Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal

Neuropsychopharmacology

Volumn 42, Issue 1, 2017, Pages 46-61

  Weber, Michael D ^a   Godbout, Jonathan P ^a   Sheridan, John F ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 1BETA;

AFFECT; BEHAVIOR; BEHAVIOR CHANGE; BLOOD BRAIN BARRIER; BONE MARROW CELL; CELL ACTIVITY; CELL COMMUNICATION; CENTRAL NERVOUS SYSTEM; CHRONIC STRESS; CLINICAL RESEARCH; DISEASE ASSOCIATION; ENDOTHELIUM; ENDOTHELIUM CELL; EVIDENCE BASED PRACTICE; HEMATOPOIESIS; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; INFLAMMATION; MONOCYTE; MYELOPOIESIS; NERVOUS SYSTEM INFLAMMATION; NEUROENDOCRINE SYSTEM; PRIORITY JOURNAL; REPEATED SOCIAL DEFEAT; REVIEW; SIGNAL TRANSDUCTION; SOCIAL ASPECT; ANIMAL; COMPLICATION; IMMUNOLOGY; MENTAL DISEASE; MENTAL STRESS; PHYSIOLOGY;

ANIMALS; BEHAVIOR; CENTRAL NERVOUS SYSTEM; HUMANS; IMMUNE SYSTEM; INFLAMMATION; MENTAL DISORDERS; MONOCYTES; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL;

EID: 84978743318     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2016.102     Document Type: Review

References (149)

1. Aloisi F (2001). Immune function of microglia. Glia 36: 165-179.
2. Asahi M, Asahi K, Jung JC, del Zoppo GJ, Fini ME, Lo EH (2000). Role for matrixmetalloproteinase 9 after focal cerebral ischemia: effects of gene knockout andenzyme inhibition with BB-94. J Cereb Blood Flow Metab 20: 1681-1689.
3. Ataka K, Asakawa A, Nagaishi K, Kaimoto K, Sawada A, Hayakawa Y, et al. (2013).Bone marrow-derived microglia infiltrate into the paraventricular nucleus ofchronic psychological stress-loaded mice. Plos One 8: e81744.
4. Audoy-Remus J, Richard JF, Soulet D, Zhou H, Kubes P, Vallieres L (2008).Rod-shaped monocytes patrol the brain vasculature and give rise to perivascularmacrophages under the influence of proinflammatory cytokines andangiopoietin-2. J Neurosci 28: 10187-10199.
5. Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, Kayal S, et al. (2007). Monitoringof blood vessels and tissues by a population of monocytes with patrollingbehavior. Science 317: 666-670.
6. Avitsur R, Kinsey SG, Bidor K, Bailey MT, Padgett DA, Sheridan JF (2007).Subordinate social status modulates the vulnerability to the immunological effectsof social stress. Psychoneuroendocrinology 32: 1097-1105.
7. Avitsur R, Padgett DA, Dhabhar FS, Stark JL, Kramer KA, Engler H, et al. (2003).Expression of glucocorticoid resistance following social stress requires a secondsignal. J Leukoc Biol 74: 507-513.
8. Avitsur R, Stark JL, Dhabhar FS, Padgett DA, Sheridan JF (2002). Social disruptioninducedglucocorticoid resistance: kinetics and site specificity. J Neuroimmunol124: 54-61.
9. Avolio C, Ruggieri M, Giuliani F, Liuzzi GM, Leante R, Riccio P, et al. (2003). SerumMMP-2 and MMP-9 are elevated in different multiple sclerosis subtypes.J Neuroimmunol 136: 46-53.
10. Bailey MT, Engler H, Powell ND, Padgett DA, Sheridan JF (2007). Repeated socialdefeat increases the bactericidal activity of splenic macrophages through a Tolllikereceptor-dependent pathway. Am J Physiol Regul Integrd Comp Physiol 293:R1180-R1190.
11. Bauer ME, Perks P, Lightman SL, Shanks N (2001). Restraint stress is associatedwith changes in glucocorticoid immunoregulation. Physiol Behav 73: 525-532.
12. Bebo BF Jr, Linthicum DS (1995). Expression of mRNA for 55-kDa and 75-kDatumor necrosis factor (TNF) receptors in mouse cerebrovascular endothelium:effects of interleukin-1 beta, interferon-gamma and TNF-alpha on cultured cells.J Neuroimmunol 62: 161-167.
13. Bechmann I, Galea I, Perry VH (2007). What is the blood-brain barrier (not)? TrendsImmunol 28: 5-11.
14. Bian YQ, Pan Z, Hou ZY, Huang C, Li W, Zhao BH (2012). Learning, memory, andglial cell changes following recovery from chronic unpredictable stress. Brain ResBull 88: 471-476.
15. Bianchi ME (2007). DAMPs, PAMPs and alarmins: all we need to know aboutdanger. J Leukoc Biol 81: 1-5.
16. Blandino P Jr, Barnum CJ, Deak T (2006). The involvement of norepinephrineand microglia in hypothalamic and splenic IL-1beta responses to stress.J Neuroimmunol 173: 87-95.
17. Brevet M, Kojima H, Asakawa A, Atsuchi K, Ushikai M, Ataka K, et al. (2010). Chronicfoot-shock stress potentiates the influx of bone marrow-derived microglia intohippocampus. J Neurosci Res 88: 1890-1897.
18. Calhoon GG, Tye KM (2015). Resolving the neural circuits of anxiety. Nat Neurosci18: 1394-1404.
19. Cannuscio CC, Jones C, Kawachi I, Colditz GA, Berkman L, Rimm E (2002).Reverberations of family illness: a longitudinal assessment of informal caregivingand mental health status in the Nurses' Health Study. Am J Public Health 92:1305-1311.
20. Catanzaro JM, Hueston CM, Deak MM, Deak T (2014). The impact of the P2X7receptor antagonist A-804598 on neuroimmune and behavioral consequences ofstress. Behav Pharmacol 25: 582-598.
21. Chijiwa T, Oka T, Lkhagvasuren B, Yoshihara K, Sudo N (2015). Prior chronic stressinduces persistent polyI:C-induced allodynia and depressive-like behavior in rats:possible involvement of glucocorticoids and microglia. Physiol Behav 147:264-273.
22. Colomar A, Marty V, Medina C, Combe C, Parnet P, Amedee T (2003).Maturation and release of interleukin-1beta by lipopolysaccharide-primed mouseSchwann cells require the stimulation of P2X7 receptors. J Biol Chem 278:30732-30740.
23. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990). Glutamate inducescalcium waves in cultured astrocytes: long-range glial signaling. Science 247:470-473.
24. Cotrina ML, Lin JH, Lopez-Garcia JC, Naus CC, Nedergaard M (2000).ATP-mediated glia signaling. J Neurosci 20: 2835-2844.
25. Coutinho AE, Chapman KE (2011). The anti-inflammatory and immunosuppressiveeffects of glucocorticoids, recent developments and mechanistic insights. MolCell Endocrinol 335: 2-13.
26. D'Mello C, Le T, Swain MG (2009). Cerebral microglia recruit monocytes into thebrain in response to tumor necrosis factor alpha signaling during peripheral organinflammation. J Neurosci 29: 2089-2102.
27. Dantzer R, Bluthe RM, Gheusi G, Cremona S, Laye S, Parnet P, et al. (1998).Molecular basis of sickness behavior. Ann NY Acad Sci 856: 132-138.
28. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW (2008). Frominflammation to sickness and depression: when the immune system subjugatesthe brain. Nat Rev Neurosci 9: 46-57.
29. Davies TH, Ning YM, Sanchez ER (2002). A new first step in activation of steroidreceptors-Hormone-induced switching of FKBP51 and FKBP52 immunophilins.J Biol Chem 277: 4597-4600.
30. Dhabhar FS, Malarkey WB, Neri E, McEwen BS (2012). Stress-induced redistributionof immune cells-from barracks to boulevards to battlefields: a tale ofthree hormones-Curt Richter Award winner. Psychoneuroendocrinology 37:1345-1368.
31. Dimitrijevic OB, Stamatovic SM, Keep RF, Andjelkovic AV (2006). Effects of thechemokine CCL2 on blood-brain barrier permeability during ischemia-reperfusioninjury. J Cereb Blood Flow Metab 26: 797-810.
32. Diserbo M, Agin A, Lamproglou I, Mauris J, Staali F, Multon E, et al. (2002). Bloodbrainbarrier permeability after gamma whole-body irradiation: an in vivomicrodialysis study. Can J Physiol Pharmacol 80: 670-678.
33. Donnelly DJ, Longbrake EE, Shawler TM, Kigerl KA, Lai W, Tovar CA, et al. (2011).Deficient CX3CR1 signaling promotes recovery after mouse spinal cord injury bylimiting the recruitment and activation of Ly6Clo/iNOS+ macrophages. J Neurosci31: 9910-9922.
34. Duits FH, Hernandez-Guillamon M, Montaner J, Goos JD, Montanola A, Wattjes MPet al (2015). Matrix metalloproteinases in Alzheimer's disease and concurrentcerebral microbleeds. J Alzheimers Dis 48: 711-720.
35. Eash KJ, Means JM, White DW, Link DC (2009). CXCR4 is a key regulator ofneutrophil release from the bone marrow under basal and stress granulopoiesisconditions. Blood 113: 4711-4719.
36. Engler H, Bailey MT, Engler A, Sheridan JF (2004). Effects of repeated social stresson leukocyte distribution in bone marrow, peripheral blood and spleen.J Neuroimmunol 148: 106-115.
37. Ericsson A, Liu C, Hart RP, Sawchenko PE (1995). Type 1 interleukin-1 receptor inthe rat brain: distribution, regulation, and relationship to sites of IL-1-inducedcellular activation. J Comp Neurol 361: 681-698.
38. Eugenin EA, Osiecki K, Lopez L, Goldstein H, Calderon TM, Berman JW (2006).CCL2/monocyte chemoattractant protein-1 mediates enhanced transmigration ofhuman immunodeficiency virus (HIV)-infected leukocytes across the blood-brainbarrier: A potential mechanism of HIV-CNS invasion and NeuroAIDS. J Neurosci26: 1098-1106.
39. Felten DL, Felten SY, Carlson SL, Olschowka JA, Livnat S (1985). Noradrenergic andpeptidergic innervation of lymphoid tissue. J Immunol 135(2 Suppl): 755s-765s.
40. Frank MG, Baratta MV, Sprunger DB, Watkins LR, Maier SF (2007). Microglia serveas a neuroimmune substrate for stress-induced potentiation of CNS proinflammatorycytokine responses. Brain Behav Immun 21: 47-59.
41. Frank MG, Thompson BM, Watkins LR, Maier SF (2012). Glucocorticoids mediatestress-induced priming of microglial pro-inflammatory responses. Brain BehavImmun 26: 337-345.
42. Frank MG, Weber MD, Fonken LK, Hershman SA, Watkins LR, Maier SF (2015a).The redox state of the alarmin HMGB1 is a pivotal factor in neuroinflammatory andmicroglial priming: a role for the NLRP3 inflammasome. Brain Behav Immun 55:215-224.
43. Frank MG, Weber MD, Watkins LR, Maier SF (2015b). Stress sounds the alarmin:the role of the danger-associated molecular pattern HMGB1 in stress-inducedneuroinflammatory priming. Brain Behav Immun 48: 1-7.
44. Galigniana NM, Ballmer LT, Toneatto J, Erlejman AG, Lagadari M, Galigniana MD(2012). Regulation of the glucocorticoid response to stress-related disorders bythe Hsp90-binding immunophilin FKBP51. J Neurochem 122: 4-18.
45. Gehrmann J, Matsumoto Y, Kreutzberg GW (1995). Microglia: intrinsic immuneffectorcell of the brain. Brain Res Brain Res Rev 20: 269-287.
46. Gilman SE, Trinh NH, Smoller JW, Fava M, Murphy JM, Breslau J (2013).Psychosocial stressors and the prognosis of major depression: a test of Axis IV.Psychol Med 43: 303-316.
47. Gomez-Nicola D, Schetters ST, Perry VH (2014). Differential role of CCR2 in thedynamics of microglia and perivascular macrophages during prion disease. Glia62: 1041-1052.
48. Greenwood J, Heasman SJ, Alvarez JI, Prat A, Lyck R, Engelhardt B (2011).Leucocyte-endothelial cell crosstalk at the blood-brain barrier: a prerequisite forsuccessful immune cell entry to the brain. Neuropathol Appl Neurobiol 37: 24-39.
49. Grozdanov V, Bliederhaeuser C, Ruf WP, Roth V, Fundel-Clemens K, Zondler L, et al.(2014). Inflammatory dysregulation of blood monocytes in Parkinson's diseasepatients. Acta Neuropathol 128: 651-663.
50. Haegeman G, De Bosscher K, Vanden Berghe W (2003). The interplay between theglucocorticoid receptor and nuclear factor-kappa B or activator protein-1:molecular mechanisms for gene repression. Endocr Rev 24: 488-522.
51. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, Reinheckel T, et al. (2008).The NALP3 inflammasome is involved in the innate immune response to amyloidbeta.Nat Immunol 9: 857-865.
52. Hamilton JA, Achuthan A (2013). Colony stimulating factors and myeloid cell biologyin health and disease. Trends Immunol 34: 81-89.
53. Hammond MD, Taylor RA, Mullen MT, Ai YX, Aguila HL, Mack M, et al. (2014). CCR2(+)Ly6C(hi) inflammatory monocyte recruitment exacerbates acute disabilityfollowing intracerebral hemorrhage. J Neurosci 34: 3901-3909.
54. Hanamsagar R, Hanke ML, Kielian T (2012). Toll-like receptor (TLR) andinflammasome actions in the central nervous system. Trends Immunol 33:333-342.
55. Hanke ML, Powell ND, Stiner LM, Bailey MT, Sheridan JF (2012). Beta adrenergicblockade decreases the immunomodulatory effects of social disruption stress.Brain Behav Immun 26: 1150-1159.
56. Haroon E, Raison CL, Miller AH (2012). Psychoneuroimmunology meets neuropsychopharmacology:translational implications of the impact of inflammation onbehavior. Neuropsychopharmacology 37: 137-162.
57. He X, Zhang L, Yao X, Hu J, Yu L, Jia H, et al. (2013). Association studies of MMP-9 inParkinson's disease and amyotrophic lateral sclerosis. PLoS One 8: e73777.
58. Heidt T, Sager HB, Courties G, Dutta P, Iwamoto Y, Zaltsman A, et al. (2014). Chronicvariable stress activates hematopoietic stem cells. Nat Med 20: 754-758.
59. Hinwood M, Morandini J, Day TA, Walker FR (2012). Evidence that microglia mediatethe neurobiological effects of chronic psychological stress on the medial prefrontalcortex. Cereb Cortex 22: 1442-1454.
60. Hinwood M, Tynan RJ, Charnley JL, Beynon SB, Day TA, Walker FR (2013). Chronicstress induced remodeling of the prefrontal cortex: structural re-organization ofmicroglia and the inhibitory effect of minocycline. Cereb Cortex 23: 1784-1797.
61. Hodes GE, Kana V, Menard C, Merad M, Russo SJ (2015). Neuroimmunemechanisms of depression. Nat Neurosci 18: 1386-1393.
62. Hodes GE, Pfau ML, Leboeuf M, Golden SA, Christoffel DJ, Bregman D, et al. (2014).Individual differences in the peripheral immune system promote resilience versussusceptibility to social stress. Proc Natl Acad Sci USA 111: 16136-16141.
63. Hunzeker J, Padgett DA, Sheridan PA, Dhabhar FS, Sheridan JF (2004). Modulationof natural killer cell activity by restraint stress during an influenza A/PR8 infectionin mice. Brain Behav Immun 18: 526-535.
64. Iwata M, Ota KT, Li XY, Sakaue F, Li N, Dutheil S, et al. (2015). Psychological stressactivates the inflammasome via release of adenosine triphosphate and stimulationof the purinergic type 2X7 receptor. Biol Psychiatry 80: 12-22.
65. Jin J, Wang X, Wang Q, Guo X, Cao J, Zhang X, et al. (2013). Chronic psychologicalstress induces the accumulation of myeloid-derived suppressor cells in mice.PLoS One 8: e74497.
66. Johnson JD, O'Connor KA, Hansen MK, Watkins LR, Maier SF (2003). Effects ofprior stress on LPS-induced cytokine and sickness responses. Am J PhysiolRegul Integr Comp Physiol 284: R422-R432.
67. Johnson JD, Zimomra ZR, Stewart LT (2013). Beta-adrenergic receptor activationprimes microglia cytokine production. J Neuroimmunol 254: 161-164.
68. Jung SH, Wang YF, Kim T, Tarr A, Reader B, Powell N, et al. (2015). Molecularmechanisms of repeated social defeat-induced glucocorticoid resistance: role ofmicroRNA. Brain Behav Immun 44: 195-206.
69. Kang R, Chen R, Zhang Q, Hou W, Wu S, Cao L, et al. (2014). HMGB1 in health anddisease. Mol Aspects Med 40: 1-116.
70. Katayama Y, Battista M, Kao WM, Hidalgo A, Peired AJ, Thomas SA, et al. (2006).Signals from the sympathetic nervous system regulate hematopoietic stem cellegress from bone marrow. Cell 124: 407-421.
71. Kessler RC (1997). The effects of stressful life events on depression. Annu RevPsychol 48: 191-214.
72. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011). Physiology of microglia.Physiol Rev 91: 461-553.
73. Khansari DN, Murgo AJ, Faith RE (1990). Effects of stress on the immune-system.Immunol Today 11: 170-175.
74. Kiecolt-glaser JK, Marucha PT, Malarkey WB, Mercado AM, Glaser R (1995).Slowing of wound-healing by psychological stress. Lancet 346: 1194-1196.
75. Kiecolt-glaser JK, Speicher CE, Glaser R, Dura JR, Trask OJ (1991). Spousalcaregivers of dementia victims-longitudinal changes in immunity and health.Psychosom Med 53: 345-362.
76. Kierdorf K, Katzmarski N, Haas CA, Prinz M (2013). Bone marrow cell recruitment tothe brain in the absence of irradiation or parabiosis bias. PLoS One 8: e58544.
77. Kim M, Carman CV, Springer TA (2003). Bidirectional transmembrane signaling bycytoplasmic domain separation in integrins. Science 301: 1720-1725.
78. Kinsey SG, Bailey MT, Sheridan JF, Padgett DA, Avitsur R (2007). Repeated socialdefeat causes increased anxiety-like behavior and alters splenocyte function inC57BL/6 and CD-1 mice. Brain Behav Immun 21: 458-466.
79. Kopp BL, Wick D, Herman JP (2013). Differential effects of homotypic vs. heterotypicchronic stress regimens on microglial activation in the prefrontal cortex. PhysiolBehav 122: 246-252.
80. Kreisel T, Frank MG, Licht T, Reshef R, Ben-Menachem-Zidon O, Baratta MV, et al.(2014). Dynamic microglial alterations underlie stress-induced depressive-likebehavior and suppressed neurogenesis. Mol Psychiatry 19: 699-709.
81. LeDoux J (2003). The emotional brain, fear, and the amygdala. Cell Mol Neurobiol23: 727-738.
82. Leemans JC, Cassel SL, Sutterwala FS (2011). Sensing damage by the NLRP3inflammasome. Immunol Rev 243: 152-162.
83. Levine J, Barak Y, Chengappa KN, Rapoport A, Rebey M, Barak V (1999).Cerebrospinal cytokine levels in patients with acute depression. Neuropsychobiology40: 171-176.
84. Li QM, Powell N, Zhang H, Belevych N, Ching S, Chen Q, et al. (2011). EndothelialIL-1R1 is a critical mediator of EAE pathogenesis. Brain Behav Immun 25:160-167.
85. Liesz A, Dalpke A, Mracsko E, Antoine DJ, Roth S, Zhou W, et al. (2015). DAMPsignaling is a key pathway inducing immune modulation after brain injury.J Neurosci 35: 583-598.
86. Liu YN, Peng YL, Liu L, Wu TY, Zhang Y, Lian YJ, et al. (2015). TNFalphamediates stress-induced depression by upregulating indoleamine 2,3-dioxygenasein a mouse model of unpredictable chronic mild stress. Eur Cytokine Netw 26:15-25.
87. Lorant V, Deliege D, Eaton W, Robert A, Philippot P, Ansseau M (2003).Socioeconomic inequalities in depression: a meta-analysis. Am J Epidemiol 157:98-112.
88. Maier SF, Watkins LR (1998). Cytokines for psychologists: implications ofbidirectional immune-to-brain communication for understanding behavior, mood,and cognition. Psychol Rev 105: 83-107.
89. Maier SF, Watkins LR (2003). Immune-to-central nervous system communicationand its role in modulating pain and cognition: Implications for cancer and cancertreatment. Brain Behav Immun 17: S125-S131.
90. Martinon F, Burns K, Tschopp J (2002). The inflammasome: a molecular platformtriggering activation of inflammatory caspases and processing of proIL-beta. MolCell 10: 417-426.
91. Matzinger P (2002). The danger model: a renewed sense of self. Science 296:301-305.
92. McEwen BS (1999). Stress and hippocampal plasticity. Annu Rev Neurosci 22:105-122.
93. McKim DB, Niraula A, Tarr A, Wohleb ES, Sheridan J, Godbout JP (2016).Neuroinflammatory dynamics underlie memory impairments following repeatedsocial defeat. J Neurosci 36: 2590-2604.
94. McKim DB, Patterson JM, Wohleb ES, Jarrett BL, Reader BF, Godbout JP, et al.(2015). Sympathetic release of splenic monocytes promotes recurring anxietyfollowing repeated social defeat. Biol Psychiatry 79: 803-813.
95. Miller AH, Haroon E, Raison CL, Felger JC (2013). Cytokine targets in the brain:impact on neurotransmitters and neurocircuits. Depress Anxiety 30: 297-306.
96. Miller AH, Raison CL (2015). The role of inflammation in depression: fromevolutionary imperative to modern treatment target. Nat Rev Immunol 16:22-34.
97. Miller GE, Chen E, Fok AK, Walker H, Lim A, Nicholls EF, et al. (2009). Low early-lifesocial class leaves a biological residue manifested by decreased glucocorticoidand increased proinflammatory signaling. Proc Natl Acad Sci USA 106:14716-14721.
98. Miller GE, Chen E, Sze J, Marin T, Arevalo JM, Doll R, et al. (2008). A functionalgenomic fingerprint of chronic stress in humans: blunted glucocorticoid andincreased NF-kappaB signaling. Biol Psychiatry 64: 266-272.
99. Miller GE, Cole SW (2012). Clustering of depression and inflammation in adolescentspreviously exposed to childhood adversity. Biol Psychiatry 72: 34-40.
100. Miller GE, Murphy ML, Cashman R, Ma R, Ma J, Arevalo JM, et al. (2014). Greaterinflammatory activity and blunted glucocorticoid signaling in monocytes ofchronically stressed caregivers. Brain Behav Immun 41: 191-199.
101. Monif M, Reid CA, Powell KL, Smart ML, Williams DA (2009). The P2X7 receptordrives microglial activation and proliferation: a trophic role for P2X7R pore.J Neurosci 29: 3781-3791.
102. Monteiro S, Roque S, de Sa-Calcada D, Sousa N, Correia-Neves M, Cerqueira JJ(2015). An efficient chronic unpredictable stress protocol to induce stress-relatedresponses in C57BL/6 mice. Front Psychiatry 6: 6.
103. Nair A, Bonneau RH (2006). Stress-induced elevation of glucocorticoids increasesmicroglia proliferation through NMDA receptor activation. J Neuroimmunol 171:72-85.
104. Nie YC, Han YC, Zou YR (2008). CXCR4 is required for the quiescence of primitivehematopoietic cells. J Exp Med 205: 777-783.
105. O'Carroll SJ, Kho DT, Wiltshire R, Nelson V, Rotimi O, Johnson R, et al. (2015). ProinflammatoryTNFalpha and IL-1beta differentially regulate the inflammatoryphenotype of brain microvascular endothelial cells. J Neuroinflammation 12: 131.
106. O'Connor KA, Hansen MK, Pugh CR, Deak MM, Biedenkapp JC, Milligan ED, et al.(2003a). Further characterization of high mobility group box 1 (HMGB1) as aproinflammatory cytokine: central nervous system effects. Cytokine 24: 254-265.
107. O'Connor KA, Johnson JD, Hansen MK, Wieseler Frank JL, Maksimova E,Watkins LR, et al. (2003b). Peripheral and central proinflammatory cytokineresponse to a severe acute stressor. Brain Res 991: 123-132.
108. Pan Y, Chen XY, Zhang QY, Kong LD (2014). Microglial NLRP3 inflammasomeactivation mediates IL-1beta-related inflammation in prefrontal cortex ofdepressive rats. Brain Behav Immun 41: 90-100.
109. Powell ND, Bailey MT, Mays JW, Stiner-Jones LM, Hanke ML, Padgett DA, et al.(2009). Repeated social defeat activates dendritic cells and enhances Toll-likereceptor dependent cytokine secretion. Brain Behav Immun 23: 225-231.
110. Powell ND, Sloan EK, Bailey MT, Arevalo JM, Miller GE, Chen E, et al. (2013). Socialstress up-regulates inflammatory gene expression in the leukocyte transcriptomevia beta-adrenergic induction of myelopoiesis. Proc Natl Acad Sci USA 110:16574-16579.
111. Pradeu T, Cooper EL (2012). The danger theory: 20 years later. Front Immunol 3:287.
112. Quan N, Avitsur R, Stark JL, He LL, Lai WM, Dhabhar F, et al. (2003). Molecularmechanisms of glucocorticoid resistance in splenocytes of socially stressedmale mice. J Neuroimmunol 137: 51-58.
113. Quan N, Banks WA (2007). Brain-immune communication pathways. Brain BehavImmun 21: 727-735.
114. Raison CL, Capuron L, Miller AH (2006). Cytokines sing the blues: inflammation andthe pathogenesis of depression. Trends Immunol 27: 24-31.
115. Ramirez K, Niraula A, Sheridan JF (2015a). GABAergic modulation with classicalbenzodiazepines prevent stress-induced neuro-immune dysregulation andbehavioral alterations. Brain Behav Immun 51: 154-168.
116. Ramirez K, Shea DT, McKim DB, Reader BF, Sheridan JF (2015b). Imipramineattenuates neuroinflammatory signaling and reverses stress-induced socialavoidance. Brain Behav Immun 46: 212-220.
117. Ransohoff RM, Cardona AE (2010). The myeloid cells of the central nervous systemparenchyma. Nature 468: 253-262.
118. Ransohoff RM, Kivisakk P, Kidd G (2003). Three or more routes for leukocytemigration into the central nervous system. Nat Rev Immunol 3: 569-581.
119. Reader BF, Jarrett BL, McKim DB, Wohleb ES, Godbout JP, Sheridan JF (2015).Peripheral and central effects of repeated social defeat stress: monocytetrafficking, microglial activation, and anxiety. Neuroscience 289: 429-442.
120. Rose S, Misharin A, Perlman H (2012). A novel Ly6C/Ly6G-based strategy toanalyze the mouse splenic myeloid compartment. Cytometry A 81A: 343-350.
121. Saederup N, Cardona AE, Croft K, Mizutani M, Cotleur AC, Tsou CL, et al. (2010).Selective chemokine receptor usage by central nervous system myeloid cells inCCR2-red fluorescent protein knock-in mice. PLoS One 5: e13693.
122. Sawicki CM, McKim DB, Wohleb ES, Jarrett BL, Reader BF, Norden DM, et al. (2015).Social defeat promotes a reactive endothelium in a brain region-dependentmanner with increased expression of key adhesion molecules, selectins andchemokines associated with the recruitment of myeloid cells to the brain.Neuroscience 302: 151-164.
123. Segerstrom SC, Miller GE (2004). Psychological stress and the human immunesystem: a meta-analytic study of 30 years of inquiry. Psychol Bull 130: 601-630.
124. Serbina NV, Jia T, Hohl TM, Pamere EG (2008). Monocyte-mediated defenseagainst microbial pathogens. Annu Rev Immunol 26: 421-452.
125. Setiawan E, Wilson AA, Mizrahi R, Rusjan PM, Miler L, Rajkowska G, et al. (2015).Role of translocator protein density, a marker of neuroinflammation, in the brainduring major depressive episodes. JAMA Psychiatry 72: 268-275.
126. Smith RS (1991). The macrophage theory of depression. Med Hypotheses 35:298-306.
127. Sood AK, Bhatty R, Kamat AA, Landen CN, Han L, Thaker PH, et al. (2006).Stress hormone-mediated invasion of ovarian cancer cells. Clin Cancer Res 12:369-375.
128. Stamatovic SM, Keep RF, Andjelkovic AV (2008). Brain endothelial cell-cell junctions:how to 'Open' the blood brain barrier. Curr Neuropharmacol 6: 179-192.
129. Stark JL, Avitsur R, Padgett DA, Campbell KA, Beck FM, Sheridan JF (2001). Socialstress induces glucocorticoid resistance in macrophages. Am J Physiol RegulIntegr Comp Physiol 280: R1799-R1805.
130. Torres-Platas SG, Cruceanu C, Chen GG, Turecki G, Mechawar N (2014). Evidencefor increased microglial priming and macrophage recruitment in the dorsal anteriorcingulate white matter of depressed suicides. Brain Behav Immun 42: 50-59.
131. Tseng RJ, Padgett DA, Dhabhar FS, Engler H, Sheridan JF (2005). Stress-inducedmodulation of NK activity during influenza viral infection: role of glucocorticoidsand opioids. Brain Behav Immun 19: 153-164.
132. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, et al. (2007).Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrowand recruitment to inflammatory sites. J Clin Invest 117: 902-909.
133. Tynan RJ, Naicker S, Hinwood M, Nalivaiko E, Buller KM, Pow DV, et al. (2010).Chronic stress alters the density and morphology of microglia in a subset ofstress-responsive brain regions. Brain Behav Immun 24: 1058-1068.
134. Ulrich-Lai YM, Herman JP (2009). Neural regulation of endocrine and autonomicstress responses. Nat Rev Neurosci 10: 397-409.
135. Vallieres L, Rivest S (1999). Interleukin-6 is a needed proinflammatory cytokine in theprolonged neural activity and transcriptional activation of corticotropin-releasingfactor during endotoxemia. Endocrinology 140: 3890-3903.
136. Weber MD, Frank MG, Sobesky JL, Watkins LR, Maier SF (2013). Blocking toll-likereceptor 2 and 4 signaling during a stressor prevents stress-induced priming ofneuroinflammatory responses to a subsequent immune challenge. Brain BehavImmun. 32: 112-121.
137. Weber MD, Frank MG, Tracey KJ, Watkins LR, Maier SF (2015). Stress induces thedanger-associated molecular pattern HMGB-1 in the hippocampus of maleSprague Dawley Rats: a priming stimulus of microglia and the NLRP3inflammasome. J Neurosci 35: 316-324.
138. Wohleb ES, Fenn AM, Pacenta AM, Powell ND, Sheridan JF, Godbout JP (2012).Peripheral innate immune challenge exaggerated microglia activation, increasedthe number of inflammatory CNS macrophages, and prolonged social withdrawalin socially defeated mice. Psychoneuroendocrinology 37: 1491-1505.
139. Wohleb ES, Hanke ML, Corona AW, Powell ND, Stiner LM, Bailey MT, et al. (2011).beta-Adrenergic receptor antagonism prevents anxiety-like behavior andmicroglial reactivity induced by repeated social defeat. J Neurosci 31:6277-6288.
140. Wohleb ES, McKim DB, Shea DT, Powell ND, Tarr AJ, Sheridan JF, et al. (2014a). Reestablishmentof anxiety in stress-sensitized mice is caused by monocytetrafficking from the spleen to the brain. Biol Psychiatry 75: 970-981.
141. Wohleb ES, Patterson JM, Sharma V, Quan N, Godbout JP, Sheridan JF (2014b).Knockdown of interleukin-1 receptor type-1 on endothelial cells attenuatedstress-induced neuroinflammation and prevented anxiety-like behavior.J Neurosci 34: 2583-2591.
142. Wohleb ES, Powell ND, Godbout JP, Sheridan JF (2013). Stress-inducedrecruitment of bone marrow-derived monocytes to the brain promotes anxietylikebehavior. J Neurosci 33: 13820-13833.
143. Xiang M, Shi X, Li Y, Xu J, Yin L, Xiao G, et al. (2011). Hemorrhagic shock activation ofNLRP3 inflammasome in lung endothelial cells. J Immunol 187: 4809-4817.
144. Yang EV, Sood AK, Chen M, Li Y, Eubank TD, Marsh CB, et al. (2006).Norepinephrine up-regulates the expression of vascular endothelial growth factor,matrix metalloproteinase (MMP)-2, and MMP-9 in nasopharyngeal carcinomatumor cells. Cancer Res 66: 10357-10364.
145. Yang H, Ochani M, Li J, Qiang X, Tanovic M, Harris HE, et al. (2004). Reversingestablished sepsis with antagonists of endogenous high-mobility group box 1.Proc Natl Acad Sci USA 101: 296-301.
146. Yang H, Tracey KJ (2009). Targeting HMGB1 in inflammation. Biochim Biophys Acta1799: 149-156.
147. Yang H, Wang H, Czura CJ, Tracey KJ (2005). The cytokine activity of HMGB1.J Leukoc Biol 78: 1-8.
148. Yang J, Zhang L, Yu C, Yang XF, Wang H (2014). Monocyte and macrophagedifferentiation: circulation inflammatory monocyte as biomarker for inflammatorydiseases. Biomark Res 2: 1.
149. Zhou H, Andonegui G, Wong CHY, Kubes P (2009). Role of endothelial TLR4 forneutrophil recruitment into central nervous system microvessels in systemicinflammation. J Immunol 183: 5244-5250.