Enriched environment decreases microglia and brain macrophages inflammatory phenotypes through adiponectin-dependent mechanisms: Relevance to depressive-like behavior

Brain, Behavior, and Immunity

Volumn 50, Issue , 2015, Pages 275-287

  Chabry, Joëlle ^a,b   Nicolas, Sarah ^a,b   Cazareth, Julie ^a,b   Murris, Emilie ^a,b   Guyon, Alice ^a,b   Glaichenhaus, Nicolas ^a,b   Heurteaux, Catherine ^a,b   Petit Paitel, Agnès ^a,b  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b CNRS   (France)

Author keywords

Adiponectin; Antidepressant; Brain macrophages; Cytokines; Depression; Enriched environment; Microglia; Neuroinflammation

Indexed keywords

ADIPONECTIN; ARGINASE 1; CHEMOKINE RECEPTOR CCR2; CORTICOSTERONE; I KAPPA B ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBROSPINAL FLUID; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEPRESSION; ENVIRONMENTAL ENRICHMENT; GENE EXPRESSION PROFILING; GENE INDUCTION; HIPPOCAMPUS; HYPOTHALAMUS; MACROPHAGE; MALE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COMPLICATION; ENCEPHALITIS; ENVIRONMENT; GENETICS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; KNOCKOUT MOUSE; METABOLISM;

ADIPONECTIN; ANIMALS; CORTICOSTERONE; CYTOKINES; DEPRESSION; ENCEPHALITIS; ENVIRONMENT; HIPPOCAMPUS; HYPOTHALAMUS; INJECTIONS, INTRAVENTRICULAR; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; PHENOTYPE; RNA, MESSENGER;

EID: 84937855833     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.07.018     Document Type: Article

References (104)

1. Abke S., et al. Adiponectin-induced secretion of interleukin-6 (IL-6), monocyte chemotactic protein-1 (MCP-1, CCL2) and interleukin-8 (IL-8, CXCL8) is impaired in monocytes from patients with type I diabetes. Cardiovasc. Diabetol. 2006, 5:17.
2. Anacker C., Zunszain P.A., Carvalho L.A., Pariante C.M. The glucocorticoid receptor: pivot of depression and of antidepressant treatment?. Psychoneuroendocrinology 2011, 36:415-425.
3. Ardayfio P., Kim K.S. Anxiogenic-like effect of chronic corticosterone in the light-dark emergence task in mice. Behav. Neurosci. 2006, 120:249-256.
4. Beishuizen A., Thijs L.G. Endotoxin and the hypothalamo-pituitary-adrenal (HPA) axis. J. Endotoxin Res. 2003, 9:3-24.
5. Brooks S.P., Trueman R.C., Dunnett S.B. Assessment of motor coordination and balance in mice using the rotarod, elevated bridge, and footprint tests. Curr. Protoc. Mouse Biol. 2012, 2:37-53.
6. Campanella M., Sciorati C., Tarozzo G., Beltramo M. Flow cytometric analysis of inflammatory cells in ischemic rat brain. Stroke 2002, 33:586-592.
7. Capuron L., Miller A.H. Immune system to brain signaling: neuropsychopharmacological implications. Pharmacol. Ther. 2011, 130:226-238.
8. Cardona A.E., Huang D., Sasse M.E., Ransohoff R.M. Isolation of murine microglial cells for RNA analysis or flow cytometry. Nat. Protoc. 2006, 1:1947-1951.
9. Carter B.S., Meng F., Thompson R.C. Glucocorticoid treatment of astrocytes results in temporally dynamic transcriptome regulation and astrocyte-enriched mRNA changes in vitro. Physiol. Genomics 2012, 44:1188-1200.
10. Carvalho A.F., et al. Adipokines as emerging depression biomarkers: a systematic review and meta-analysis. J. Psychiatr. Res. 2014, 59:28-37.
11. Cazareth J., Guyon A., Heurteaux C., Chabry J., Petit-Paitel A. Molecular and cellular neuroinflammatory status of mouse brain after systemic lipopolysaccharide challenge: importance of CCR2/CCL2 signaling. J. Neuroinflammation 2014, 11:132.
12. Chinetti G., Zawadski C., Fruchart J.C., Staels B. Expression of adiponectin receptors in human macrophages and regulation by agonists of the nuclear receptors PPARalpha, PPARgamma, and LXR. Biochem. Biophys. Res. Commun. 2004, 314:151-158.
13. Cizza G., et al. Low 24-hour adiponectin and high nocturnal leptin concentrations in a case-control study of community-dwelling premenopausal women with major depressive disorder: the Premenopausal, Osteopenia/Osteoporosis, Women, Alendronate, Depression (POWER) study. J. Clin. Psychiatry 2010, 71:1079-1087.
14. Cryan J.F., Mombereau C., Vassout A. The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci. Biobehav. Rev. 2005, 29:571-625.
15. da Silva Correia J., Soldau K., Christen U., Tobias P.S., Ulevitch R.J. Lipopolysaccharide is in close proximity to each of the proteins in its membrane receptor complex transfer from CD14 to TLR4 and MD-2. J. Biol. Chem. 2001, 276:21129-21135.
16. Dantzer R. Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur. J. Pharmacol. 2004, 500:399-411.
17. David D.J., et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 2009, 62:479-493.
18. Dickens C., Jackson J., Tomenson B., Hay E., Creed F. Association of depression and rheumatoid arthritis. Psychosomatics 2003, 44:209-215.
19. Dowlati Y., et al. A meta-analysis of cytokines in major depression. Biol. Psychiatry 2010, 67:446-457.
20. Downer E.J., et al. A novel anti-inflammatory role of NCAM-derived mimetic peptide, FGL. Neurobiol. Aging 2010, 31:118-128.
21. Drevets W.C., Price J.L., Furey M.L. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct. Funct. 2008, 213:93-118.
22. Ebinuma H., et al. Improved ELISA for selective measurement of adiponectin multimers and identification of adiponectin in human cerebrospinal fluid. Clin. Chem. 2007, 53:1541-1544.
23. Eisch A.J., Petrik D. Depression and hippocampal neurogenesis: a road to remission?. Science 2012, 338:72-75.
24. Eisenberger N.I., et al. Inflammation-induced anhedonia: endotoxin reduces ventral striatum responses to reward. Biol. Psychiatry 2010, 68:748-754.
25. Espinosa-Oliva A.M., et al. Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol. Aging 2011, 32:85-102.
26. Feldman S., Conforti N. Participation of the dorsal hippocampus in the glucocorticoid feedback effect on adrenocortical activity. Neuroendocrinology 1980, 30:52-55.
27. Franco R., Fernandez-Suarez D. Alternatively activated microglia and macrophages in the central nervous system. Prog. Neurobiol. 2015.
28. Frank M.G., et al. MRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol. Aging 2006, 27:717-722.
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. 2010, 24:19-30.
30. Frank M.G., Watkins L.R., Maier S.F. Stress- and glucocorticoid-induced priming of neuroinflammatory responses: potential mechanisms of stress-induced vulnerability to drugs of abuse. Brain Behav. Immun. 2011, 25(Suppl. 1):S21-28.
31. 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. 2012, 26:337-345.
32. 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 2014, 40:191-200.
33. Fry M., et al. Area postrema neurons are modulated by the adipocyte hormone adiponectin. J. Neurosci. 2006, 26:9695-9702.
34. Fu X., et al. Central administration of lipopolysaccharide induces depressive-like behavior in vivo and activates brain indoleamine 2,3 dioxygenase in murine organotypic hippocampal slice cultures. J. Neuroinflammation 2010, 7:43.
35. Godbout J.P., et al. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 2005, 19:1329-1331.
36. Goshen I., et al. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol. Psychiatry 2008, 13:717-728.
37. Gourley S.L., Wu F.J., Taylor J.R. Corticosterone regulates pERK1/2 map kinase in a chronic depression model. Ann. NY Acad. Sci. 2008, 1148:509-514.
38. Guillod-Maximin E., et al. Adiponectin receptors are expressed in hypothalamus and colocalized with proopiomelanocortin and neuropeptide Y in rodent arcuate neurons. J. Endocrinol. 2009, 200:93-105.
39. Haapakoski R., Mathieu J., Ebmeier K.P., Alenius H., Kivimaki M. Cumulative meta-analysis of interleukins 6 and 1beta, tumour necrosis factor alpha and C-reactive protein in patients with major depressive disorder. Brain Behav. Immun. 2015.
40. Hattori Y., Hattori S., Kasai K. Globular adiponectin activates nuclear factor-kappaB in vascular endothelial cells, which in turn induces expression of proinflammatory and adhesion molecule genes. Diabetes Care 2006, 29:139-141.
41. Henry C.J., Huang Y., Wynne A.M., Godbout J.P. 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. 2009, 23:309-317.
42. Hoogland I.C., Houbolt C., van Westerloo D.J., van Gool W.A., van de Beek D. Systemic inflammation and microglial activation: systematic review of animal experiments. J. Neuroinflammation 2015, 12:114.
43. Hotta K., et al. Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler. Thromb. Vasc. Biol. 2000, 20:1595-1599.
44. Howren M.B., Lamkin D.M., Suls J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom. Med. 2009, 71:171-186.
45. Hoyda T.D., Smith P.M., Ferguson A.V. Adiponectin acts in the nucleus of the solitary tract to decrease blood pressure by modulating the excitability of neuropeptide Y neurons. Brain Res. 2009, 1256:76-84.
46. Jow G.M., Yang T.T., Chen C.L. Leptin and cholesterol levels are low in major depressive disorder, but high in schizophrenia. J. Affect. Disord. 2006, 90:21-27.
47. Kaster M.P., Gadotti V.M., Calixto J.B., Santos A.R., Rodrigues A.L. Depressive-like behavior induced by tumor necrosis factor-alpha in mice. Neuropharmacology 2012, 62:419-426.
48. Kelly K.A., Miller D.B., Bowyer J.F., O'Callaghan J.P. Chronic exposure to corticosterone enhances the neuroinflammatory and neurotoxic responses to methamphetamine. J. Neurochem. 2012, 122:995-1009.
49. Kempermann G., Kronenberg G. Depressed new neurons-adult hippocampal neurogenesis and a cellular plasticity hypothesis of major depression. Biol. Psychiatry 2003, 54:499-503.
50. Kotani K., et al. Adiponectin and smoking status: a systematic review. J. Atheroscler. Thromb. 2012, 19:787-794.
51. Kubota N., et al. Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab. 2007, 6:55-68.
52. Kumada M., et al. Adiponectin specifically increased tissue inhibitor of metalloproteinase-1 through interleukin-10 expression in human macrophages. Circulation 2004, 109:2046-2049.
53. Lara-Castro C., Fu Y., Chung B.H., Garvey W.T. Adiponectin and the metabolic syndrome: mechanisms mediating risk for metabolic and cardiovascular disease. Curr. Opin. Lipidol. 2007, 18:263-270.
54. Liu J., et al. Adiponectin is critical in determining susceptibility to depressive behaviors and has antidepressant-like activity. Proc. Natl. Acad. Sci. USA 2012, 109:12248-12253.
55. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 2009, 10:434-445.
56. MacQueen G., Frodl T. The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research?. Mol. Psychiatry 2011, 16:252-264.
57. Maes M. Major depression and activation of the inflammatory response system. Adv. Exp. Med. Biol. 1999, 461:25-46.
58. Maes M., et al. Increased serum IL-6 and IL-1 receptor antagonist concentrations in major depression and treatment resistant depression. Cytokine 1997, 9:853-858.
59. Mantovani A., et al. Infiltration of tumours by macrophages and dendritic cells: tumour-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Novartis Found Symp. 2004, 256:137-145. discussion 146-138, 259-169.
60. Marques C.P., et al. Prolonged microglial cell activation and lymphocyte infiltration following experimental herpes encephalitis. J. Immunol. 2008, 181:6417-6426.
61. Mildner A., et al. CCR2+Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain 2009, 132:2487-2500.
62. Murray F., Smith D.W., Hutson P.H. Chronic low dose corticosterone exposure decreased hippocampal cell proliferation, volume and induced anxiety and depression like behaviours in mice. Eur. J. Pharmacol. 2008, 583:115-127.
63. Nair A., Bonneau R.H. Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J. Neuroimmunol. 2006, 171:72-85.
64. Neumeier M., et al. Detection of adiponectin in cerebrospinal fluid in humans. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E965-969.
65. Nicolas S., et al. Neurogenesis-independent antidepressant-like effects of enriched environment is dependent on adiponectin. Psychoneuroendocrinology 2015, 57:72-83.
66. Nithianantharajah J., Hannan A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 2006, 7:697-709.
67. O'Connor J.C., et al. 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.
68. Otake H., et al. Relation between plasma adiponectin, high-sensitivity C-reactive protein, and coronary plaque components in patients with acute coronary syndrome. Am. J. Cardiol. 2008, 101:1-7.
69. Otero M., et al. Changes in plasma levels of fat-derived hormones adiponectin, leptin, resistin and visfatin in patients with rheumatoid arthritis. Ann. Rheum. Dis. 2006, 65:1198-1201.
70. Ouchi N., Walsh K. Adiponectin as an anti-inflammatory factor. Clin. Chim. Acta 2007, 380:24-30.
71. Pang T.T., Narendran P. The distribution of adiponectin receptors on human peripheral blood mononuclear cells. Ann. NY Acad. Sci. 2008, 1150:143-145.
72. Pasco J.A., et al. Association of high-sensitivity C-reactive protein with de novo major depression. Br. J. Psychiatry 2010, 197:372-377.
73. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
74. Psilopanagioti A., Papadaki H., Kranioti E.F., Alexandrides T.K., Varakis J.N. Expression of adiponectin and adiponectin receptors in human pituitary gland and brain. Neuroendocrinology 2009, 89:38-47.
75. Qi Y., et al. Adiponectin acts in the brain to decrease body weight. Nat. Med. 2004, 10:524-529.
76. Quan N., Whiteside M., Kim L., Herkenham M. Induction of inhibitory factor kappaBalpha mRNA in the central nervous system after peripheral lipopolysaccharide administration: an in situ hybridization histochemistry study in the rat. Proc. Natl. Acad. Sci. USA 1997, 94:10985-10990.
77. Quan N., He L., Lai W., Shen T., Herkenham M. Induction of IkappaBalpha mRNA expression in the brain by glucocorticoids: a negative feedback mechanism for immune-to-brain signaling. J. Neurosci. 2000, 20:6473-6477.
78. Scheinman R.I., Cogswell P.C., Lofquist A.K., Baldwin A.S. Role of transcriptional activation of I kappa B alpha in mediation of immunosuppression by glucocorticoids. Science 1995, 270:283-286.
79. Schiepers O.J., Wichers M.C., Maes M. Cytokines and major depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:201-217.
80. Schilling M., Strecker J.K., Ringelstein E.B., Kiefer R., Schabitz W.R. Turn-over of meningeal and perivascular macrophages in the brain of MCP-1-, CCR-2- or double knockout mice. Exp. Neurol. 2009, 219:583-585.
81. Schwartz M., Baruch K. The resolution of neuroinflammation in neurodegeneration: leukocyte recruitment via the choroid plexus. EMBO J. 2014, 33:7-22.
82. Senolt L., Pavelka K., Housa D., Haluzik M. Increased adiponectin is negatively linked to the local inflammatory process in patients with rheumatoid arthritis. Cytokine 2006, 35:247-252.
83. Siegert R.J., Abernethy D.A. Depression in multiple sclerosis: a review. J. Neurol. Neurosurg. Psychiatry 2005, 76:469-475.
84. Spranger J., et al. Adiponectin does not cross the blood-brain barrier but modifies cytokine expression of brain endothelial cells. Diabetes 2006, 55:141-147.
85. Strle K., et al. Interleukin-10 in the brain. Crit. Rev. Immunol. 2001, 21:427-449.
86. Swiergiel A.H., Dunn A.J. Effects of interleukin-1beta and lipopolysaccharide on behavior of mice in the elevated plus-maze and open field tests. Pharmacol. Biochem. Behav. 2007, 86:651-659.
87. Takuma K., Ago Y., Matsuda T. Preventive effects of an enriched environment on rodent psychiatric disorder models. J. Pharmacol. Sci. 2011, 117:71-76.
88. Thompson W.L., Karpus W.J., Van Eldik L.J. MCP-1-deficient mice show reduced neuroinflammatory responses and increased peripheral inflammatory responses to peripheral endotoxin insult. J. Neuroinflammation 2008, 5:35.
89. Thundyil J., Pavlovski D., Sobey C.G., Arumugam T.V. Adiponectin receptor signalling in the brain. Br. J. Pharmacol. 2012, 165:313-327.
90. Tomizawa A., Hattori Y., Kasai K., Nakano Y. Adiponectin induces NF-kappaB activation that leads to suppression of cytokine-induced NF-kappaB activation in vascular endothelial cells: globular adiponectin vs. high molecular weight adiponectin. Diab. Vasc. Dis. Res. 2008, 5:123-127.
91. Tomizawa A., Hattori Y., Kasai K. Induction of gene expression in response to globular adiponectin in vascular endothelial cells. Life Sci. 2009, 85:457-461.
92. van Praag H., Kempermann G., Gage F.H. Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 2000, 1:191-198.
93. Wan Z., Mah D., Simtchouk S., Klegeris A., Little J.P. Globular adiponectin induces a pro-inflammatory response in human astrocytic cells. Biochem. Biophys. Res. Commun. 2014, 446:37-42.
94. Weigert J., et al. Reduced response to adiponectin and lower abundance of adiponectin receptor proteins in type 2 diabetic monocytes. FEBS Lett. 2008, 582:1777-1782.
95. Williamson L.L., Chao A., Bilbo S.D. Environmental enrichment alters glial antigen expression and neuroimmune function in the adult rat hippocampus. Brain Behav. Immun. 2012, 26:500-510.
96. Wolf A.M., Wolf D., Rumpold H., Enrich B., Tilg H. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem. Biophys. Res. Commun. 2004, 323:630-635.
97. Wulster-Radcliffe M.C., Ajuwon K.M., Wang J., Christian J.A., Spurlock M.E. Adiponectin differentially regulates cytokines in porcine macrophages. Biochem. Biophys. Res. Commun. 2004, 316:924-929.
98. Yamauchi T., et al. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 2003, 423:762-769.
99. Yau S.Y., et al. Physical exercise-induced hippocampal neurogenesis and antidepressant effects are mediated by the adipocyte hormone adiponectin. Proc. Natl. Acad. Sci. USA 2014, 111:15810-15815.
100. Yirmiya R. Endotoxin produces a depressive-like episode in rats. Brain Res. 1996, 711:163-174.
101. Zeman M., et al. Leptin, adiponectin, leptin to adiponectin ratio and insulin resistance in depressive women. Neuro. Endocrinol. Lett. 2009, 30:387-395.
102. Zhang D., Guo M., Zhang W., Lu X.Y. Adiponectin stimulates proliferation of adult hippocampal neural stem/progenitor cells through activation of p38 mitogen-activated protein kinase (p38MAPK)/glycogen synthase kinase 3beta (GSK-3beta)/beta-catenin signaling cascade. J. Biol. Chem. 2011, 286:44913-44920.
103. Zhou H., Lapointe B.M., Clark S.R., Zbytnuik L., Kubes P. A requirement for microglial TLR4 in leukocyte recruitment into brain in response to lipopolysaccharide. J. Immunol. 2006, 177:8103-8110.
104. Zhou H., Andonegui G., Wong C.H., Kubes P. Role of endothelial TLR4 for neutrophil recruitment into central nervous system microvessels in systemic inflammation. J. Immunol. 2009, 183:5244-5250.