Neuroimmune and neuroendocrine abnormalities in depression: Two sides of the same coin

Annals of the New York Academy of Sciences

Volumn 1351, Issue 1, 2015, Pages 68-79

  Horowitz, Mark A ^a   Zunszain, Patricia A ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Cytokines; Glucocorticoid resistance; HPA axis; Inflammation; Stress

Indexed keywords

CYTOKINE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CHRONIC STRESS; CYTOKINE RELEASE; DEPRESSION; EX VIVO STUDY; HORMONE RESISTANCE; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOPATHOGENESIS; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NEUROENDOCRINE DISEASE; NEUROENDOCRINE SYSTEM; NEUROIMMUNOLOGY; NEUROPATHOLOGY; NONHUMAN; SIGNAL TRANSDUCTION; STRESS; ANIMAL; BLOOD; IMMUNOLOGY; IMMUNOMODULATION; INFLAMMATION; MAJOR DEPRESSION; MENTAL STRESS; METABOLISM; NEUROSECRETION; PATHOPHYSIOLOGY;

ANIMALS; CYTOKINES; DEPRESSION; DEPRESSIVE DISORDER, MAJOR; GLUCOCORTICOIDS; HUMANS; HYDROCORTISONE; IMMUNITY, INNATE; INFLAMMATION; NEUROIMMUNOMODULATION; NEUROSECRETORY SYSTEMS; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL;

EID: 84942079455     PISSN: 00778923     EISSN: 17496632     Source Type: Journal    
DOI: 10.1111/nyas.12781     Document Type: Article

References (79)

1. Cohen, S., D. Janicki-Deverts & G. Miller 2007. Psychological stress and disease. JAMA 298: 1685-1687.
2. Pariante, C.M.C. & S.L. Lightman 2008. The HPA axis in major depression: classical theories and new developments. Trends Neurosci. 31: 464-468.
3. Holsboer, F. 2000. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 23: 477-501.
4. Miller, A.H., V. Maletic & C.L. Raison 2009. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 65: 732-741.
5. Dowlati, Y., N. Herrmann, W. Swardfager, et al. 2010. A meta-analysis of cytokines in major depression. Biol. Psychiatry 67: 446-457.
6. Kudielka, B.M., A. Buske-Kirschbaum, D.H. Hellhammer & C. Kirschbaum 2004. HPA axis responses to laboratory psychosocial stress in healthy elderly adults, younger adults, and children: impact of age and gender. Psychoneuroendocrinology 29: 83-98.
7. Pariante, C.M. 2009. Risk factors for development of depression and psychosis. Glucocorticoid receptors and pituitary implications for treatment with antidepressant and glucocorticoids. Ann. N.Y. Acad. Sci. 1179: 144-152.
8. Juruena, M.F., A.J. Cleare, A.S. Papadopoulos, et al. 2006. Different responses to dexamethasone and prednisolone in the same depressed patients. Psychopharmacology (Berl) 189: 225-235.
9. Burke, H.M., M.C. Davis, C. Otte & D.C. Mohr 2005. Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology 30: 846-856.
10. Pariante, C.M.C. & A.H. Miller 2001. Glucocorticoid receptors in major depression: relevance to pathophysiology and treatment. Biol. Psychiatry 49: 391-404.
11. Pace, T.W.W. & A.H. Miller 2009. Cytokines and glucocorticoid receptor signaling. Relevance to major depression. Ann. N.Y. Acad. Sci. 1179: 86-105.
12. Anacker, C., P.A. Zunszain, L.A. Carvalho & C.M. Pariante 2011. The glucocorticoid receptor: Pivot of depression and of antidepressant treatment? Psychoneuroendocrinology 36: 415-425.
13. Miller, G.E., S. Cohen & A.K. Ritchey 2002. Chronic psychological stress and the regulation of pro-inflammatory cytokines: a glucocorticoid-resistance model. Heal. Psychol. 21: 531-541.
14. Menke, A., J. Arloth, B. Putz, et al. 2012. Dexamethasone stimulated gene expression in peripheral blood is a sensitive marker for glucocorticoid receptor resistance in depressed patients. Neuropsychopharmacology 37: 1455-1464.
15. Raison, C.L. & A.H. Miller 2003. When not enough is too much: the role of insufficient glucocorticoid signaling in the pathophysiology of stress-related disorders. Am. J. Psychiatry 160: 1554-1565.
16. Herbert, J., I.M. Goodyer, A.B. Grossman, et al. 2006. Do corticosteroids damage the brain? J. Neuroendocrinol. 18: 393-411.
17. Dantzer, R., J.C. O'Connor, G.G. Freund, et al. 2008. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9: 46-56.
18. Howren, M., D. Lamkin & J. Suls 2009. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom. Med. 186: 171-186.
19. Maes, M. 1999. Major depression and activation of the inflammatory response system. In Cytokines, Stress, and Depression: 25-46. New York: Springer.
20. Zunszain, P.A., N. Hepgul & C.M. Pariante 2013. Inflammation and depression. Curr. Top. Behav. Neurosci. 14: 135-151.
21. Bellavance, M. & S. Rivest 2014. The HPA-immune axis and the immunomodulatory actions of glucocorticoids in the brain. Front. Immunol. 5: 1-13.
22. Zunszain, P.A., C. Anacker, A. Cattaneo, et al. 2011. Glucocorticoids, cytokines and brain abnormalities in depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 35: 722-729.
23. Silverman, M.N. & E.M. Sternberg 2012. Glucocorticoid regulation of inflammation and its functional correlates: from HPA axis to glucocorticoid receptor dysfunction. Ann. N.Y. Acad. Sci. 1261: 55-63.
24. Cohen, S., D. Janicki-Deverts, W.J. Doyle, et al. 2012. Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk. Proc. Natl. Acad. Sci. 109: 5995-5999.
25. Miller, A.H. 2008. Inflammation versus glucocorticoids as purveyors of pathology during stress: have we reached the tipping point? Biol. Psychiatry 64: 263-265.
26. Pace, T.W.W., F. Hu & A.H. Miller 2007. Cytokine-Effects on glucocorticoid receptor function: relevance to glucocorticoid resistance and the pathophysiology and treatment of major depression. Brain Behav. Immun. 21: 9-19.
27. Avitsur, R., J.L. Stark & J.F. Sheridan 2001. Social stress induces glucocorticoid resistance in subordinate animals. Horm. Behav. 39: 247-257.
28. De Bosscher, K., W. Vanden Berghe & G. Haegeman 2003. The Interplay between the glucocorticoid receptor and nuclear factor-κB or activator protein-1: molecular mechanisms for gene repression. Endocr. Rev. 24: 488-522.
29. Drew, P.D. & J.A. Chavis 2000. Inhibition of microglial cell activation by cortisol. Brain Res. Bull. 52: 391-396.
30. Tanaka, J., H. Fujita, S. Matsuda, et al. 1997. Glucocorticoid- and mineralocorticoid receptors in microglial cells: the two receptors mediate differential effects of corticosteroids. Glia 20: 23-37.
31. Miller, G.E., E. Chen, J. Sze, et al. 2008. A functional genomic fingerprint of chronic stress in humans: blunted glucocorticoid and increased NF-kappaB signaling. Biol. Psychiatry 64: 266-272.
32. Cole, S.W. 2008. Social regulation of leukocyte homeostasis: the role of glucocorticoid sensitivity. Brain. Behav. Immun. 22: 1049-1055.
33. Miller, G.E., E. Chen, A.K. Fok, et al. 2009. Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc. Natl. Acad. Sci. U. S. A. 106: 14716-14721.
34. Sheridan, J.F., J.L. Stark, R. Avitsur & D.A. Padgett 2000. Social disruption, immunity, and susceptibility to viral infection. Role of glucocorticoid insensitivity and NGF. Ann. N.Y. Acad. Sci. 917: 894-905.
35. Wirtz, P.H., R. Von Känel, P. Schnorpfeil, et al. 2003. Re-duced glucocorticoid sensitivity of monocyte interleukin-6 production in male industrial employees who are vitally exhausted. Psychosom. Med. 65: 672-678.
36. Avitsur, R., N. Powell, D.A. Padgett & J.F. Sheridan 2009. Social interactions, stress, and immunity. Immunol. Allergy Clin. North Am. 29: 285-293.
37. Landmann, R., B. Schaub, S. Link & H.R. Wacker 1997. Unaltered monocyte function in patients with major depression before and after three months of antidepressive therapy. Biol. Psychiatry 41: 675-681.
38. Bauer, E., A. Papadopoulos, L. Poon, et al. 2003. Altered glucocorticoid immunoregulation in treatment resistant depression. Psychoneuroendocrinology 28: 49-65.
39. Lisi, L., G. Camardese, M. Treglia, et al. 2013. Monocytes from depressed patients display an altered pattern of response to endotoxin challenge. PLoS One 8: e52585.
40. Maes, M., E. Bosmans, H.Y. Meltzer, S. Scharpe & E. Suy 1993. Interleukin 1B: a putative mediator of HPA axis hyperacticity in major depression? Am. J. Psychiatry 150: 1189-1193.
41. Maes, M., S. Scharpe, H.Y. Meltzer, et al. 1993. Relationships between interleukin-6 activity, acute phase proteins, and function of the hypothalamic-pituitary-adrenal axis in severe depression. Psychiatry Res. 49: 11-27.
42. Fitzgerald, P., S.M.S.S.M. O'Brien, P. Scully, et al. 2006. Cutaneous glucocorticoid receptor sensitivity and pro-inflammatory cytokine levels in antidepressant-resistant depression. Psychol. Med. 36: 37-43.
43. Carvalho, L.A., M.F. Juruena, A.S. Papadopoulos, et al. 2008. Clomipramine in vitro reduces glucocorticoid receptor function in healthy subjects but not in patients with major depression. Neuropsychopharmacology 33: 3182-3189.
44. Humphreys, D., L. Schlesinger, M. Lopez & A.V. Araya 2006. Interleukin-6 production and deregulation of the hypothalamic - pituitary - adrenal axis in patients with major depressive disorders. Endocrine 30: 371-376.
45. Ising, M., H.E. Künzel, E.B. Binder, et al. 2005. The combined dexamethasone/CRH test as a potential surrogate marker in depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 29: 1085-1093.
46. Sorrells, S.F., J.R. Caso, C.D. Munhoz & R.M. Sapolsky 2009. The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 64: 33-39.
47. Frank, M.G., L.R. Watkins & S.F. Maier 2013. Stress-induced glucocorticoids as a neuroendocrine alarm signal of danger. Brain. Behav. Immun. 33: 1-6.
48. Tynan, R.J., S. Naicker, M. Hinwood, et al. 2010. Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions. Brain Behav. Immun. 24: 1058-1068.
49. Nair, A. & R.H. Bonneau 2006. Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J. Neuroimmunol. 171: 72-85.
50. Blandino Jr., P., C.J. Barnum & T. Deak 2006. The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1β responses to stress. J. Neuroimmunol. 173: 87-95.
51. Goujon, E., P. Parnet, S. Laye, et al. 1995. Stress downregulates lipopolysaccharide-induced expression of proinflammatory cytokines in the spleen, pituitary, and brain of mice. Brain Behav. Immun. 9: 292-303.
52. Johnson, J., K. O'Connor, T. Deak & M. Stark 2002. Prior stressor exposure sensitizes LPS-induced cytokine production. Brain Behav. Immun. 476: 461-476.
53. Argu, S., A.J. Herrera, J.L. Venero, et al. 2006. Stress increases vulnerability to inflammation in the rat prefrontal cortex. J. Neurosci. 26: 5709-5719.
54. Espinosa-Oliva, A.M., R.M. de Pablos, R.F. Villarán, et al. 2011. Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol. Aging 32: 85-102.
55. Frank, M.G., Z.D. Miguel, L.R. Watkins & S.F. Maier 2010. Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain Behav. Immun. 24: 19-30.
56. Munhoz, C.D., L.B. Lepsch, E.M. Kawamoto, et al. 2006. Chr-onic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-kappaB in the frontal cortex and hippocampus via glucocorticoid secretion. J. Neurosci. 26: 3813-3820.
57. Munhoz, C.D., S.F. Sorrells, J.R. Caso, et al. 2010. Glucocorticoids exacerbate lipopolysaccharide-induced signaling in the frontal cortex and hippocampus in a dose-dependent manner. J. Neurosci. 30: 13690-13698.
58. Smyth, G.P., P.P. Stapleton, D. Ph, et al. 2004. Glucocorticoid pretreatment induces cytokine overexpression and nuclear factor- B activation in macrophages. J. Surg. Res. 261: 253-261.
59. Barber, A.E., S.M. Coyle, M.A. Marano, et al. 1993. Glucocorticoid therapy alters hormonal and cytokine responses to endotoxin in man. J. Immunol. 150: 1999-2006.
60. Yeager, M., P. Pioli & P. Guyre 2011. Cortisol exerts bi-phasic regulation of inflammation in humans. Dose-Response 1949: 332-347.
61. Zhang, T. & R.A. Daynes 2007. Macrophages from 11β-hydroxysteroid dehydrogenase type 1-deficient mice exhibit an increased sensitivity to lipopolysaccharide stimulation due to TGF-β-mediated up-regulation of SHIP1 expression. J. Immunol. 179: 6325-6335.
62. Frank, M.G.M., B.M.B. Thompson, L.R.L. Watkins & S.F. Maier 2011. Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses. Brain Behav. Immun. 26: 337-345.
63. Wiegers, G.J. & J.M.H.M. Reul 1998. Induction of cytokine receptors by glucocorticoids: functional and pathological significance. Trends Pharmacol. Sci. 19: 317-321.
64. Re, F., M. Muzio, M. De Rossi, et al. 1994. The type II "receptor" as a decoy target for interleukin 1 in polymorphonuclear leukocytes: characterization of induction by dexamethasone and ligand binding properties of the released decoy receptor. J. Exp. Med. 179: 739-743.
65. Yeager, M.P., P.M. Guyre & A.U. Munck 2004. Glucocorticoid regulation of the inflammatory response to injury. Acta Anaesthesiol. Scand. 48: 799-813.
66. Horowitz, M.A., P.A. Zunszain, C. Anacker, et al. 2013. Glucocorticoids and inflammation: a double-headed sword in depression? Mod. Trends Pharmacopsychiatry 28: 127-143.
67. Busillo, J. & K. Azzam 2011. Glucocorticoids sensitize the innate immune system through regulation of the NLRP3 inflammasome. J. Biol. Chem. 286: 38703-38713.
68. Walker, F.R., M. Nilsson & K. Jones 2013. Acute and chronic stress-induced disturbances of microglial plasticity, phenotype and function. Curr. Drug Targets 14: 1262-1276.
69. Kawai, T. & S. Akira 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11: 373-384.
70. Aravalli, R., P. Peterson & J. Lokensgard 2007. Toll-like receptors in defense and damage of the central nervous system. J. Neuroimmune Pharmacol. 2: 297-312.
71. Hornung, V. & E. Latz 2010. Critical functions of priming and lysosomal damage for NLRP3 activation. Eur. J. Immunol. 40: 620-623.
72. Woodcock, T. & C. Morganti-Kossmann 2013. The role of markers of inflammation in traumatic brain injury. Front. Neurol. 4: 18.
73. Wu, C., F. Li, G. Niu & X. Chen 2013. PET imaging of inflammation biomarkers. Theranostics 3: 448-466.
74. Barnum, C.J., T.W.W. Pace, F. Hu, et al. 2012. Psychological stress in adolescent and adult mice increases neuroinflammation and attenuates the response to LPS challenge. J. Neuroinflammation 9: 9.
75. Ulrich-Lai, Y.M. & J.P. Herman 2009. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 10: 397-409.
76. Miller, A.H. 2007. Letter to the editor Re: "An inflammatory review of glucocorticoids in the CNS" by Sorrells et al. Brain, Behavior and Immunity 21, 259-272, 2007. Brain Behav. Immun. 21: 988-989.
77. Sorrells, S.F. & R.M. Sapolsky 2007. Reply to letter to the editor Re: "An inflammatory review of glucocorticoids in the CNS" by Sorrells et al. Brain, Behavior, and Immunity 21:259-272, 2007. Brain Behav. Immun. 21: 990.
78. Zunszain, P., C. Anacker, A. Cattaneo, et al. 2012. Interleukin-1β: a new regulator of the kynurenine pathway affecting human hippocampal neurogenesis. Neuropsychopharmacology 37: 939-949.
79. Horowitz, M.A., J. Wertz, D. Zhu, et al. 2014. Antidepressant compounds can be both pro- and anti-inflammatory in human hippocampal cells. Int. J. Neuropsychopharmacol. 18.