Dynamic microglial alterations underlie stress-induced depressive-like behavior and suppressed neurogenesis (original) (raw)

• Manji HK, Drevets WC, Charney DS . The cellular neurobiology of depression. Nat Med 2001; 7: 541–547.
  Article CAS Google Scholar
• Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM . Neurobiology of depression. Neuron 2002; 34: 13–25.
  Article CAS Google Scholar
• Belmaker RH, Agam G . Major depressive disorder. N Engl J Med 2008; 358: 55–68.
  Article CAS Google Scholar
• Rajkowska G, Miguel-Hidalgo JJ . Gliogenesis and glial pathology in depression. CNS Neurol Disord Drug Targets 2007; 6: 219–233.
  Article CAS Google Scholar
• Banasr M, Duman RS . Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors. Biol Psychiatry 2008; 64: 863–870.
  Article Google Scholar
• Cotter D, Mackay D, Landau S, Kerwin R, Everall I . Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder. Arch Gen Psychiatry 2001; 58: 545–553.
  Article CAS Google Scholar
• Tremblay ME, Stevens B, Sierra A, Wake H, Bessis A, Nimmerjahn A . The role of microglia in the healthy brain. J Neurosci 2011; 31: 16064–16069.
  Article CAS Google Scholar
• Kettenmann H, Hanisch UK, Noda M, Verkhratsky A . Physiology of microglia. Physiol Rev 2011; 91: 461–553.
  Article CAS Google Scholar
• Bayer TA, Buslei R, Havas L, Falkai P . Evidence for activation of microglia in patients with psychiatric illnesses. Neurosci Lett 1999; 271: 126–128.
  Article CAS Google Scholar
• Steiner J, Bielau H, Brisch R, Danos P, Ullrich O, Mawrin C et al. Immunological aspects in the neurobiology of suicide: elevated microglial density in schizophrenia and depression is associated with suicide. J Psychiatr Res 2008; 42: 151–157.
  Article Google Scholar
• Evans DL, Charney DS, Lewis L, Golden RN, Gorman JM, Krishnan KR et al. Mood disorders in the medically ill: scientific review and recommendations. Biol Psychiatry 2005; 58: 175–189.
  Article Google Scholar
• Howren MB, Lamkin DM, Suls J . Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom Med 2009; 71: 171–186.
  Article CAS Google Scholar
• Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK et al. A meta-analysis of cytokines in major depression. Biol Psychiatry 2010; 67: 446–457.
  Article CAS Google Scholar
• Raison CL, Capuron L, Miller AH . Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol 2006; 27: 24–31.
  Article CAS Google Scholar
• Reichenberg A, Yirmiya R, Schuld A, Kraus T, Haack M, Morag A et al. Cytokine-associated emotional and cognitive disturbances in humans. Arch Gen Psychiatry 2001; 58: 445–452.
  Article CAS Google Scholar
• Krabbe KS, Reichenberg A, Yirmiya R, Smed A, Pedersen BK, Bruunsgaard H . Low-dose endotoxemia and human neuropsychological functions. Brain Behav Immun 2005; 19: 453–460.
  Article CAS Google Scholar
• Yirmiya R . Endotoxin produces a depressive-like episode in rats. Brain Res 1996; 711: 163–174.
  Article CAS Google Scholar
• Yirmiya R, Pollak Y, Barak O, Avitsur R, Ovadia H, Bette M et al. Effects of antidepressant drugs on the behavioral and physiological responses to lipopolysaccharide (LPS) in rodents. Neuropsychopharmacology 2001; 24: 531–544.
  Article CAS Google Scholar
• Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW . From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008; 9: 46–56.
  Article CAS Google Scholar
• Tynan RJ, Weidenhofer J, Hinwood M, Cairns MJ, Day TA, Walker FR . A comparative examination of the anti-inflammatory effects of SSRI and SNRI antidepressants on LPS stimulated microglia. Brain Behav Immun 2012; 26: 469–479.
  Article CAS Google Scholar
• Hashioka S, Klegeris A, Monji A, Kato T, Sawada M, McGeer PL et al. Antidepressants inhibit interferon-gamma-induced microglial production of IL-6 and nitric oxide. Exp Neurol 2007; 206: 33–42.
  Article CAS Google Scholar
• Kempermann G, Neumann H . Neuroscience. Microglia: the enemy within? Science 2003; 302: 1689–1690.
  Article CAS Google Scholar
• Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O . Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 2003; 100: 13632–13637.
  Article CAS Google Scholar
• Ekdahl CT, Kokaia Z, Lindvall O . Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 2009; 158: 1021–1029.
  Article CAS Google Scholar
• Monje ML, Toda H, Palmer TD . Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003; 302: 1760–1765.
  Article CAS Google Scholar
• Sahay A, Hen R . Adult hippocampal neurogenesis in depression. Nat Neurosci 2007; 10: 1110–1115.
  Article CAS Google Scholar
• Jacobs BL, Praag H, Gage FH . Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol Psychiatry 2000; 5: 262–269.
  Article CAS Google Scholar
• Malberg JE, Eisch AJ, Nestler EJ, Duman RS . Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 2000; 20: 9104–9110.
  Article CAS Google Scholar
• Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003; 301: 805–809.
  Article CAS Google Scholar
• Goshen I, Yirmiya R . Interleukin-1 (IL-1): a central regulator of stress responses. Front Neuroendocrinol 2009; 30: 30–45.
  Article CAS Google Scholar
• McGonagle KA, Kessler RC . Chronic stress, acute stress, and depressive symptoms. Am J Community Psychol 1990; 18: 681–706.
  Article CAS Google Scholar
• Hammen C . Stress and depression. Annu Rev Clin Psychol 2005; 1: 293–319.
  Article Google Scholar
• Kendler KS, Karkowski LM, Prescott CA . Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry 1999; 156: 837–841.
  Article CAS Google Scholar
• Willner P . Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl) 1997; 134: 319–329.
  CAS Google Scholar
• Frank MG, Baratta MV, Sprunger DB, Watkins LR, Maier SF . Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav Immun 2007; 21: 47–59.
  Article CAS Google Scholar
• Sugama S, Fujita M, Hashimoto M, Conti B . Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18. Neuroscience 2007; 146: 1388–1399.
  Article CAS Google Scholar
• Blandino P Jr., Barnum CJ, Deak T . The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1beta responses to stress. J Neuroimmunol 2006; 173: 87–95.
  Article CAS Google Scholar
• Blandino P Jr., Barnum CJ, Solomon LG, Larish Y, Lankow BS, Deak T . Gene expression changes in the hypothalamus provide evidence for regionally-selective changes in IL-1 and microglial markers after acute stress. Brain Behav Immun 2009; 23: 958–968.
  Article CAS Google Scholar
• Nair A, Bonneau RH . Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J Neuroimmunol 2006; 171: 72–85.
  Article CAS Google Scholar
• Wohleb ES, Hanke ML, Corona AW, Powell ND, Stiner LM, Bailey MT et al. beta-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J Neurosci 2011; 31: 6277–6288.
  Article CAS Google Scholar
• Tynan RJ, Naicker S, Hinwood M, Nalivaiko E, Buller KM, Pow DV et al. Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions. Brain Behav Immun 2010; 24: 1058–1068.
  Article CAS Google Scholar
• Goshen I, Kreisel T, Ben-Menachem-Zidon O, Licht T, Weidenfeld J, Ben-Hur T 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.
  Article CAS Google Scholar
• Koo JW, Duman RS . IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci USA 2008; 105: 751–756.
  Article CAS Google Scholar
• Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 2000; 20: 4106–4114.
  Article CAS Google Scholar
• Lundkvist J, Sundgren-Andersson AK, Tingsborg S, Ostlund P, Engfors C, Alheim K et al. Acute-phase responses in transgenic mice with CNS overexpression of IL-1 receptor antagonist. Am J Physiol 1999; 276: R644–R651.
  CAS PubMed Google Scholar
• Bajayo A, Goshen I, Feldman S, Csernus V, Iverfeldt K, Shohami E et al. Central IL-1 receptor signaling regulates bone growth and mass. Proc Natl Acad Sci USA 2005; 102: 12956–12961.
  Article CAS Google Scholar
• Hinwood M, Tynan RJ, Charnley JL, Beynon SB, Day TA, Walker FR . Chronic stress induced remodeling of the prefrontal cortex: structural re-organization of microglia and the inhibitory effect of minocycline. Cereb Cortex 2012; 23: 1784–1797.
  Article Google Scholar
• Hinwood M, Morandini J, Day TA, Walker FR . Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex. Cereb Cortex 2012; 22: 1442–1454.
  Article CAS Google Scholar
• Boissonneault V, Filali M, Lessard M, Relton J, Wong G, Rivest S . Powerful beneficial effects of macrophage colony-stimulating factor on beta-amyloid deposition and cognitive impairment in Alzheimer's disease. Brain 2009; 132: 1078–1092.
  Article Google Scholar
• Giulian D, Ingeman JE . Colony-stimulating factors as promoters of ameboid microglia. J Neurosci 1988; 8: 4707–4717.
  Article CAS Google Scholar
• Suzumura A, Sawada M, Yamamoto H, Marunouchi T . Effects of colony stimulating factors on isolated microglia in vitro. J Neuroimmunol 1990; 30: 111–120.
  Article CAS Google Scholar
• Chomczynski P, Sacchi N . Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162: 156–159.
  Article CAS Google Scholar
• Frank MG, Wieseler-Frank JL, Watkins LR, Maier SF . Rapid isolation of highly enriched and quiescent microglia from adult rat hippocampus: immunophenotypic and functional characteristics. J Neurosci Methods 2006; 151: 121–130.
  Article Google Scholar
• Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25: 3389–3402.
  Article CAS Google Scholar
• Burguillos MA, Deierborg T, Kavanagh E, Persson A, Hajji N, Garcia-Quintanilla A et al. Caspase signalling controls microglia activation and neurotoxicity. Nature 2011; 472: 319–324.
  Article CAS Google Scholar
• Shi Y . Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 2002; 9: 459–470.
  Article CAS Google Scholar
• Castanon N, Leonard BE, Neveu PJ, Yirmiya R . Effects of antidepressants on cytokine production and actions. Brain Behav Immun 2002; 16: 569–574.
  Article CAS Google Scholar
• Walker FR . A critical review of the mechanism of action for the selective serotonin reuptake inhibitors: do these drugs possess anti-inflammatory properties and how relevant is this in the treatment of depression? Neuropharmacology 2013; 67: 304–317.
  Article CAS Google Scholar
• Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J . Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 2007; 27: 2596–2605.
  Article CAS Google Scholar
• Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW . Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci USA 1996; 93: 3908–3913.
  Article CAS Google Scholar
• Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, Charney DS . Hippocampal volume reduction in major depression. Am J Psychiatry 2000; 157: 115–118.
  Article CAS Google Scholar
• Liu B, Wang K, Gao HM, Mandavilli B, Wang JY, Hong JS . Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J Neurochem 2001; 77: 182–189.
  Article CAS Google Scholar
• Tanebe K, Nishijo H, Muraguchi A, Ono T . Effects of chronic stress on hypothalamic lnterleukin-1beta, interleukin-2, and gonadotrophin-releasing hormone gene expression in ovariectomized rats. J Neuroendocrinol 2000; 12: 13–21.
  Article CAS Google Scholar
• Bartolomucci A, Palanza P, Parmigiani S, Pederzani T, Merlot E, Neveu PJ et al. Chronic psychosocial stress down-regulates central cytokines mRNA. Brain Res Bull 2003; 62: 173–178.
  Article CAS Google Scholar
• Girotti M, Donegan JJ, Morilak DA . Chronic intermittent cold stress sensitizes neuro-immune reactivity in the rat brain. Psychoneuroendocrinology 2011; 36: 1164–1174.
  Article CAS Google Scholar
• Plata-Salaman CR, Ilyin SE, Turrin NP, Gayle D, Flynn MC, Bedard T et al. Neither acute nor chronic exposure to a naturalistic (predator) stressor influences the interleukin-1beta system, tumor necrosis factor-alpha, transforming growth factor-beta1, and neuropeptide mRNAs in specific brain regions. Brain Res Bull 2000; 51: 187–193.
  Article CAS Google Scholar
• Mormede C, Castanon N, Medina C, Moze E, Lestage J, Neveu PJ et al. Chronic mild stress in mice decreases peripheral cytokine and increases central cytokine expression independently of IL-10 regulation of the cytokine network. Neuroimmunomodulation 2002; 10: 359–366.
  Article CAS Google Scholar
• Yirmiya R, Goshen I . Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 2011; 25: 181–213.
  Article CAS Google Scholar
• McAfoose J, Baune BT . Evidence for a cytokine model of cognitive function. Neurosci Biobehav Rev 2009; 33: 355–366.
  Article CAS Google Scholar
• Pittenger C, Duman RS . Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 2008; 33: 88–109.
  Article CAS Google Scholar
• Thored P, Heldmann U, Gomes-Leal W, Gisler R, Darsalia V, Taneera J et al. Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 2009; 57: 835–849.
  Article Google Scholar
• Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N et al. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 2006; 9: 268–275.
  Article CAS Google Scholar
• Lai AY, Todd KG . Differential regulation of trophic and proinflammatory microglial effectors is dependent on severity of neuronal injury. Glia 2008; 56: 259–270.
  Article Google Scholar
• Kohman RA, DeYoung EK, Bhattacharya TK, Peterson LN, Rhodes JS . Wheel running attenuates microglia proliferation and increases expression of a proneurogenic phenotype in the hippocampus of aged mice. Brain Behav Immun 2012; 26: 803–810.
  Article CAS Google Scholar
• Bouhy D, Malgrange B, Multon S, Poirrier AL, Scholtes F, Schoenen J et al. Delayed GM-CSF treatment stimulates axonal regeneration and functional recovery in paraplegic rats via an increased BDNF expression by endogenous macrophages. FASEB J 2006; 20: 1239–1241.
  Article CAS Google Scholar
• Kern S, Skoog I, Börjesson-Hanson A, Blennow K, Zetterberg H, Ostling S et al. Lower CSF interleukin-6 predicts future depression in a population-based sample of older women followed for 17 years. Brain Behav Immun 2013; 32: 153–158.
  Article CAS Google Scholar
• Hannestad J, DellaGioia N, Bloch M . The effect of antidepressant medication treatment on serum levels of inflammatory cytokines: a meta-analysis. Neuropsychopharmacology 2011; 36: 2452–2459.
  Article CAS Google Scholar
• Warner-Schmidt JL, Vanover KE, Chen EY, Marshall JJ, Greengard P . Antidepressant effects of selective serotonin reuptake inhibitors (SSRIs) are attenuated by antiinflammatory drugs in mice and humans. Proc Natl Acad Sci USA 2011; 108: 9262–9267.
  Article CAS Google Scholar
• Fields C, Drye L, Vaidya V, Lyketsos C . Celecoxib or naproxen treatment does not benefit depressive symptoms in persons age 70 and older: findings from a randomized controlled trial. Am J Geriatr Psychiatry 2012; 20: 505–513.
  Article Google Scholar
• Gallagher PJ, Castro V, Fava M, Weilburg JB, Murphy SN, Gainer VS et al. Antidepressant response in patients with major depression exposed to NSAIDs: a pharmacovigilance study. Am J Psychiatry 2012; 169: 1065–1072.
  Article Google Scholar
• Perez-Caballero L, Pérez-Egea R, Romero-Grimaldi C, Puigdemont D, Molet J, Caso JR et al. Early responses to deep brain stimulation in depression are modulated by anti-inflammatory drugs. Mol Psychiatry, advance online publication, 28 May 2013; doi:10.1038/mp.2013.63 (e-pub ahead of print).
• Raison CL, Rutherford RE, Woolwine BJ, Shuo C, Schettler P, Drake DF et al. A randomized controlled trial of the tumor necrosis factor antagonist infliximab for treatment-resistant depression: the role of baseline inflammatory biomarkers. JAMA Psychiatry 2013; 70: 31–41.
  Article CAS Google Scholar
• Maes M, Yirmyia R, Noraberg J, Brene S, Hibbeln J, Perini G et al. The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab Brain Dis 2009; 24: 27–53.
  Article CAS Google Scholar
• Bauer J, Hohagen F, Gimmel E, Bruns F, Lis S, Krieger S et al. Induction of cytokine synthesis and fever suppresses REM sleep and improves mood in patients with major depression. Biol Psychiatry 1995; 38: 611–621.
  Article CAS Google Scholar