Stress-induced neuroinflammation is mediated by GSK3-dependent TLR4 signaling that promotes susceptibility to depression-like behavior

Brain, Behavior, and Immunity

Volumn 53, Issue , 2016, Pages 207-222

  Cheng, Yuyan ^a   Pardo, Marta ^a   Armini, Rubia de Souza ^a   Martinez, Ana ^b   Mouhsine, Hadley ^c   Zagury, Jean Francois ^c   Jope, Richard S ^a   Beurel, Eleonore ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c University of Paris Cité   (France)

Author keywords

Depression; Fluoxetine; Glycogen synthase kinase 3; Neuroinflammation; Stress; Toll like receptor 4

Indexed keywords

CRYOPYRIN; CXCL1 CHEMOKINE; EOTAXIN; GAMMA INTERFERON; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HIGH MOBILITY GROUP B1 PROTEIN; I KAPPA B ALPHA; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; FLUOXETINE; HMGB1 PROTEIN, MOUSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; TLR4 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEPRESSION; DISEASE PREDISPOSITION; ENZYME ACTIVATION; HIPPOCAMPUS; LEARNED HELPLESSNESS; MALE; MENTAL STRESS; MOUSE; NEUROPATHOLOGY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; CYTOKINES; DEPRESSION; FLUOXETINE; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; HMGB1 PROTEIN; INFLAMMASOMES; INFLAMMATION; MALE; MICE; MICE, KNOCKOUT; NEUROIMMUNOMODULATION; NF-KAPPA B; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84959475408     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.12.012     Document Type: Article

References (100)

1. Abdel-Salam O.M., Baiuomy A.R., Arbid M.S. Studies on the anti-inflammatory effect of fluoxetine in the rat. Pharmacol. Res. 2004, 49:119-131.
2. Alcocer-Gómez E., de Miguel M., Casas-Barquero N., Núñez-Vasco J., Sánchez-Alcazar J.A., Fernández-Rodríguez A., Cordero M.D. NLRP3 inflammasome is activated in mononuclear blood cells from patients with major depressive disorder. Brain Behav. Immun. 2014, 36:111-117.
3. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
4. Anisman H., Merali Z., Hayley S. Sensitization associated with stressors and cytokine treatments. Brain Behav. Immun. 2003, 17:86-93.
5. Audet M., Jacobson-Pick S., Wann B.P., Anisman H. Social defeat promotes specific cytokine variations within the prefrontal cortex upon subsequent aggressive or endotoxin challenges. Brain Behav. Immun. 2011, 25:1197-1205.
6. Barrientos R.M., Sprunger D.B., Campeau S., Watkins L.R., Rudy J.W., Maier S.F. BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1β administration. J. Neuroimmunol. 2004, 155:119-126.
7. Bauernfeind F.G., Horvath G., Stutz A., Alnemri E.S., MacDonald K., Speert D., Latz E. Cutting edge: NF-κB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 2009, 183:787-791.
8. Baumeister, D., Ciufolini, S., Mondelli, V., in press. Effects of psychotropic drugs on inflammation: consequence or mediator of therapeutic effects in psychiatric treatment? Psychopharmacology (Berl).
9. Belmaker R.H., Agam G. Major depressive disorder. N. Engl. J. Med. 2008, 358:55-68.
10. Beninson L.A., Brown P.N., Loughridge A.B., Saludes J.P., Maslanik T., Hills A.K., Fleshner M. Acute stressor exposure modifies plasma exosome-associated heat shock protein 72 (hsp72) and microRNA (miR-142-5p and miR-203). PLoS One 2014, 9:e108748.
11. Beurel E. Regulation by glycogen synthase kinase-3 of inflammation and T cells in CNS diseases. Front. Mol. Neurosci. 2011, 31:4-18.
12. Beurel E., Jope R.S. Lipopolysaccharide-induced interleukin-6 production is controlled by glycogen synthase kinase-3 and STAT3 in the brain. J. Neuroinflammation 2009, 6:9-20.
13. Beurel E., Harrington L.E., Jope R.S. Inflammatory T helper 17 cells promote depression-like behavior in mice. Biol. Psychiatry 2013, 73:622-630.
14. Beurel E., Grieco S.F., Jope R.S. Glycogen synthase kinase-3 (GSK3): regulation, actions, and diseases. Pharmacol. Ther. 2015, 148:114-131.
15. Bland S.T., Tamlyn J.P., Barrientos R.M., Greenwood B.N., Watkins L.R., Campeau S., Day H.E., Maier S.F. Expression of fibroblast growth factor-2 and brain-derived neurotrophic factor mRNA in the medial prefrontal cortex and hippocampus after uncontrollable or controllable stress. Neuroscience 2007, 144:1219-1228.
16. Blandino P., Barnum C.J., Deak T. The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1β responses to stress. J. Neuroimmunol. 2006, 173:87-95.
17. Blandino P., Barnum C.J., Solomon L.G., Larish Y., Lankow B.S., Deak T. Gene expression changes in the hypothalamus provide evidence for regionally-selective changes in IL-1 and microglial markers after acute stress. Brain Behav. Immun. 2009, 23:958-968.
18. Blondea N., Widmann C., Lazdunski M., Heurteaux C. Activation of the nuclear factor-κB is a key event in brain tolerance. J. Neurosci. 2001, 21:4668-4677.
19. Bluthé R.M., Michaud B., Poli V., Dantzer R. Role of IL-6 in cytokine-induced sickness behavior: a study with IL-6 deficient mice. Physiol. Behav. 2000, 70:367-373.
20. Bortolozzi A., Castañé A., Semakova J., Santana N., Alvarado G., Cortés R., Ferrés-Coy A., Fernández G., Carmona M.C., Toth M., Perales J.C., Montefeltro A., Artigas F. Selective siRNA-mediated suppression of 5-HT1A autoreceptors evokes strong anti-depressant-like effects. Mol. Psychiatr. 2012, 17:612-623.
21. Campisi J., Leem T.H., Fleshner M. Stress-induced extracellular Hsp72 is a functionally significant danger signal to the immune system. Cell Stress Chaperones 2003, 8:272-286.
22. Campisi J., Sharkey C., Johnson J.D., Asea A., Maslanik T., Bernstein-Hanley I., Fleshner M. Stress-induced facilitation of host response to bacterial challenge in F344 rats is dependent on extracellular heat shock protein 72 and independent of alpha beta T cells. Stress 2012, 15:637-646.
23. Crack P.J., Bray P.J. Toll-like receptors in the brain and their potential roles in neuropathology. Immunol. Cell Biol. 2007, 85:476-480.
24. Dantzer R., Kelley K.W. Twenty years of research on cytokine-induced sickness behavior. Brain Behav. Immun. 2007, 21:153-160.
25. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
26. De La Garza R. Endotoxin- or pro-inflammatory cytokine-induced sickness behavior as an animal model of depression: focus on anhedonia. Neurosci. Biobehav. Rev. 2005, 29:761-770.
27. De Pablos R.M., Villaran R.F., Argüelles S., Herrera A.J., Venero J.L., Ayala A., Machado A. Stress increases vulnerability to inflammation in the rat prefrontal cortex. J. Neurosci. 2006, 26:5709-5719.
28. Dean B. Understanding the role of inflammatory-related pathways in the pathophysiology and treatment of psychiatric disorders: evidence from human peripheral studies and CNS studies. Int. J. Neuropsychopharmacol. 2011, 14:997-1012.
29. Deak T., Bellamy C., D'Agostino L.G. Exposure to forced swim stress does not alter central production of IL-1. Brain Res. 2003, 972:53-63.
30. Deak T., Bordner K.A., McElderry N.K., Barnum C.J., Blandino P., Deak M.M., Tammariello S.P. Stress-induced increases in hypothalamic IL-1: a systematic analysis of multiple stressor paradigms. Brain Res. Bull. 2005, 64:541-556.
31. Espinosa-Oliva A.M., De Pablos R.M., Villarán R.F., Argüelles S., Venero J.L., Machado A., Cano J. Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol. Aging 2011, 32:85-102.
32. Fanous S., Hammer R.P., Nikulina E.M. Short- and long-term effects of intermittent social defeat stress on brain-derived neurotrophic factor expression in mesocorticolimbic brain regions. Neuroscience 2010, 167:598-607.
33. Ferrés-Coy A., Pilar-Cuellar F., Vidal R., Paz V., Masana M., Cortés R., Carmona M.C., Campa L., Pazos A., Montefeltro A., Valdizán E.M., Artigas F., Bortolozzi A. RNAi-mediated serotonin transporter suppression rapidly increases serotonergic neurotransmission and hippocampal neurogenesis. Transl. Psychiatr. 2013, 3:e211.
34. Ferrés-Coy A., Galofré M., Pilar-Cuéllar F., Vidal R., Paz V., Ruiz-Bronchal E., Campa L., Pazos Á., Caso J.R., Leza J.C., Alvarado G., Montefeltro A., Valdizán E.M., Artigas F., Bortolozzi A. Therapeutic antidepressant potential of a conjugated siRNA silencing the serotonin transporter after intranasal administration. Mol. Psychiatr. 2015, 10.1038/mp.2015.80.
35. Fleshner M., Campisi J., Amiri L., Diamond D.M. Cat exposure induces both intra-and extracellular Hsp72: the role of adrenal hormones. Psychoneuroendocrinology 2004, 29:1142-1152.
36. Frank M.G., Baratta M.V., Sprunger D.B., Watkins L.R., Maier S.F. Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav. Immun. 2007, 21:47-59.
37. Frank M.G., Hershman S.A., Weber M.D., Watkins L.R., Maier S.F. Chronic exposure to exogenous glucocorticoids primes microglia to pro-inflammatory stimuli and induces NLRP3 mRNA in the hippocampus. Psychoneuroendocrinology 2014, 40:191-200.
38. Frank M.G., Weber M.D., Watkins L.R., Maier S.F. Stress sounds the alarmin: the role of the danger-associated molecular pattern HMGB1 in stress-induced neuroinflammatory priming. Brain Behav. Immun. 2015, 48:1-7.
39. Fu X., Zunich S.M., O'Connor J.C., Kavelaars A., Dantzer R., Kelley K.W. Central administration of lipopolysaccharide induces depressive-like behavior in vivo and activates brain indoleamine 2, 3 dioxygenase in murine organotypic hippocampal slice cultures. J. Neuroinflammation 2010, 7:43.
40. Gárate I., García-Bueno B., Madrigal J.L., Bravo L., Berrocoso E., Caso J.R., Micó J.A., Leza J.C. Origin and consequences of brain Toll-like receptor 4 pathway stimulation in an experimental model of depression. J. Neuroinflammation 2011, 8:151.
41. Gárate I., Garcia-Bueno B., Madrigal J.L., Caso J.R., Alou L., Gomez-Lus M.L., Micó J.A., Leza J.C. Stress-induced neuroinflammation: role of the Toll-like receptor-4 pathway. Biol. Psychiatry 2013, 73:32-43.
42. Gárate I., García-Bueno B., Madrigal J.L., Caso J.R., Alou L., Gómez-Lus M.L., Leza J.C. Toll-like 4 receptor inhibitor TAK-242 decreases neuroinflammation in rat brain frontal cortex after stress. J. Neuroinflammation 2014, 11:8.
43. Goshen I., Kreisel T., Ben-Menachem-Zidon O., Licht T., Weidenfeld J., Ben-Hur T., Yirmiya R. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol. Psychiatr. 2008, 13:717-728.
44. Guo H., Callawa J.B., Ting J.P. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat. Med. 2015, 21:677-687.
45. Hanke M.L., Kielian T. Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. Clin. Sci. 2011, 121:367-387.
46. Hayley S., Brebner K., Lacosta S., Merali Z., Anisman H. Sensitization to the effects of tumor necrosis factor-α: neuroendocrine, central monoamine, and behavioral variations. J. Neurosci. 1999, 19:5654-5665.
47. Hayley S., Staines W., Merali Z., Anisman H. Time-dependent sensitization of corticotropin-releasing hormone, arginine vasopressin and c-fos immunoreactivity within the mouse brain in response to tumor necrosis factor-α. Neuroscience 2001, 106:137-148.
48. Hayley S., Merali Z., Anisman H. Stress and cytokine-elicited neuroendocrine and neurotransmitter sensitization: implications for depressive illness. Stress 2003, 6:19-32.
49. Hudson S.P., Jacobson-Pick S., Anisman H. Sex differences in behavior and pro-inflammatory cytokine mRNA expression following stressor exposure and re-exposure. Neuroscience 2014, 277:239-249.
50. Johnson J.D., O'Connor K.A., Deak T., Stark M., Watkins L.R., Maier S.F. Prior stressor exposure sensitizes LPS-induced cytokine production. Brain Behav. Immun. 2002, 16:461-476.
51. Johnson J.D., O'Connor K.A., Hansen M.K., Watkins L.R., Maier S.F. Effects of prior stress on LPS-induced cytokine and sickness responses. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 284:422-432.
52. Johnson J.D., O'Connor K.A., Stark M., Watkins L.R., Maier S.F. The role of IL-1beta in stress-induced sensitization of proinflammatory cytokine and corticosterone responses. Neuroscience 2004, 127:569-577.
53. Jope R.S., Yuskaitis C.J., Beurel E. Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem. Res. 2007, 32:577-595.
54. Jope R.S. Glycogen synthase kinase-3 in the etiology and treatment of mood disorders. Front. Mol. Neurosci. 2011, 4:16-26.
55. Kanazawa T., Morisaki K., Suzuki S., Takashima Y. Prolongation of life in rats with malignant glioma by intranasal siRNA/drug codelivery to the brain with cell-penetrating peptide-modified micelles. Mol. Pharmacol. 2014, 11:1471-1478.
56. Karson A., Demirtaş T., Bayramgürler D., Balci F., Utkan T. Chronic administration of infliximab (TNF-α inhibitor) decreases depression and anxiety-like behaviour in rat model of chronic mild stress. Basic Clin. Pharmacol. Toxicol. 2013, 112:335-340.
57. Kaster M.P., Gadotti V.M., Calixto J.B., Santos A.R., Rodrigues A.L.S. Depressive-like behavior induced by tumor necrosis factor-α in mice. Neuropharmacology 2012, 62:419-426.
58. Kim I.D., Shin J.H., Kim S.W., Choi S., Ahn J., Han P.L., Park J.S., Lee J.K. Intranasal delivery of HMGB1 siRNA confers target gene knockdown and robust neuroprotection in the postischemic brain. Mol. Ther. 2012, 20:829-839.
59. Kreisel T., Frank M.G., Licht T., Reshef R., Ben-Menachem-Zidon O., Baratta M.V., Yirmiya R. Dynamic microglial alterations underlie stress-induced depressive-like behavior and suppressed neurogenesis. Mol. Psychiatr. 2014, 19:699-709.
60. Kubera M., Obuchowicz E., Goehler L., Brzeszcz J., Maes M. In animal models, psychosocial stress-induced (neuro) inflammation, apoptosis and reduced neurogenesis are associated to the onset of depression. Prog. Neuro-Psychopharmacol. Biol. Psychiatr. 2011, 35:744-759.
61. Lawson L.J., Perry V.H., Dri P., Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990, 39:151-170.
62. Li X., Zhu W., Roh M.S., Friedman A.B., Rosborough K., Jope R.S. In vivo regulation of glycogen synthase kinase-3β (GSK3β) by serotonergic activity in mouse brain. Neuropsychopharmacology 2004, 29:1426-1431.
63. Liu D., Wang Z., Liu S., Wang F., Zhao S., Hao A. Anti-inflammatory effects of fluoxetine in lipopolysaccharide (LPS)-stimulated microglial cells. Neuropharmacology 2011, 61:592-599.
64. Madrigal J.L., Hurtado O., Moro M.A., Lizasoain I., Lorenzo P., Castrillo A., Boscá L., Leza J.C. The increase in TNF-alpha levels is implicated in NF-B activation and inducible nitric oxide synthase expression in brain cortex after immobilization stress. Neuropsychopharmacology 2002, 26:155-163.
65. Martin M., Rehani K., Jope R.S., Michalek S.M. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 2005, 6:777-784.
66. Martinez A., Alonso M., Castro A., Pérez C., Moreno F.J. First non-ATP competitive glycogen synthase kinase 3β (GSK-3β) inhibitors: thiadiazolidinones (TDZD) as potential drugs for the treatment of Alzheimer's disease. J. Med. Chem. 2002, 45:1292-1299.
67. Maslanik T., Mahaffey L., Tannura K., Beninson L., Greenwood B.N., Fleshner M. The inflammasome and danger associated molecular patterns (DAMPs) are implicated in cytokine and chemokine responses following stressor exposure. Brain Behav. Immun. 2013, 28:54-62.
68. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 2009, 65:732-741.
69. Mohanty C., Kundu P., Sahoo S.K. Brain targeting of siRNA via intranasal pathway. Curr. Pharm. Des. 2015, 21:4606-4613.
70. Munhoz C.D., Lepsch L.B., Kawamoto E.M., Malta M.B., de Sá Lima L., Avellar M.C.W., Scavone C. Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-κB in the frontal cortex and hippocampus via glucocorticoid secretion. J. Neurosci. 2006, 26:3813-3820.
71. Nguyen K.T., Deak T., Will M.J., Hansen M.K., Hunsaker B.N., Fleshner M., Watkins L.R., Maier S.F. Time course and corticosterone sensitivity of the brain, pituitary, and serum interleukin-1beta protein response to acute stress. Brain Res. 2000, 859:193-201.
72. O'Connor K.A., Johnson J.D., Hansen M.K., Wieseler Frank J.L., Maksimova E., Watkins L.R., Maier S.F. Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res. 2003, 991:123-132.
73. Palin K., McCusker R.H., Strle K., Moos F., Dantzer R., Kelley K.W. Tumor necrosis factor-α-induced sickness behavior is impaired by central administration of an inhibitor of c-jun N-terminal kinase. Psychopharmacology 2008, 197:629-635.
74. Pan Y., Chen X.Y., Zhang Q.Y., Kong L.D. Microglial NLRP3 inflammasome activation mediates IL-1β-related inflammation in prefrontal cortex of depressive rats. Brain Behav. Immun. 2014, 41:90-100.
75. Pandey G.N., Rizavi H.S., Ren X., Fareed J., Hoppensteadt D.A., Roberts R.C., Dwivedi Y. Proinflammatory cytokines in the prefrontal cortex of teenage suicide victims. J. Psychiatr. Res. 2012, 46:57-63.
76. Pandey S., Agrawal D.K. Immunobiology of Toll-like receptors: emerging trends. Immunol. Cell Biol. 2006, 84:333-341.
77. Piccinini A.M., Midwood K.S. (2010) DAMPening inflammation by modulating TLR signalling. Mediators Inflamm. 2010.
78. Pizarro J.M., Lumley L.A., Medina W., Robison C.L., Chang W.E., Alagappan A., Bah M.J., Dawood M.Y., Shah J.D., Mark B., Kendall N., Smith M.A., Saviolakis G.A., Meyerhoff J.L. Acute social defeat reduces neurotrophin expression in brain cortical and subcortical areas in mice. Brain Res. 2004, 1025:10-20.
79. Quan N., Avitsur R., Stark J.L., He L., Shah M., Caligiuri M., Sheridan J.F. Social stress increases the susceptibility to endotoxic shock. J. Neuroimmunol. 2001, 115:36-45.
80. Raison C.L., Miller A.H. Anti-inflammatory agents as antidepressants: truth or dare?. Psychiat. Ann. 2015, 45:255-261.
81. Roumestan C., Michel A., Bichon F., Portet K., Detoc M., Henriquet C., Mathieu M. Anti-inflammatory properties of desipramine and fluoxetine. Respir. Res. 2007, 8:35-45.
82. Sacre S., Medghalchi M., Gregory B., Brennan F., Williams R. Fluoxetine and citalopram exhibit potent antiinflammatory activity in human and murine models of rheumatoid arthritis and inhibit toll-like receptors. Arthritis Rheum. 2010, 62:683-693.
83. Schaefer L. Complexity of danger: the diverse nature of damage-associated molecular patterns. J. Biol. Chem. 2014, 289:35237-35245.
84. Schmidt E.D., Aguilera G., Binnekade R., Tilders F.J.H. Single administration of interleukin-1 increased corticotropin releasing hormone and corticotropin releasing hormone-receptor mRNA in the hypothalamic paraventricular nucleus which paralleled long-lasting (weeks) sensitization to emotional stressors. Neuroscience 2003, 116:275-283.
85. Simen B.B., Duman C.H., Simen A.A., Duman R.S. TNFalpha signaling in depression and anxiety: behavioral consequences of individual receptor targeting. Biol. Psychiatry 2006, 59:775-785.
86. Smith M.A., Makino S., Kvetnansky R., Post R.M. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J. Neurosci. 1995, 15:1768-1777.
87. Tanga F.Y., Nutile-McMenemy N., DeLeo J.A. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5856-5861.
88. Tilders F.J., Schmidt E.D. Cross-sensitization between immune and non-immune stressors. A role in the etiology of depression?. Adv. Exp. Med. Biol. 1999, 461:179-197.
89. Tonelli L.H., Stiller J., Rujescu D., Giegling I., Schneider B., Maurer K., Postolache T.T. Elevated cytokine expression in the orbitofrontal cortex of victims of suicide. Acta Psychiatr. Scand. 2008, 117:198-206.
90. Tschopp J., Schroder K. NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production?. Nat. Rev. Immunol. 2010, 10:210-215.
91. Warner-Schmidt J.L., Vanover K.E., Chen E.Y., Marshall J.J., Greengard P. Antidepressant effects of selective serotonin reuptake inhibitors (SSRIs) are attenuated by antiinflammatory drugs in mice and humans. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9262-9267.
92. Weber M.D., Frank M.G., Sobesky J.L., Watkins L.R., Maier S.F. Blocking toll-like receptor 2 and 4 signaling during a stressor prevents stress-induced priming of neuroinflammatory responses to a subsequent immune challenge. Brain Behav. Immun. 2013, 32:112-121.
93. Weber M.D., Frank M.G., Tracey K.J., Watkins L.R., Maier S.F. Stress induces the danger-associated molecular pattern HMGB-1 in the hippocampus of male Sprague Dawley rats: a priming stimulus of microglia and the NLRP3 inflammasome. J. Neurosci. 2015, 35:316-324.
94. Wohleb E.S., Hanke M.L., Corona A.W., Powell N.D., La'Tonia M.S., Bailey M.T., Sheridan J.F. β-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. 2011, 31:6277-6288.
95. Wohleb E.S., Fenn A.M., Pacenta A.M., Powell N.D., Sheridan J.F., Godbout J.P. Peripheral innate immune challenge exaggerated microglia activation, increased the number of inflammatory CNS macrophages, and prolonged social withdrawal in socially defeated mice. Psychoneuroendocrinology 2012, 37:1491-1505.
96. Xiang M., Shi X., Li Y., Xu J., Yin L., Xiao G., Fan J. Hemorrhagic shock activation of NLRP3 inflammasome in lung endothelial cells. J. Immunol. 2011, 187:4809-4817.
97. You Z., Luo C., Zhang W., Chen Y., He J., Zhao Q., Wu Y. Pro-and anti-inflammatory cytokines expression in rat's brain and spleen exposed to chronic mild stress: involvement in depression. Behav. Brain Res. 2011, 225:135-141.
98. Yuskaitis C.J., Jope R.S. Glycogen synthase kinase-3 regulates microglial migration, inflammation, and inflammation-induced neurotoxicity. Cell. Signal. 2009, 21:264-273.
99. Zhang, Y., Liu, L., Liu, Y.Z., Shen, X.L., Wu, T.Y., Zhang, T., Jiang, C.L., in press. NLRP3 Inflammasome mediates chronic mild stress-induced depression in mice via neuroinflammation. Int. J. Neuropsychopharmacol.
100. Zunszain P.A., Hepgul N., Pariante C.M. Inflammation and depression. Curr. Top Behav. Neurosci. 2013, 14:135-151.