalynchuk, L.E., Effect of different doses of corticosterone on depression-like behavior and HPA axis responses to a novel stressor. Behav. Brain Res. 168 (2006), 280–288.
52. Joëls, M., Sarabdjitsingh, R.A., Karst, H., Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes. Pharmacol. Rev. 64 (2012), 901–938.
53. Juruena, M.F., Cleare, A.J., Pariante, C.M., The hypothalamic pituitary adrenal axis, glucocorticoid receptor function and relevance to depression. Braz. J. Psychiatry 26 (2004), 189–201.
54. Karten, Y.J.G., Nair, S.M., van Essen, L., Sibug, R., Joëls, M., Long-term exposure to high corticosterone levels attenuates serotonin responses in rat hippocampal CA1 neurons. Proc. Natl. Acad. Sci. U.S.A. 96 (1999), 13456–13461.
55. Kinlein, S.A., Wilson, C.D., Karatsoreos, I.N., Dysregulated hypothalamic-pituitary-adrenal axis function contributes to altered endocrine and neurobehavioral responses to acute stress. Front. Psychiatry, 6, 2015, 31.
56. Kott, J.M., Mooney-Leber, S.M., Shoubah, F.A., Brummelte, S., Effectiveness of different corticosterone administration methods to elevate corticosterone serum levels, induce depressive-like behavior, and affect neurogenesis levels in female rats. Neuroscience 312 (2016), 201–214.
57. Krishnan, V., Nestler, E.J., The molecular neurobiology of depression. Nature 455 (2008), 894–902.
58. Kutiyanawalla, A., Terry, A.V. Jr., Pillai, A., Cysteamine attenuates the decreases in TrkB protein levels and the anxiety/depression-like behaviors in mice induced by corticosterone treatment. PloS One, 6, 2011, e26153.
59. 1a , glucocorticoid, and mineralocorticoid receptor in rat and human hippocampus: implications for the neurobiology of depression. Biol. Psychiatry 43 (1998), 547–573.
60. Lai, M., McCormick, J.A., Chapman, K.E., Kelly, P.A.T., Seckl, J.R., Yau, J.L.W., Differential regulation of corticosteroid receptors by monoamine neurotransmitters and antidepressant drugs in primary hippocampal culture. Neuroscience 118 (2003), 975–984.
61. Lee, B., Sur, B., Shim, I., Lee, H., Hahm, D.-H., Angelica gigas ameliorate depression-like symptoms in rats following chronic corticosterone injection. BMC Complement. Altern. Med., 15, 2015, 210.
62. Leitch, M.M., Ingram, C.D., Young, A.H., McQuade, R., Gartside, S.E., Flattening the corticosterone rhythm attenuates 5-HT1A autoreceptor function in the rat: Relevance for depression. Neuropsychopharmacology 28 (2003), 119–125.
63. Liao, J.-F., Hsu, J.-J., Chou, G.-T., Hsu, J.-S., Liong, M.-T., Tsai, Y.-C., in press. Lactobacillus paracasei PS23 reduced early-life stress abnormalities in maternal separation mouse model. Benef. Microbes.
64. Liu, W.-H., Chuang, H.-L., Huang, Y.-T., Wu, C.-C., Chou, G.-T., Wang, S., Tsai, Y.-C., Alteration of behavior and monoamine levels attributable to Lactobacillus plantarum PS128 in germ-free mice. Behav. Brain Res. 298:Part B (2016), 202–209.
65. Liu, Y.-W., Liu, W.-H., Wu, C.-C., Juan, Y.-C., Wu, Y.-C., Tsai, H.-P., Wang, S., Tsai, Y.-C., Psychotropic effects of Lactobacillus plantarum PS128 in early life-stressed and naïve adult mice. Brain Res. 1631 (2016), 1–12.
66. Maier, L., Pruteanu, M., Kuhn, M., Zeller, G., Telzerow, A., Anderson, E.E., Brochado, A.R., Fernandez, K.C., Dose, H., Mori, H., Patil, K.R., Bork, P., Typas, A., Extensive impact of non-antibiotic drugs on human gut bacteria. Nature, 555, 2018, 623.
67. Marin, I.A., Goertz, J.E., Ren, T., Rich, S.S., Onengut-Gumuscu, S., Farber, E., Wu, M., Overall, C.C., Kipnis, J., Gaultier, A., Microbiota alteration is associated with the development of stress-induced despair behavior. Sci. Rep., 7, 2017, 43859.
68. Meltzer, H., Serotonergic dysfunction in depression. Br. J. Psychiatry(Suppl.), 1989, 25–31.
69. Messaoudi, M., Lalonde, R., Violle, N., Javelot, H., Desor, D., Nejdi, A., Bisson, J.-F., Rougeot, C., Pichelin, M., Cazaubiel, M., 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. 105 (2011), 755–764.
70. Millan, M.J., The neurobiology and control of anxious states. Prog. Neurobiol. 70 (2003), 83–244.
71. Mishima, Y., Shinoda, Y., Sadakata, T., Kojima, M., Wakana, S., Furuichi, T., Lack of stress responses to long-term effects of corticosterone in Caps2 knockout mice. Sci. Rep., 5, 2015, 8932.
72. Miyazaki, I., Asanuma, M., Dopaminergic neuron-specific oxidative stress caused by dopamine itself. Acta Med. Okayama 62 (2008), 141–150.
73. Mora, F., Segovia, G., Del Arco, A., de Blas, M., Garrido, P., Stress, neurotransmitters, corticosterone and body-brain integration. Brain Res. 1476 (2012), 71–85.
74. Moussavi, S., Chatterji, S., Verdes, E., Tandon, A., Patel, V., Ustun, B., Depression, chronic diseases, and decrements in health: results from the World Health Surveys. Lancet 370 (2007), 851–858.
75. Moya-Pérez, A., Perez-Villalba, A., Benítez-Páez, A., Campillo, I., Sanz, Y., Bifidobacterium CECT 7765 modulates early stress-induced immune, neuroendocrine and behavioral alterations in mice. Brain Behav. Immun. 65 (2017), 43–56.
76. Piwowarska, J., Chimiak, A., Matsumoto, H., Dziklińska, A., Radziwoń-Zaleska, M., Szelenberger, W., Pachecka, J., Serum cortisol concentration in patients with major depression after treatment with fluoxetine. Psychiatry Res. 198 (2012), 407–411.
77. Porsolt, R.D., Le Pichon, M., Jalfre, M., Depression: a new animal model sensitive to antidepressant treatments. Nature 266 (1977), 730–732.
78. Qin, H.-Y., Cheng, C.-W., Tang, X.-D., Bian, Z.-X., Impact of psychological stress on irritable bowel syndrome. World J. Gastroenterol. 20 (2014), 14126–14131.
79. Quesseveur, G., Gardier, A.M., Guiard, B.P., The monoaminergic tripartite synapse: a putative target for currently available antidepressant drugs. Curr. Drug Targets 14 (2013), 1272–1289.
80. Reber, S.O., Siebler, P.H., Donner, N.C., Morton, J.T., Smith, D.G., Kopelman, J.M., Lowe, K.R., Wheeler, K.J., Fox, J.H., Hassell, J.E. Jr., Greenwood, B.N., Jansch, C., Lechner, A., Schmidt, D., Uschold-Schmidt, N., Füchsl, A.M., Langgartner, D., Walker, F.R., Hale, M.W., Lopez Perez, G., Van Treuren, W., González, A., Halweg-Edwards, A.L., Fleshner, M., Raison, C.L., Rook, G.A., Peddada, S.D., Knight, R., Lowry, C.A., Immunization with a heat-killed preparation of the environmental bacterium Mycobacterium vaccae promotes stress resilience in mice. Proc. Natl. Acad. Sci. U.S.A. 113 (2016), E3130–E3139.
81. Sapolsky, R.M., Krey, L.C., McEwen, B.S., Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc. Natl. Acad. Sci. U.S.A. 81 (1984), 6174–6177.
82. Sawamoto, A., Okuyama, S., Yamamoto, K., Amakura, Y., Yoshimura, M., Nakajima, M., Furukawa, Y., 3,5,6,7,8,3’,4’-Heptamethoxyflavone, a citrus flavonoid, ameliorates corticosterone-induced depression-like behavior and restores brain-derived neurotrophic factor expression, neurogenesis, and neuroplasticity in the hippocampus. Molecules, 21, 2016, 541.
83. Steenbergen, L., Sellaro, R., van Hemert, S., Bosch, J.A., Colzato, L.S., A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain Behav. Immun. 48 (2015), 258–264.
84. Sterner, E.Y., Kalynchuk, L.E., Behavioral and neurobiological consequences of prolonged glucocorticoid exposure in rats: relevance to depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 34 (2010), 777–790.
85. Sturm, M., Becker, A., Schroeder, A., Bilkei-Gorzo, A., Zimmer, A., Effect of chronic corticosterone application on depression-like behavior in C57BL/6N and C57BL/6J mice. Genes Brain Behav. 14 (2015), 292–300.
86. Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X.-N., Kubo, C., Koga, Y., Postnatal microbial colonization programs the hypothalamic–pituitary–adrenal system for stress response in mice. J. Physiol. 558 (2004), 263–275.
87. Sullivan, R.M., Dufresne, M.M., Mesocortical dopamine and HPA axis regulation: Role of laterality and early environment. Brain Res. 1076 (2006), 49–59.
88. Swaab, D.F., Bao, A.-M., Lucassen, P.J., The stress system in the human brain in depression and neurodegeneration. Ageing Res. Rev. 4 (2005), 141–194.
89. Szyszkowicz, J.K., Wong, A., Anisman, H., Merali, Z., Audet, M.-C., Implications of the gut microbiota in vulnerability to the social avoidance effects of chronic social defeat in male mice. Brain Behav. Immun. 66 (2017), 45–55.
90. Teilmann, A.C., Nygaard Madsen, A., Holst, B., Hau, J., Rozell, B., Abelson, K.S., Physiological and pathological impact of blood sampling by retro-bulbar sinus puncture and facial vein phlebotomy in laboratory mice. PLoS One, 9, 2014, e113225.
91. Tõnissaar, M., Philips, M.-A., Eller, M., Harro, J., Sociability trait and serotonin metabolism in the rat social interaction test. Neurosci. Lett. 367 (2004), 309–312.
92. Thoenen, H., Neurotrophins and neuronal plasticity. Science (New York, N.Y.) 270 (1995), 593–598.
93. Trivedi, M.H., Rush, A.J., Wisniewski, S.R., Nierenberg, A.A., Warden, D., Ritz, L., Norquist, G., Howland, R.H., Lebowitz, B., McGrath, P.J., Shores-Wilson, K., Biggs, M.M., Balasubramani, G.K., Fava, M., Team, S.D.S., Evaluation of outcomes with citalopram for depression using measurement-based care in STAR*D: Implications for clinical practice. Am. J. Psychiat. 163 (2006), 28–40.
94. Webster, M.J., Knable, M.B., O'Grady, J., Orthmann, J., Weickert, C.S., Regional specificity of brain glucocorticoid receptor mRNA alterations in subjects with schizophrenia and mood disorders. Mol. Psychiatr. 7 (2002), 985–994.
95. Wu, T.-C., Chen, H.-T., Chang, H.-Y., Yang, C.-Y., Hsiao, M.-C., Cheng, M.-L., Chen, J.-C., Mineralocorticoid receptor antagonist spironolactone prevents chronic corticosterone induced depression-like behavior. Psychoneuroendocrinology 38 (2013), 871–883.
96. Xu, Z., Zhang, Y., Hou, B., Gao, Y., Wu, Y., Zhang, C., Chronic corticosterone administration from adolescence through early adulthood attenuates depression-like behaviors in mice. J. Affect. Disord. 131 (2011), 128–135.
97. Yan, T., Xu, M., Wan, S., Wang, M., Wu, B., Xiao, F., Bi, K., Jia, Y., Schisandra chinensis produces the antidepressant-like effects in repeated corticosterone-induced mice via the BDNF/TrkB/CREB signaling pathway. Psychiatry Res. 243 (2016), 135–142.
98. Yi, L.-T., Li, J., Li, H.-C., Zhou, Y., Su, B.-F., Yang, K.-F., Jiang, M., Zhang, Y.-T., Ethanol extracts from Hemerocallis citrina attenuate the decreases of brain-derived neurotrophic factor, TrkB levels in rat induced by corticosterone administration. J. Ethnopharmacol. 144 (2012), 328–334.
99. Zhao, Y., Ma, R., Shen, J., Su, H., Xing, D., Du, L., A mouse model of depression induced by repeated corticosterone injections. Eur. J. Pharmacol. 581 (2008), 113–120.