Re-establishment of anxiety in stress-sensitized mice is caused by monocyte trafficking from the spleen to the brain

Biological Psychiatry

Volumn 75, Issue 12, 2014, Pages 970-981

  Wohleb, Eric S ^a   McKim, Daniel B ^a   Shea, Daniel T ^a   Powell, Nicole D ^a   Tarr, Andrew J ^a   Sheridan, John F ^a   Godbout, Jonathan P ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Anxiety; microglia; monocytes; neuroinflammation; PTSD; stress

Indexed keywords

CD14 ANTIGEN; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; BONE MARROW CELL; BRAIN; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; CYTOKINE PRODUCTION; FOLLOW UP; GENE EXPRESSION; LATENT PERIOD; MACROPHAGE; MALE; MICROGLIA; MONOCYTE; MOUSE; MYELOID PROGENITOR CELL; NERVOUS SYSTEM INFLAMMATION; NEUROIMMUNOLOGY; NONHUMAN; PRIORITY JOURNAL; REPEATED SOCIAL DEFEAT; SOCIAL AVOIDANCE BEHAVIOR; SPLEEN; STRESS; ANIMAL; ANXIETY; CELL MOTION; CENTRAL NERVOUS SYSTEM SENSITIZATION; COMPLICATION; CYTOLOGY; IMMUNOLOGY; MENTAL STRESS; PATHOLOGY; SOCIAL BEHAVIOR; SPLENECTOMY; SURGERY;

ANIMALS; ANXIETY; BRAIN; CELL MOVEMENT; CENTRAL NERVOUS SYSTEM SENSITIZATION; MACROPHAGES; MALE; MICE; MONOCYTES; SOCIAL BEHAVIOR; SPLEEN; SPLENECTOMY; STRESS, PSYCHOLOGICAL;

EID: 84901310699     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.11.029     Document Type: Article

References (64)

1. K.S. Kendler, L.M. Karkowski, and C.A. Prescott Causal relationship between stressful life events and the onset of major depression Am J Psychiatry 156 1999 837 841
2. S.E. Gilman, N.H. Trinh, J.W. Smoller, M. Fava, J.M. Murphy, and J. Breslau Psychosocial stressors and the prognosis of major depression: A test of Axis IV Psychol Med 43 2013 303 316
3. D.S. Charney Psychobiological mechanisms of resilience and vulnerability: Implications for successful adaptation to extreme stress Am J Psychiatry 161 2004 195 216
4. S.J. Mathew, R.B. Price, and D.S. Charney Recent advances in the neurobiology of anxiety disorders: Implications for novel therapeutics Am J Med Genet C Semin Med Genet 148C 2008 89 98
5. R. Dantzer, J.C. OConnor, G.G. Freund, R.W. Johnson, and K.W. Kelley From inflammation to sickness and depression: When the immune system subjugates the brain Nat Rev Neurosci 9 2008 46 56
6. E. Haroon, C.L. Raison, and A.H. Miller Psychoneuroimmunology meets neuropsychopharmacology: Translational implications of the impact of inflammation on behavior Neuropsychopharmacology 37 2012 137 162
7. W. Beumer, S.M. Gibney, R.C. Drexhage, L. Pont-Lezica, J. Doorduin, and H.C. Klein et al. The immune theory of psychiatric diseases: A key role for activated microglia and circulating monocytes J Leukoc Biol 92 2012 959 975
8. A.H. Miller, V. Maletic, and C.L. Raison Inflammation and its discontents: The role of cytokines in the pathophysiology of major depression Biol Psychiatry 65 2009 732 741
9. K. Tanaka, T. Furuyashiki, S. Kitaoka, Y. Senzai, Y. Imoto, and E. Segi-Nishida et al. Prostaglandin E2-mediated attenuation of mesocortical dopaminergic pathway is critical for susceptibility to repeated social defeat stress in mice J Neurosci 32 2012 4319 4329
10. D.J. Christoffel, S.A. Golden, D. Dumitriu, A.J. Robison, W.G. Janssen, and H.F. Ahn et al. IkappaB kinase regulates social defeat stress-induced synaptic and behavioral plasticity J Neurosci 31 2011 314 321
11. J.W. Koo, S.J. Russo, D. Ferguson, E.J. Nestler, and R.S. Duman Nuclear factor-kappaB is a critical mediator of stress-impaired neurogenesis and depressive behavior Proc Natl Acad Sci U S A 107 2010 2669 2674
12. J.W. Koo, and R.S. Duman IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress Proc Natl Acad Sci U S A 105 2008 751 756
13. J.A. Andrews, and K.D. Neises Cells, biomarkers, and post-traumatic stress disorder: Evidence for peripheral involvement in a central disease J Neurochem 120 2012 26 36
14. T.W. Pace, and C.M. Heim A short review on the psychoneuroimmunology of posttraumatic stress disorder: From risk factors to medical comorbidities Brain Behav Immun 25 2012 6 13
15. E.S. Wohleb, N.D. Powell, J.P. Godbout, and J.F. Sheridan Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior J Neurosci 33 2013 13820 13833
16. E.S. Wohleb, M.L. Hanke, A.W. Corona, N.D. Powell, L.M. Stiner, and M.T. Bailey et al. β-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat J Neurosci 31 2011 6277 6288
17. M.L. Hanke, N.D. Powell, L.M. Stiner, M.T. Bailey, and J.F. Sheridan β-adrenergic blockade decreases the immunomodulatory effects of social disruption stress Brain Behav Immun 26 2012 1150 1159
18. S.G. Kinsey, M.T. Bailey, J.F. Sheridan, D.A. Padgett, and R. Avitsur Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice Brain Behav Immun 21 2007 458 466
19. M.T. Bailey, S.G. Kinsey, D.A. Padgett, J.F. Sheridan, and B. Leblebicioglu Social stress enhances IL-1beta and TNF-alpha production by Porphyromonas gingivalis lipopolysaccharide-stimulated CD11b+ cells Physiol Behav 98 2009 351 358
20. H. Engler, A. Engler, M.T. Bailey, and J.F. Sheridan Tissue-specific alterations in the glucocorticoid sensitivity of immune cells following repeated social defeat in mice J Neuroimmunol 163 2005 110 119
21. H. Engler, M.T. Bailey, A. Engler, and J.F. Sheridan Effects of repeated social stress on leukocyte distribution in bone marrow, peripheral blood and spleen J Neuroimmunol 148 2004 106 115
22. R. Avitsur, A. Kavelaars, C. Heijnen, and J.F. Sheridan Social stress and the regulation of tumor necrosis factor-alpha secretion Brain Behav Immun 19 2005 311 317
23. E.S. Wohleb, A.M. Fenn, A.M. Pacenta, N.D. Powell, J.F. Sheridan, and J.P. Godbout 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
24. V. Krishnan, M.H. Han, D.H. Graham, O. Berton, W. Renthal, and S.J. Russo et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions Cell 131 2007 391 404
25. O. Berton, C.A. McClung, R.J. Dileone, V. Krishnan, W. Renthal, and S.J. Russo et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress Science 311 2006 864 868
26. L. Vallieres, and P.E. Sawchenko Bone marrow-derived cells that populate the adult mouse brain preserve their hematopoietic identity J Neurosci 23 2003 5197 5207
27. D.J. Donnelly, J.C. Gensel, D.P. Ankeny, N. van Rooijen, and P.G. Popovich An efficient and reproducible method for quantifying macrophages in different experimental models of central nervous system pathology J Neurosci Methods 181 2009 36 44
28. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 2001 402 408
29. J.L. Stark, R. Avitsur, D.A. Padgett, K.A. Campbell, F.M. Beck, and J.F. Sheridan Social stress induces glucocorticoid resistance in macrophages Am J Physiol Regul Integr Comp Physiol 280 2001 R1799 R1805
30. N.D. Powell, E.K. Sloan, M.T. Bailey, J.M. Arevalo, G.E. Miller, and E. Chen et al. Social stress up-regulates inflammatory gene expression in the leukocyte transcriptome via beta-adrenergic induction of myelopoiesis Proc Natl Acad Sci U S A 110 2013 16574 16579
31. K. Kierdorf, N. Katzmarski, C.A. Haas, and M. Prinz Bone marrow cell recruitment to the brain in the absence of irradiation or parabiosis bias PLoS One 8 2013 e58544
32. A. Lampron, M. Lessard, and S. Rivest Effects of myeloablation, peripheral chimerism, and whole-body irradiation on the entry of bone marrow-derived cells into the brain Cell Transplant 21 2012 1149 1159
33. A. Mildner, H. Schmidt, M. Nitsche, D. Merkler, U.K. Hanisch, and M. Mack et al. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions Nat Neurosci 10 2007 1544 1553
34. M. Brevet, H. Kojima, A. Asakawa, K. Atsuchi, M. Ushikai, and K. Ataka et al. Chronic foot-shock stress potentiates the influx of bone marrow-derived microglia into hippocampus J Neurosci Res 88 2010 1890 1897
35. B. Ajami, J.L. Bennett, C. Krieger, K.M. McNagny, and F.M. Rossi Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool Nat Neurosci 14 2011 1142 1149
36. C. Schulz, E. Gomez Perdiguero, L. Chorro, H. Szabo-Rogers, N. Cagnard, and K. Kierdorf et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells Science 336 2012 86 90
37. F. Ginhoux, M. Greter, M. Leboeuf, S. Nandi, P. See, and S. Gokhan et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages Science 330 2010 841 845
38. A.W. Corona, Y. Huang, J.C. OConnor, R. Dantzer, K.W. Kelley, P.G. Popovich, and J.P. Godbout Fractalkine receptor (CX3CR1) deficiency sensitizes mice to the behavioral changes induced by lipopolysaccharide J Neuroinflammation 7 2010 93
39. C.J. Henry, Y. Huang, A.M. Wynne, and J.P. Godbout Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1beta and anti-inflammatory IL-10 cytokines Brain Behav Immun 23 2009 309 317
40. J.P. Godbout, M. Moreau, J. Lestage, J. Chen, N.L. Sparkman, and J. OConnor et al. Aging exacerbates depressive-like behavior in mice in response to activation of the peripheral innate immune system Neuropsychopharmacology 33 2008 2341 2351
41. J.P. Godbout, and R.W. Johnson Age and neuroinflammation: A lifetime of psychoneuroimmune consequences Neurol Clin 24 2006 521 538
42. M. Iwata, K.T. Ota, and R.S. Duman The inflammasome: Pathways linking psychological stress, depression, and systemic illnesses Brain Behav Immun 31 2012 105 114
43. J.W. Koo, and R.S. Duman Evidence for IL-1 receptor blockade as a therapeutic strategy for the treatment of depression Curr Opin Investig Drugs 10 2009 664 671
44. R.S. Duman Neuronal damage and protection in the pathophysiology and treatment of psychiatric illness: Stress and depression Dialogues Clin Neurosci 11 2009 239 255
45. H.A. Seifert, A.A. Hall, C.B. Chapman, L.A. Collier, A.E. Willing, and K.R. Pennypacker A transient decrease in spleen size following stroke corresponds to splenocyte release into systemic circulation J Neuroimmune Pharmacol 7 2012 1017 1024
46. P. Dutta, G. Courties, Y. Wei, F. Leuschner, R. Gorbatov, and C.S. Robbins et al. Myocardial infarction accelerates atherosclerosis Nature 487 2012 325 329
47. F.K. Swirski, M. Nahrendorf, M. Etzrodt, M. Wildgruber, V. Cortez-Retamozo, and P. Panizzi et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites Science 325 2009 612 616
48. E.K. Sloan, J.P. Capitanio, R.P. Tarara, and S.W. Cole Social temperament and lymph node innervation Brain Behav Immun 22 2008 717 726
49. S.W. Cole, J.M. Arevalo, R. Takahashi, E.K. Sloan, S.K. Lutgendorf, and K. Sood et al. Computational identification of gene-social environment interaction at the human IL6 locus Proc Natl Acad Sci U S A 107 2010 5681 5686
50. D. Mehta, T. Klengel, K.N. Conneely, A.K. Smith, A. Altmann, and T.W. Pace et al. Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder Proc Natl Acad Sci U S A 110 2013 8302 8307
51. G.E. Miller, E. Chen, J. Sze, T. Marin, J.M. Arevalo, and R. Doll et al. A functional genomic fingerprint of chronic stress in humans: Blunted glucocorticoid and increased NF-kappaB signaling Biol Psychiatry 64 2008 266 272
52. F.S. Dhabhar Enhancing versus suppressive effects of stress on immune function: Implications for immunoprotection and immunopathology Neuroimmunomodulation 16 2009 300 317
53. C. DMello, T. Le, and M.G. Swain Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factoralpha signaling during peripheral organ inflammation J Neurosci 29 2009 2089 2102
54. V.G. Olson, H.R. Rockett, R.K. Reh, V.A. Redila, P.M. Tran, and H.A. Venkov et al. The role of norepinephrine in differential response to stress in an animal model of posttraumatic stress disorder Biol Psychiatry 70 2011 441 448
55. J. Qian, L. Zhu, Q. Li, N. Belevych, Q. Chen, and F. Zhao et al. Interleukin-1R3 mediates interleukin-1-induced potassium current increase through fast activation of Akt kinase Proc Natl Acad Sci U S A 109 2012 12189 12194
56. D. Stellwagen, and R.C. Malenka Synaptic scaling mediated by glial TNF-alpha Nature 440 2006 1054 1059
57. D.L. Gruol, and T.E. Nelson Purkinje neuron physiology is altered by the inflammatory factor interleukin-6 Cerebellum 4 2005 198 205
58. J. Serrats, J.C. Schiltz, B. Garcia-Bueno, N. van Rooijen, T.M. Reyes, and P.E. Sawchenko Dual roles for perivascular macrophages in immune-to-brain signaling Neuron 65 2010 94 106
59. N.C. Derecki, K.M. Quinnies, and J. Kipnis Alternatively activated myeloid (M2) cells enhance cognitive function in immune compromised mice Brain Behav Immun 25 2011 379 385
60. R. Dantzer, and K.W. Kelley Twenty years of research on cytokine-induced sickness behavior Brain Behav Immun 21 2007 153 160
61. H. Anisman Cascading effects of stressors and inflammatory immune system activation: Implications for major depressive disorder J Psychiatry Neurosci 34 2009 4 20
62. K.A. McLaughlin, K.J. Conron, K.C. Koenen, and S.E. Gilman Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: A test of the stress sensitization hypothesis in a population-based sample of adults Psychol Med 40 2010 1647 1658
63. T.W. Pace, T.C. Mletzko, O. Alagbe, D.L. Musselman, C.B. Nemeroff, A.H. Miller, and C.M. Heim Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress Am J Psychiatry 163 2006 1630 1633
64. R.L. Sidman, B. Kosaras, B.M. Misra, and S.L. Senft High Resolution Mouse Brain Atlas 1999 Available at http://www.hms.harvard.edu/research/brain Accessed September 2012