Stress-induced neuroinflammatory priming: A liability factor in the etiology of psychiatric disorders

Neurobiology of Stress

Volumn 4, Issue , 2016, Pages 62-70

  Frank, Matthew G ^a   Weber, Michael D ^b   Watkins, Linda R ^a   Maier, Steven F ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Glucocorticoids; HMGB 1; Microglia; Neuroinflammation; Priming; Stress

Indexed keywords

CELL NUCLEUS DNA; CHEMOKINE RECEPTOR CXCR4; CORTICOSTERONE; CRYOPYRIN; CYSTEINE; CYTOKINE RECEPTOR; DISULFIDE; DNA BINDING PROTEIN; GLUCOCORTICOID; HEAT SHOCK PROTEIN; HIGH MOBILITY GROUP B PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOGEN ACTIVATED PROTEIN KINASE 3; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PATTERN RECOGNITION RECEPTOR; PROTEIN S 100; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR;

CELL ACTIVATION; CELL FUNCTION; CENTRAL NERVOUS SYSTEM; FEAR CONDITIONING TEST; HIPPOCAMPUS; ILLNESS BEHAVIOR; IMMUNOSURVEILLANCE; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MACROPHAGE; MAJOR DEPRESSION; MENTAL DISEASE; MICROGLIA; MONONUCLEAR PHAGOCYTE; MOOD DISORDER; NERVOUS SYSTEM INFLAMMATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STRESS;

EID: 84952361750     PISSN: None     EISSN: 23522895     Source Type: Journal    
DOI: 10.1016/j.ynstr.2015.12.004     Document Type: Review

References (93)

1. Albus, C., Psychological and social factors in coronary heart disease. Ann. Med. 42 (2010), 487–494.
2. Aloisi, F., Immune function of microglia. Glia 36 (2001), 165–179.
3. Antoine, D.J., Harris, H.E., Andersson, U., Tracey, K.J., Bianchi, M.E., A systematic nomenclature for the redox states of high mobility group box (HMGB) proteins. Mol. Med. 20 (2014), 135–137.
4. Aravalli, R.N., Peterson, P.K., Lokensgard, J.R., Toll-like receptors in defense and damage of the central nervous system. J. Neuroimmune Pharmacol. 2 (2007), 297–312.
5. Banks, W.A., The blood-brain barrier in neuroimmunology: tales of separation and assimilation. Brain Behav. Immun. 44 (2015), 1–8.
6. Barton, G.M., Kagan, J.C., A cell biological view of toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 9 (2009), 535–542.
7. Basu, A., Krady, J.K., Levison, S.W., Interleukin-1: a master regulator of neuroinflammation. J. Neurosci. Res. 78 (2004), 151–156.
8. Bianchi, M.E., DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol. 81 (2007), 1–5.
9. Bianchi, M.E., Manfredi, A.A., Immunology. Dangers in and out. Science 323 (2009), 1683–1684.
10. Blandino, P. Jr., 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. 23 (2009), 958–968.
11. Bonaldi, T., Talamo, F., Scaffidi, P., Ferrera, D., Porto, A., Bachi, A., Rubartelli, A., Agresti, A., Bianchi, M.E., Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 22 (2003), 5551–5560.
12. Boumpas, D.T., Chrousos, G.P., Wilder, R.L., Cupps, T.R., Balow, J.E., Glucocorticoid therapy for immune-mediated diseases: basic and clinical correlates. Ann. Intern. Med. 119 (1993), 1198–1208.
13. Busillo, J.M., Azzam, K.M., Cidlowski, J.A., Glucocorticoids sensitize the innate immune system through regulation of the NLRP3 inflammasome. J. Biol. Chem. 286 (2011), 38703–38713.
14. Busillo, J.M., Cidlowski, J.A., The five Rs of glucocorticoid action during inflammation: ready, reinforce, repress, resolve, and restore. Trends Endocrinol. Metab. 24 (2013), 109–119.
15. Carpentier, P.A., Duncan, D.S., Miller, S.D., Glial toll-like receptor signaling in central nervous system infection and autoimmunity. Brain Behav. Immun. 22 (2008), 140–147.
16. Chen, G.Y., Nunez, G., Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10 (2010), 826–837.
17. Christianson, J.P., Paul, E.D., Irani, M., Thompson, B.M., Kubala, K.H., Yirmiya, R., Watkins, L.R., Maier, S.F., The role of prior stressor controllability and the dorsal raphe nucleus in sucrose preference and social exploration. Behav. Brain Res. 193 (2008), 87–93.
18. Dantzer, R., Cytokine, sickness behavior, and depression. Immunol. Allergy Clin. North Am. 29 (2009), 247–264.
19. 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. 9 (2008), 46–56.
20. de Pablos, R.M., Herrera, A.J., Espinosa-Oliva, A.M., Sarmiento, M., Munoz, M.F., Machado, A., Venero, J.L., Chronic stress enhances microglia activation and exacerbates death of nigral dopaminergic neurons under conditions of inflammation. J. Neuroinflamm., 11, 2014, 34.
21. de Pablos, R.M., Villaran, R.F., Arguelles, S., Herrera, A.J., Venero, J.L., Ayala, A., Cano, J., Machado, A., Stress increases vulnerability to inflammation in the rat prefrontal cortex. J. Neurosci. 26 (2006), 5709–5719.
22. Dinarello, C.A., A clinical perspective of IL-1beta as the gatekeeper of inflammation. Eur. J. Immunol. 41 (2011), 1203–1217.
23. Ehtesham, M., Min, E., Issar, N.M., Kasl, R.A., Khan, I.S., Thompson, R.C., The role of the CXCR4 cell surface chemokine receptor in glioma biology. J. Neuro Oncol. 113 (2013), 153–162.
24. Espinosa-Oliva, A.M., de Pablos, R.M., Villaran, R.F., Arguelles, 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 32 (2011), 85–102.
25. Fang, P., Schachner, M., Shen, Y.Q., HMGB1 in development and diseases of the central nervous system. Mol. Neurobiol. 45 (2012), 499–506.
26. Fleshner, M., Deak, T., Spencer, R.L., Laudenslager, M.L., Watkins, L.R., Maier, S.F., A long-term increase in basal levels of corticosterone and a decrease in corticosteroid-binding globulin after acute stressor exposure. Endocrinology 136 (1995), 5336–5342.
27. 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. 21 (2007), 47–59.
28. 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 40 (2014), 191–200.
29. Frank, M.G., Miguel, Z.D., Watkins, L.R., Maier, S.F., Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain Behav. Immun. 24 (2010), 19–30.
30. Frank, M.G., Thompson, B.M., Watkins, L.R., Maier, S.F., Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses. Brain, Behav. Immun. 26 (2012), 337–345.
31. Frank, M.G., Watkins, L.R., Maier, S.F., Stress-induced glucocorticoids as a neuroendocrine alarm signal of danger. Brain Behav. Immun. 33 (2013), 1–6.
32. Frank, M.G., Watkins, L.R., Maier, S.F., The permissive role of glucocorticoids in neuroinflammatory priming: mechanisms and insights. Curr. Opin. Endocrinol. Diabetes Obes. 22 (2015), 300–305.
33. 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. 48 (2015), 1–7.
34. Frank, M.G., Wieseler-Frank, J.L., Watkins, L.R., Maier, S.F., Rapid isolation of highly enriched and quiescent microglia from adult rat hippocampus: immunophenotypic and functional characteristics. J. Neurosci. Methods 151 (2006), 121–130.
35. Goshen, I., Yirmiya, R., Interleukin-1 (IL-1): a central regulator of stress responses. Front. Neuroendocrinol. 30 (2009), 30–45.
36. Graeber, M.B., Li, W., Rodriguez, M.L., Role of microglia in CNS inflammation. FEBS Lett. 585 (2011), 3798–3805.
37. Hammen, C., Stress and depression. Annu. Rev. Clin. Psychol. 1 (2005), 293–319.
38. Hanke, M.L., Powell, N.D., Stiner, L.M., Bailey, M.T., Sheridan, J.F., Beta adrenergic blockade decreases the immunomodulatory effects of social disruption stress. Brain Behav. Immun. 26 (2012), 1150–1159.
39. Hornung, V., Latz, E., Critical functions of priming and lysosomal damage for NLRP3 activation. Eur. J. Immunol. 40 (2010), 620–623.
40. Janeway, C.A. Jr., Medzhitov, R., Innate immune recognition. Annu. Rev. Immunol. 20 (2002), 197–216.
41. Johnson, J.D., Campisi, J., Sharkey, C.M., Kennedy, S.L., Nickerson, M., Greenwood, B.N., Fleshner, M., Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience 135 (2005), 1295–1307.
42. 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. 16 (2002), 461–476.
43. 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. 284 (2003), R422–R432.
44. Johnson, J.D., O'Connor, K.A., Watkins, L.R., Maier, S.F., The role of IL-1beta in stress-induced sensitization of proinflammatory cytokine and corticosterone responses. Neuroscience 127 (2004), 569–577.
45. Jones, K.A., Thomsen, C., The role of the innate immune system in psychiatric disorders. Mol. Cell. Neurosci. 53 (2013), 52–62.
46. Kang, R., Chen, R., Zhang, Q., Hou, W., Wu, S., Cao, L., Huang, J., Yu, Y., Fan, X.G., Yan, Z., Sun, X., Wang, H., Wang, Q., Tsung, A., Billiar, T.R., Zeh, H.J. 3rd, Lotze, M.T., Tang, D., HMGB1 in health and disease. Mol. Asp. Med. 40 (2014), 1–116.
47. Katsumoto, A., Lu, H., Miranda, A.S., Ransohoff, R.M., Ontogeny and functions of central nervous system macrophages. J. Immunol. 193 (2014), 2615–2621.
48. Kawai, T., Akira, S., Signaling to NF-kappaB by Toll-like receptors. Trends Mol. Med. 13 (2007), 460–469.
49. Kawai, T., Akira, S., The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11 (2010), 373–384.
50. Kessler, R.C., The effects of stressful life events on depression. Annu. Rev. Psychol. 48 (1997), 191–214.
51. Kumar, H., Kawai, T., Akira, S., Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30 (2011), 16–34.
52. Latz, E., Xiao, T.S., Stutz, A., Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13 (2013), 397–411.
53. Leemans, J.C., Cassel, S.L., Sutterwala, F.S., Sensing damage by the NLRP3 inflammasome. Immunol. Rev. 243 (2011), 152–162.
54. Lehnardt, S., Massillon, L., Follett, P., Jensen, F.E., Ratan, R., Volpe, J.J., Vartanian, T., Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 8514–8519.
55. LeMay, L.G., Vander, A.J., Kluger, M.J., The effects of psychological stress on plasma interleukin-6 activity in rats. Physiol. Behav. 47 (1990), 957–961.
56. Liu, B., Xu, C., Wu, X., Liu, F., Du, Y., Sun, J., Tao, J., Dong, J., Icariin exerts an antidepressant effect in an unpredictable chronic mild stress model of depression in rats and is associated with the regulation of hippocampal neuroinflammation. Neuroscience 294 (2015), 193–205.
57. Maier, S.F., Bi-directional immune-brain communication: implications for understanding stress, pain, and cognition. Brain Behav. Immun. 17 (2003), 69–85.
58. Martinon, F., Mayor, A., Tschopp, J., The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27 (2009), 229–265.
59. Maruta, E., Yabuuchi, K., Nishiyori, A., Takami, S., Minami, M., Satoh, M., Beta2-adrenoceptors on the glial cells mediate the induction of interleukin-1beta mRNA in the rat brain. Brain Res. Mol. Brain Res. 49 (1997), 291–294.
60. McCusker, R.H., Kelley, K.W., Immune-neural connections: how the immune system's response to infectious agents influences behavior. J. Exp. Biol. 216 (2013), 84–98.
61. Miller, A.H., Maletic, V., Raison, C.L., Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 65 (2009), 732–741.
62. Mosser, D.M., Edwards, J.P., Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8 (2008), 958–969.
63. Munck, A., Guyre, P.M., Holbrook, N.J., Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev. 5 (1984), 25–44.
64. Munhoz, C.D., Lepsch, L.B., Kawamoto, E.M., Malta, M.B., Lima Lde, S., Avellar, M.C., Sapolsky, R.M., Scavone, C., Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-kappaB in the frontal cortex and hippocampus via glucocorticoid secretion. J. Neurosci. 26 (2006), 3813–3820.
65. Munhoz, C.D., Sorrells, S.F., Caso, J.R., Scavone, C., Sapolsky, R.M., Glucocorticoids exacerbate lipopolysaccharide-induced signaling in the frontal cortex and hippocampus in a dose-dependent manner. J. Neurosci. 30 (2010), 13690–13698.
66. Norden, D.M., Muccigrosso, M.M., Godbout, J.P., Microglial priming and enhanced reactivity to secondary insult in aging, and traumatic CNS injury, and neurodegenerative disease. Neuropharmacology 96 (2015), 29–41.
67. Pan, Y., Chen, X.Y., Zhang, Q.Y., Kong, L.D., Microglial NLRP3 inflammasome activation mediates IL-1beta-related inflammation in prefrontal cortex of depressive rats. Brain Behav. Immun. 41 (2014), 90–100.
68. Perry, V.H., The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav. Immun. 18 (2004), 407–413.
69. Perry, V.H., Cunningham, C., Holmes, C., Systemic infections and inflammation affect chronic neurodegeneration. Nat. Rev. Immunol. 7 (2007), 161–167.
70. Pugh, C.R., Nguyen, K.T., Gonyea, J.L., Fleshner, M., Wakins, L.R., Maier, S.F., Rudy, J.W., Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation. Behav. Brain Res. 106 (1999), 109–118.
71. Raison, C.L., Miller, A.H., Role of inflammation in depression: implications for phenomenology, pathophysiology and treatment. Mod. Trends Pharmacopsychiatry 28 (2013), 33–48.
72. Ransohoff, R.M., Cardona, A.E., The myeloid cells of the central nervous system parenchyma. Nature 468 (2010), 253–262.
73. Ransohoff, R.M., Perry, V.H., Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27 (2009), 119–145.
74. Rivest, S., Regulation of innate immune responses in the brain. Nat. Rev. Immunol. 9 (2009), 429–439.
75. Rutgeerts, P.J., Review article: the limitations of corticosteroid therapy in Crohn's disease. Aliment. Pharmacol. Ther. 15 (2001), 1515–1525.
76. Salminen, A., Huuskonen, J., Ojala, J., Kaarniranta, K., Suuronen, T., Activation of innate immunity system during aging: NF-kB signaling is the molecular culprit of inflamm-aging. Ageing Res. Rev. 7 (2008), 83–105.
77. Sansone, R.A., Sansone, L.A., Depression and cardiovascular disease: just an urban legend?. Psychiatry 5 (2008), 45–48.
78. Scaffidi, P., Misteli, T., Bianchi, M.E., Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418 (2002), 191–195.
79. Schiltz, J.C., Sawchenko, P.E., Signaling the brain in systemic inflammation: the role of perivascular cells. Front. Biosci. 8 (2003), s1321–1329.
80. Schiraldi, M., Raucci, A., Munoz, L.M., Livoti, E., Celona, B., Venereau, E., Apuzzo, T., De Marchis, F., Pedotti, M., Bachi, A., Thelen, M., Varani, L., Mellado, M., Proudfoot, A., Bianchi, M.E., Uguccioni, M., HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4. J. Exp. Med. 209 (2012), 551–563.
81. Schwarz, J.M., Bilbo, S.D., Sex, glia, and development: interactions in health and disease. Horm. Behav. 62 (2012), 243–253.
82. Schwarz, J.M., Sholar, P.W., Bilbo, S.D., Sex differences in microglial colonization of the developing rat brain. J. Neurochem. 120 (2012), 948–963.
83. Sun, S.C., Ganchi, P.A., Ballard, D.W., Greene, W.C., NF-kappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway. Science 259 (1993), 1912–1915.
84. Venereau, E., Casalgrandi, M., Schiraldi, M., Antoine, D.J., Cattaneo, A., De Marchis, F., Liu, J., Antonelli, A., Preti, A., Raeli, L., Shams, S.S., Yang, H., Varani, L., Andersson, U., Tracey, K.J., Bachi, A., Uguccioni, M., Bianchi, M.E., Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J. Exp. Med. 209 (2012), 1519–1528.
85. Venereau, E., Ceriotti, C., Bianchi, M.E., DAMPs from cell death to new life. Front. Immunol., 6, 2015, 422.
86. 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. 32 (2013), 112–121.
87. 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. 35 (2015), 316–324.
88. Webster Marketon, J.I., Glaser, R., Stress hormones and immune function. Cell. Immunol. 252 (2008), 16–26.
89. 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 37 (2012), 1491–1505.
90. Wohleb, E.S., Hanke, M.L., Corona, A.W., Powell, N.D., Stiner, L.M., Bailey, M.T., Nelson, R.J., Godbout, J.P., Sheridan, J.F., beta-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. 31 (2011), 6277–6288.
91. Wohleb, E.S., McKim, D.B., Sheridan, J.F., Godbout, J.P., Monocyte trafficking to the brain with stress and inflammation: a novel axis of immune-to-brain communication that influences mood and behavior. Front. Neurosci., 8, 2014, 447.
92. Xiang, M., Shi, X., Li, Y., Xu, J., Yin, L., Xiao, G., Scott, M.J., Billiar, T.R., Wilson, M.A., Fan, J., Hemorrhagic shock activation of NLRP3 inflammasome in lung endothelial cells. J. Immunol. 187 (2011), 4809–4817.
93. Yang, H., Antoine, D.J., Andersson, U., Tracey, K.J., The many faces of HMGB1: molecular structure-functional activity in inflammation, apoptosis, and chemotaxis. J. Leukoc. Biol. 93 (2013), 865–873.