Social defeat promotes a reactive endothelium in a brain region-dependent manner with increased expression of key adhesion molecules, selectins and chemokines associated with the recruitment of myeloid cells to the brain

Neuroscience

Volumn 302, Issue , 2015, Pages 151-164

  Sawicki, C M ^a   McKim, D B ^a   Wohleb, E S ^a,c   Jarrett, B L ^a   Reader, B F ^a   Norden, D M ^a   Godbout, J P ^a   Sheridan, J F ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b Department of Neuroscience The Ohio State University ^*  (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adhesion molecules; Chemokines; Myeloid cell trafficking; Neurovascular unit; Reactive endothelium; Social defeat

Indexed keywords

CD11B ANTIGEN; CD31 ANTIGEN; CELL ADHESION MOLECULE; CHEMOKINE; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; EXCITATORY AMINO ACID TRANSPORTER 1; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PADGEM PROTEIN; SELECTIN; STROMAL CELL DERIVED FACTOR 1; VASCULAR CELL ADHESION MOLECULE 1;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; ASTROCYTE; BONE MARROW CELL; CELL ISOLATION; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEAR; HYPOTHALAMUS; MACROPHAGE; MALE; MENTAL STRESS; MICROGLIA; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REPEATED SOCIAL DEFEAT; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; DISEASE MODEL; ENDOTHELIUM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANALYSIS OF VARIANCE; ANIMALS; ASTROCYTES; BRAIN; CELL ADHESION MOLECULES; CHEMOKINES; DISEASE MODELS, ANIMAL; ENDOTHELIUM; GENE EXPRESSION REGULATION; MALE; MICE; MICROGLIA; MYELOID CELLS; RNA, MESSENGER; SELECTINS; STRESS, PSYCHOLOGICAL;

EID: 84938416117     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.10.004     Document Type: Article

References (64)

1. Audet M.C., Anisman H. Interplay between pro-inflammatory cytokines and growth factors in depressive illnesses. Front Cell Neurosci 2013, 7:68.
2. Avitsur R., Padgett D.A., Dhabhar F.S., Stark J.L., Kramer K.A., Engler H., Sheridan J.F. Expression of glucocorticoid resistance following social stress requires a second signal. J Leukoc Biol 2003, 74:507-513.
3. Brydon L., Edwards S., Jia H., Mohamed-Ali V., Zachary I., Martin J.F., Steptoe A. Psychological stress activates interleukin-1beta gene expression in human mononuclear cells. Brain Behav Immun 2005, 19:540-546.
4. Canteras N.S., Mota-Ortiz S.R., Motta S.C. What ethologically based models have taught us about the neural systems underlying fear and anxiety. Braz J Med Biol Res 2012, 45:321-327.
5. Cartier L., Hartley O., Dubois-Dauphin M., Krause K.H. Chemokine receptors in the central nervous system: role in brain inflammation and neurodegenerative diseases. Brain Res Brain Res Rev 2005, 48:16-42.
6. Cole S.W. Social regulation of leukocyte homeostasis: the role of glucocorticoid sensitivity. Brain Behav Immun 2008, 22:1049-1055.
7. Cole S.W., Arevalo J.M., Takahashi R., Sloan E.K., Lutgendorf S.K., Sood A.K., Sheridan J.F., Seeman T.E. Computational identification of gene-social environment interaction at the human IL6 locus. Proc Natl Acad Sci U S A 2010, 107:5681-5686.
8. Curry J.M., Hanke M.L., Piper M.G., Bailey M.T., Bringardner B.D., Sheridan J.F., Marsh C.B. Social disruption induces lung inflammation. Brain Behav Immun 2010, 24:394-402.
9. del Zoppo G., Ginis I., Hallenbeck J.M., Iadecola C., Wang X., Feuerstein G.Z. Inflammation and stroke: putative role for cytokines, adhesion molecules and iNOS in brain response to ischemia. Brain Pathol 2000, 10:95-112.
10. Donnelly D.J., Longbrake E.E., Shawler T.M., Kigerl K.A., Lai W., Tovar C.A., Ransohoff R.M., Popovich P.G. Deficient CX3CR1 signaling promotes recovery after mouse spinal cord injury by limiting the recruitment and activation of Ly6Clo/iNOS+ macrophages. J Neurosci 2011, 31:9910-9922.
11. Engler H., Bailey M.T., Engler A., Stiner-Jones L.M., Quan N., Sheridan J.F. Interleukin-1 receptor type 1-deficient mice fail to develop social stress-associated glucocorticoid resistance in the spleen. Psychoneuroendocrinology 2008, 33:108-117.
12. Engler H., Dawils L., Hoves S., Kurth S., Stevenson J.R., Schauenstein K., Stefanski V. Effects of social stress on blood leukocyte distribution: the role of alpha- and beta-adrenergic mechanisms. J Neuroimmunol 2004, 156:153-162.
13. Erickson M.A., Banks W.A. Cytokine and chemokine responses in serum and brain after single and repeated injections of lipopolysaccharide: multiplex quantification with path analysis. Brain Behav Immun 2011, 25:1637-1648.
14. Gerszten R.E., Garcia-Zepeda E.A., Lim Y.C., Yoshida M., Ding H.A., Gimbrone M.A., Luster A.D., Luscinskas F.W., Rosenzweig A. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature 1999, 398:718-723.
15. Godbout J.P., Berg B.M., Krzyszton C., Johnson R.W. Alpha-tocopherol attenuates NFkappaB activation and pro-inflammatory cytokine production in brain and improves recovery from lipopolysaccharide-induced sickness behavior. J Neuroimmunol 2005, 169:97-105.
16. Goshen I., Yirmiya R. Interleukin-1 (IL-1): a central regulator of stress responses. Front Neuroendocrinol 2009, 30:30-45.
17. Greenwood J., Heasman S.J., Alvarez J.I., Prat A., Lyck R., Engelhardt B. Review: leucocyte-endothelial cell crosstalk at the blood-brain barrier: a prerequisite for successful immune cell entry to the brain. Neuropathol Appl Neurobiol 2011, 37:24-39.
18. Hansel A., Hong S., Camara R.J., von Kanel R. Inflammation as a psychophysiological biomarker in chronic psychosocial stress. Neurosci Biobehav Rev 2010, 35:115-121.
19. Hidalgo A., Peired A.J., Wild M.K., Vestweber D., Frenette P.S. Complete identification of E-selectin ligands on neutrophils reveals distinct functions of PSGL-1, ESL-1, and CD44. Immunity 2007, 26:477-489.
20. Hol J., Wilhelmsen L., Haraldsen G. The murine IL-8 homologues KC, MIP-2, and LIX are found in endothelial cytoplasmic granules but not in Weibel-Palade bodies. J Leukoc Biol 2010, 87:501-508.
21. Hong S., Johnson T.A., Farag N.H., Guy H.J., Matthews S.C., Ziegler M.G., Mills P.J. Attenuation of T-lymphocyte demargination and adhesion molecule expression in response to moderate exercise in physically fit individuals. J Appl Physiol (1985) 2005, 98:1057-1063.
22. Indovina I., Robbins T.W., Nunez-Elizalde A.O., Dunn B.D., Bishop S.J. Fear-conditioning mechanisms associated with trait vulnerability to anxiety in humans. Neuron 2011, 69:563-571.
23. Iwata M., Ota K.T., Duman R.S. The inflammasome: pathways linking psychological stress, depression, and systemic illnesses. Brain Behav Immun 2013, 31:105-114.
24. 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.
25. Jutila M.A., Kroese F.G., Jutila K.L., Stall A.M., Fiering S., Herzenberg L.A., Berg E.L., Butcher E.C. Ly-6C is a monocyte/macrophage and endothelial cell differentiation antigen regulated by interferon-gamma. Eur J Immunol 1988, 18:1819-1826.
26. Kiecolt-Glaser J.K., Glaser R. Depression and immune function: central pathways to morbidity and mortality. J Psychosom Res 2002, 53:873-876.
27. Kiecolt-Glaser J.K., Preacher K.J., MacCallum R.C., Atkinson C., Malarkey W.B., Glaser R. Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc Natl Acad Sci U S A 2003, 100:9090-9095.
28. Kinsey S.G., Bailey M.T., Sheridan J.F., Padgett D.A., Avitsur R. Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice. Brain Behav Immun 2007, 21:458-466.
29. Ley K. The role of selectins in inflammation and disease. Trends Mol Med 2003, 9:263-268.
30. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
31. Mae M., Armulik A., Betsholtz C. Getting to know the cast - cellular interactions and signaling at the neurovascular unit. Curr Pharm Des 2011, 17:2750-2754.
32. Mahad D., Callahan M.K., Williams K.A., Ubogu E.E., Kivisakk P., Tucky B., Kidd G., Kingsbury G.A., Chang A., Fox R.J., Mack M., Sniderman M.B., Ravid R., Staugaitis S.M., Stins M.F., Ransohoff R.M. Modulating CCR2 and CCL2 at the blood-brain barrier: relevance for multiple sclerosis pathogenesis. Brain 2006, 129:212-223.
33. Martinez M., Calvo-Torrent A., Herbert J. Mapping brain response to social stress in rodents with c-fos expression: a review. Stress 2002, 5:3-13.
34. McCandless E.E., Piccio L., Woerner B.M., Schmidt R.E., Rubin J.B., Cross A.H., Klein R.S. Pathological expression of CXCL12 at the blood-brain barrier correlates with severity of multiple sclerosis. Am J Pathol 2008, 172:799-808.
35. McCandless E.E., Wang Q., Woerner B.M., Harper J.M., Klein R.S. CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis. J Immunol 2006, 177:8053-8064.
36. 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.
37. Miller G.E., Chen E., Sze J., Marin T., Arevalo J.M., Doll R., Ma R., Cole S.W. A functional genomic fingerprint of chronic stress in humans: blunted glucocorticoid and increased NF-kappaB signaling. Biol Psychiatry 2008, 64:266-272.
38. Muller W.A. How endothelial cells regulate transmigration of leukocytes in the inflammatory response. Am J Pathol 2014, 184:886-896.
39. Norden D.M., Fenn A.M., Dugan A., Godbout J.P. TGFbeta produced by IL-10 redirected astrocytes attenuates microglial activation. Glia 2014, 62:881-895.
40. Nourshargh S., Hordijk P.L., Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat Rev Mol Cell Biol 2010, 11:366-378.
41. Nourshargh S., Marelli-Berg F.M. Transmigration through venular walls: a key regulator of leukocyte phenotype and function. Trends Immunol 2005, 26:157-165.
42. O'Connor J.C., Andre C., Wang Y., Lawson M.A., Szegedi S.S., Lestage J., Castanon N., Kelley K.W., Dantzer R. Interferon-gamma and tumor necrosis factor-alpha mediate the upregulation of indoleamine 2,3-dioxygenase and the induction of depressive-like behavior in mice in response to bacillus Calmette-Guerin. J Neurosci 2009, 29:4200-4209.
43. Ottaway C.A., Husband A.J. The influence of neuroendocrine pathways on lymphocyte migration. Immunol Today 1994, 15:511-517.
44. Paxinos G., Franklin K. The mouse brain in stereotaxic coordinates 2008, Academic Press, Inc., New York, NY, USA. 3rd ed.
45. Petri B., Phillipson M., Kubes P. The physiology of leukocyte recruitment: an in vivo perspective. J Immunol 2008, 180:6439-6446.
46. Prinz M., Priller J. Tickets to the brain: role of CCR2 and CX3CR1 in myeloid cell entry in the CNS. J Neuroimmunol 2010, 224:80-84.
47. Ressler K.J., Mayberg H.S. Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nat Neurosci 2007, 10:1116-1124.
48. Roy M., Richard J.F., Dumas A., Vallieres L. CXCL1 can be regulated by IL-6 and promotes granulocyte adhesion to brain capillaries during bacterial toxin exposure and encephalomyelitis. J Neuroinflamm 2012, 9:18.
49. Sehlmeyer C., Dannlowski U., Schoning S., Kugel H., Pyka M., Pfleiderer B., Zwitserlood P., Schiffbauer H., Heindel W., Arolt V., Konrad C. Neural correlates of trait anxiety in fear extinction. Psychol Med 2011, 41:789-798.
50. Shi C., Pamer E.G. Monocyte recruitment during infection and inflammation. Nat Rev Immunol 2011, 11:762-774.
51. Shiratori M., Tozaki-Saitoh H., Yoshitake M., Tsuda M., Inoue K. P2X7 receptor activation induces CXCL2 production in microglia through NFAT and PKC/MAPK pathways. J Neurochem 2010, 114:810-819.
52. Stark J.L., Avitsur R., Hunzeker J., Padgett D.A., Sheridan J.F. Interleukin-6 and the development of social disruption-induced glucocorticoid resistance. J Neuroimmunol 2002, 124:9-15.
53. Suarez E.C., Krishnan R.R., Lewis J.G. The relation of severity of depressive symptoms to monocyte-associated proinflammatory cytokines and chemokines in apparently healthy men. Psychosom Med 2003, 65:362-368.
54. Takeshita Y., Ransohoff R.M. Inflammatory cell trafficking across the blood-brain barrier: chemokine regulation and in vitro models. Immunol Rev 2012, 248:228-239.
55. Thomas D.M., Francescutti-Verbeem D.M., Kuhn D.M. Gene expression profile of activated microglia under conditions associated with dopamine neuronal damage. FASEB J 2006, 20:515-517.
56. Wang X., Feuerstein G.Z., Gu J.L., Lysko P.G., Yue T.L. Interleukin-1 beta induces expression of adhesion molecules in human vascular smooth muscle cells and enhances adhesion of leukocytes to smooth muscle cells. Atherosclerosis 1995, 115:89-98.
57. Wilent W.B., Oh M.Y., Buetefisch C.M., Bailes J.E., Cantella D., Angle C., Whiting D.M. Induction of panic attack by stimulation of the ventromedial hypothalamus. J Neurosurg 2010, 112:1295-1298.
58. Wilson E.H., Weninger W., Hunter C.A. Trafficking of immune cells in the central nervous system. J Clin Invest 2010, 120:1368-1379.
59. 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.
60. 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 2011, 31:6277-6288.
61. Wohleb E.S., McKim D.B., Shea D.T., Powell N.D., Tarr A.J., Sheridan J.F., Godbout J.P. Re-establishment of anxiety in stress-sensitized mice is caused by monocyte trafficking from the spleen to the brain. Biol Psychiatry 2014.
62. Wohleb E.S., Patterson J.M., Sharma V., Quan N., Godbout J.P., Sheridan J.F. Knockdown of interleukin-1 receptor type-1 on endothelial cells attenuated stress-induced neuroinflammation and prevented anxiety-like behavior. J Neurosci 2014, 34:2583-2591.
63. Wohleb E.S., Powell N.D., Godbout J.P., Sheridan J.F. Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. J Neurosci 2013, 33:13820-13833.
64. Zhang X.W., Liu Q., Wang Y., Thorlacius H. CXC chemokines, MIP-2 and KC, induce P-selectin-dependent neutrophil rolling and extravascular migration in vivo. Br J Pharmacol 2001, 133:413-421.