Lymphocytes from Chronically Stressed Mice Confer Antidepressant-Like Effects to Naive Mice

Journal of Neuroscience

Volumn 35, Issue 4, 2015, Pages 1530-1538

  Brachman, Rebecca A ^a   Lehmann, Xmichael L ^a   Maric, Dragan ^b   Herkenham, Xmiles ^a  

^a Building 41   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Adaptive immune system; Cytokines; Depression; Hippocampal neurogenesis; Lymphocytes; Stress

Indexed keywords

CORTICOSTERONE; CYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ANTIDEPRESSANT AGENT; DNA BINDING PROTEIN; RAG2 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ANXIETY; ARTICLE; BEHAVIOR ASSESSMENT; CELL ACTIVITY; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM FUNCTION; CHRONIC STRESS; CONTROLLED STUDY; DEPRESSION; EXPERIMENTAL TEST; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LIGHT DARK BOX TEST; LYMPHOCYTE; MALE; MENTAL STRESS; MICROGLIA; MOOD; MOUSE; NEUROPROTECTION; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN DETERMINATION; RADIOIMMUNOASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOCIAL BEHAVIOR; SOCIAL INTERACTION TEST; TAIL SUSPENSION TEST; ADOPTIVE TRANSFER; ANIMAL; BLOOD; C57BL MOUSE; CHEMISTRY; CHRONIC DISEASE; DARK ADAPTATION; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PHYSIOLOGY; PSYCHOLOGY; THERAPY; URINE;

ADOPTIVE TRANSFER; ANIMALS; ANTIDEPRESSIVE AGENTS; CELL PROLIFERATION; CHRONIC DISEASE; CORTICOSTERONE; CYTOKINES; DARK ADAPTATION; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LYMPHOCYTES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; STRESS, PSYCHOLOGICAL; URINE;

EID: 84921900973     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2278-14.2015     Document Type: Article

References (42)

1. Battista D, Ferrari CC, Gage FH, Pitossi FJ (2006) Neurogenic niche modulation by activated microglia: transforming growth factor_ increases neurogenesis in the adult dentate gyrus. Eur J Neurosci 23:83–93. CrossRef Medline
2. Beurel E, Harrington LE, Jope RS (2013) Inflammatory T helper 17 cells promote depression-like behavior in mice. Biol Psychiatry 73:622– 630. CrossRef Medline
3. Brynskikh A, Warren T, Zhu J, Kipnis J (2008) Adaptive immunity affects learning behavior in mice. Brain Behav Immun 22:861– 869. CrossRef Medline
4. Cherry JD, Olschowka JA, O’Banion MK (2014) Neuroinflammation and M2 microglia: the good, the bad, and the inflamed. J Neuroinflammation 11:98. CrossRef Medline
5. Cho BK, Rao VP, Ge Q, Eisen HN, Chen J (2000) Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J Exp Med 192:549 –556. CrossRef Medline
6. Chun JJ, Schatz DG, Oettinger MA, Jaenisch R, Baltimore D (1991) The recombination activating gene-1 (RAG-1) transcript is present in the murine central nervous system. Cell 64:189 –200. CrossRef Medline
7. Cohen H, Ziv Y, Cardon M, Kaplan Z, Matar MA, Gidron Y, Schwartz M, Kipnis J (2006) Maladaptation to mental stress mitigated by the adaptive immune system via depletion of naturally occurring regulatory CD4_CD25_ cells. J Neurobiol 66:552-563.CrossRef Medline
8. Crawley JN (1985) Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 9:37– 44. CrossRef Medline
9. Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9:46 –56. CrossRef Medline
10. Derecki NC, Cardani AN, Yang CH, Quinnies KM, Crihfield A, Lynch KR, Kipnis J (2010) Regulation of learning and memory by meningeal immunity: a key role for IL-4. J Exp Med 207:1067-1080.CrossRef Medline
11. Dummer W, Ernst B, LeRoy E, Lee D, Surh C (2001) Autologous regulation of naive T cell homeostasis within the T cell compartment. J Immunol 166:2460 –2468. CrossRef Medline
12. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, LindvallO (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 100:13632-13637.CrossRef Medline
13. Ernst B, Lee DS, Chang JM, Sprent J, Surh CD (1999) The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity 11:173-181.
14. CrossRef Medline Frank MG, Baratta MV, Sprunger DB, Watkins LR, Maier SF (2007) Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav Immun 21:47-59.
15. CrossRef Medline Frick LR, Arcos ML, Rapanelli M, Zappia MP, Brocco M, Mongini C, Genaro AM, Cremaschi GA (2009) Chronic restraint stress impairs T-cell immunity and promotes tumor progression in mice. Stress 12:134–143. CrossRef Medline
16. Gibney SM, Drexhage HA (2013) Evidence for a dysregulated immune system in the etiology of psychiatric disorders. J Neuroimmune Pharmacol 8:900 –920. CrossRef Medline
17. Glaser R, Kiecolt-Glaser JK (2005) Stress-induced immune dysfunction: implications for health. Nat Rev Immunol 5:243-251.CrossRef Medline
18. Gould E, Tanapat P (1999) Stress and hippocampal neurogenesis. Biol Psychiatry 46:1472-1479.CrossRef Medline
19. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG (2009) Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 29:13435-13444.CrossRef Medline
20. Kim SJ, Lee H, Lee G, Oh SJ, Shin MK, Shim I, Bae H (2012) CD4_CD25_ regulatory T cell depletion modulates anxiety and depression-like behaviors in mice. PLoS One 7:42054. CrossRef Medline
21. Lehmann ML, Herkenham M (2011) Environmental enrichment confers stress resiliency to social defeat through an infralimbic cortex-dependent neuroanatomical pathway. J Neurosci 31:6159-6173.CrossRef Medline
22. Lehmann ML, Brachman RA, Martinowich K, Schloesser RJ, Herkenham M (2013a) Glucocorticoids orchestrate divergent effects on mood through adult neurogenesis. J Neurosci 33:2961-2972.CrossRef Medline
23. Lehmann ML, Geddes CE, Lee JL, Herkenham M (2013b) Urine scent marking (USM): a novel test for depressive-like behavior and a predictor of stress resiliency in mice. PLoS One 8:69822. CrossRef Medline
24. Lehmann ML, Mustafa T, Eiden AM, Herkenham M, Eiden LE (2013c) PACAP-deficient mice show attenuated corticosterone secretion and fail to develop depressive behavior during chronic social defeat stress. Psychoneuroendocrinology 38:702-715.CrossRef Medline
25. Lewitus GM, Schwartz M (2009) Behavioral immunization: immunity to self-antigens contributes to psychological stress resilience. Mol Psychiatry 14:532-536.CrossRef Medline
26. Maier SF, Watkins LR (1998) Cytokines for psychologists: implications of bidirectional immune-to-brain communication for understanding behavior, mood, and cognition. Psychol Rev 105:83-107.CrossRef Medline
27. Mathieu P, Piantanida AP, Pitossi F (2010) Chronic expression of transforming growth factor-beta enhances adult neurogenesis. Neuroimmunomodulation 17:200 –201. CrossRef Medline
28. Miller AH (2010) Depression and immunity: a role for T cells? Brain Behav Immun 24:1– 8. CrossRef Medline Miller AH, Maletic V, Raison CL (2009) Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry 65:732-741.CrossRef Medline
29. Min B, Foucras G, Meier-Schellersheim M, Paul WE (2004) Spontaneous proliferation, a response of naive CD4 T cells determined by the diversity of the memory cell repertoire. Proc Natl Acad Sci U S A 101:3874 –3879. CrossRef Medline
30. Murali-Krishna K, Ahmed R (2000) Cutting edge: naive T cells masquerading as memory cells. J Immunol 165:1733-1737.CrossRef Medline
31. Rattazzi L, Piras G, Ono M, Deacon R, Pariante CM, D’Acquisto F (2013) CD4_ but not CD8_ T cells revert the impaired emotional behavior of immunocompromised RAG-1-deficient mice. Transl Psychiatry 3:280. CrossRef Medline
32. Schloesser RJ, Lehmann M, Martinowich K, Manji HK, Herkenham M (2010) Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress. Mol Psychiatry 15:1152-1163.CrossRef Medline
33. Schwartz M, Kipnis J (2011) A conceptual revolution in the relationships between the brain and immunity. Brain Behav Immun 25:817-819.CrossRef Medline
34. Schwartz M, Shechter R (2010) Protective autoimmunity functions by intracranial immunosurveillance to support the mind: the missing link between health and disease. Mol Psychiatry 15:342-354.
35. CrossRef Medline Segerstrom SC, Miller GE (2004) Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol Bull 130:601– 630. CrossRef Medline
36. Shinkai Y, Rathbun G, Lam KP, Oltz EM, Stewart V, Mendelsohn M, Charron J, Datta M, Young F, Stall AM (1992) RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68: 855-867.CrossRef Medline
37. Silberman DM, Ayelli-Edgar V, Zorrilla-Zubilete M, Zieher LM, Genaro AM (2004) Impaired T-cell dependent humoral response and its relationship with T lymphocyte sensitivity to stress hormones in a chronic mild stress model of depression. Brain Behav Immun 18:81– 90. CrossRef Medline
38. Wolf SA, Steiner B, Wengner A, Lipp M, Kammertoens T, Kempermann G (2009) Adaptive peripheral immune response increases proliferation of neural precursor cells in the adult hippocampus. FASEB J 23:3121-3128.CrossRef Medline
39. Ziemssen T, Kern S (2007) Psychoneuroimmunology—cross-talk between the immune and nervous systems. J Neurol 254 [Suppl 2]:II8 –II11. CrossRef Medline
40. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N, Cohen H, Kipnis J, Schwartz M (2006) Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 9:268 –275. CrossRef Medline
41. Zorrilla EP, Luborsky L, McKay JR, Rosenthal R, Houldin A, Tax A, McCorkle R, Seligman DA, Schmidt K (2001) The relationship of depression and stressors to immunological assays: a meta-analytic review. Brain Behav Immun 15:199 –226. CrossRef Medline
42. Zunszain PA, Hepgul N, Pariante CM (2013) Inflammation and depression. Curr Top Behav Neurosci 14:135-151.CrossRef Medline