Microglia activation regulates GluR1 phosphorylation in chronic unpredictable stress-induced cognitive dysfunction

References

• Alfarez DN, Joels M, Krugers HJ. (2003). Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur J Neurosci 17:1928–34
   PubMed Web of Science ®Google Scholar
• Alkadhi KA, Alzoubi KH, Srivareerat M, Tran TT. (2011). Chronic psychosocial stress exacerbates impairment of synaptic plasticity in beta-amyloid rat model of Alzheimer's disease: prevention by nicotine. Curr Alzheimer Res 8:718–31
   PubMed Web of Science ®Google Scholar
• Arvin KL, Han BH, Du Y, Lin SZ, Paul SM, Holtzman DM. (2002). Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann Neurol 52:54–61
   PubMed Web of Science ®Google Scholar
• Barger SW, Basile AS. (2001). Activation of microglia by secreted amyloid precursor protein evokes release of glutamate by cystine exchange and attenuates synaptic function. J Neurochem 76:846–54
   PubMed Web of Science ®Google Scholar
• Barnum CJ, Blandino P, Jr Deak T. (2008). Social status modulates basal IL-1 concentrations in the hypothalamus of pair-housed rats and influences certain features of stress reactivity. Brain Behav Immun 22:517–27
   PubMed Web of Science ®Google Scholar
• Barria A, Derkach V, Soderling T. (1997). Identification of the Ca2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in the alpha-amino-3-hydroxyl-5-methyl-4-isoxazole- propionate-type glutamate receptor. J Biol Chem 272:32727–30
   PubMed Web of Science ®Google Scholar
• Bian Y, Pan Z, Hou Z, Huang C, Li W, Zhao B. (2012). Learning, memory, and glial cell changes following recovery from chronic unpredictable stress. Brain Res Bull 88:471–6
   PubMed Web of Science ®Google Scholar
• Bianco F, Pravettoni E, Colombo A, Schenk U, Moller T, Matteoli M, Verderio C. (2005). Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. J Immunol 174:7268–77
   PubMed Web of Science ®Google Scholar
• Bird CM, Burgess N. (2008). The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9:182–94
   PubMed Web of Science ®Google Scholar
• Blandino P Jr, Barnum CJ, Deak T. (2006). The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1beta responses to stress. J Neuroimmunol 173:87–95
   PubMed Web of Science ®Google Scholar
• Blandino P, Jr Barnum CJ, Solomon LG, Larish Y, Lankow BS, Deak T. (2009). Gene expression changes in the hypothalamus provide evidence for regionally-selective changes in IL-1 and microglial markers after acute stress. Brain Behav Immun 23:958–68
   PubMed Web of Science ®Google Scholar
• Bliss TV, Collingridge GL. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–9
   PubMed Web of Science ®Google Scholar
• Bondi CO, Rodriguez G, Gould GG, Frazer A, Morilak DA. (2008). Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology 33:320–31
   PubMed Web of Science ®Google Scholar
• Burguillos MA, Deierborg T, Kavanagh E, Persson A, Hajji N, Garcia-Quintanilla A, Cano J, et al. (2011). Caspase signalling controls microglia activation and neurotoxicity. Nature 472:319–24
   PubMed Web of Science ®Google Scholar
• Carty ML, Wixey JA, Colditz PB, Buller KM. (2008). Post-insult minocycline treatment attenuates hypoxia-ischemia-induced neuroinflammation and white matter injury in the neonatal rat: a comparison of two different dose regimens. Int J Dev Neurosci 26:477–85
   PubMed Web of Science ®Google Scholar
• Chu YX, Zhang Y, Zhang YQ, Zhao ZQ. (2010). Involvement of microglial P2X7 receptors and downstream signaling pathways in long-term potentiation of spinal nociceptive responses. Brain Behav Immun 24:1176–89
   PubMed Web of Science ®Google Scholar
• Cooke SF, Bliss TV. (2006). Plasticity in the human central nervous system. Brain 129:1659–73
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• De Leonibus E, Costantini VJ, Castellano C, Ferretti V, Oliverio A, Mele A. (2003). Distinct roles of the different ionotropic glutamate receptors within the nucleus accumbens in passive-avoidance learning and memory in mice. Eur J Neurosci 18:2365–73
   PubMed Web of Science ®Google Scholar
• Diz-Chaves Y, Pernia O, Carrero P, Garcia-Segura LM. (2012). Prenatal stress causes alterations in the morphology of microglia and the inflammatory response of the hippocampus of adult female mice. J Neuroinflammation 9:71
   PubMed Web of Science ®Google Scholar
• Dunn AJ, Swiergiel AH. (2005). Effects of interleukin-1 and endotoxin in the forced swim and tail suspension tests in mice. Pharmacol Biochem Behav 81:688–93
   PubMed Web of Science ®Google Scholar
• Ehlert U, Gaab J, Heinrichs M. (2001). Psychoneuroendocrinological contributions to the etiology of depression, posttraumatic stress disorder, and stress-related bodily disorders: the role of the hypothalamus-pituitary-adrenal axis. Biol Psychol 57:141–52
   PubMed Web of Science ®Google Scholar
• Eichenbaum H. (2000). A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 1:41–50
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Frigo DE, Vigh KA, Struckhoff AP, Elliott S, Beckman BS, Burow ME, McLachlan JA. (2005). Xenobiotic-induced TNF-alpha expression and apoptosis through the p38 MAPK signaling pathway. Toxicol Lett 155:227–38
   PubMed Web of Science ®Google Scholar
• Gecz J. (2010). Glutamate receptors and learning and memory. Nat Genet 42:925–6
   PubMed Web of Science ®Google Scholar
• Godbout JP, Moreau M, Lestage J, Chen J, Sparkman NL, OC J, Castanon N, et al. (2008). Aging exacerbates depressive-like behavior in mice in response to activation of the peripheral innate immune system. Neuropsychopharmacology 33:2341–51
   PubMed Web of Science ®Google Scholar
• Goshen I, Kreisel T, Ben-Menachem-Zidon O, Licht T, Weidenfeld J, Ben-Hur T, Yirmiya R. (2008). Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol Psychiatry 13:717–28
   PubMed Web of Science ®Google Scholar
• Goshen I, Yirmiya R. (2009). Interleukin-1 (IL-1): a central regulator of stress responses. Front Neuroendocrinol 30:30–45
   PubMed Web of Science ®Google Scholar
• Gouirand AM, Matuszewich L. (2005). The effects of chronic unpredictable stress on male rats in the water maze. Physiol Behav 86:21–31
   PubMed Web of Science ®Google Scholar
• Grippo AJ, Francis J, Beltz TG, Felder RB, Johnson AK. (2005). Neuroendocrine and cytokine profile of chronic mild stress-induced anhedonia. Physiol Behav 84:697–706
   PubMed Web of Science ®Google Scholar
• Grossmann R, Stence N, Carr J, Fuller L, Waite M, Dailey ME. (2002). Juxtavascular microglia migrate along brain microvessels following activation during early postnatal development. Glia 37(3):229–40
   PubMed Web of Science ®Google Scholar
• Hinwood M, Morandini J, Day TA, Walker FR. (2012). Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex. Cereb Cortex 22:1442–54
   PubMed Web of Science ®Google Scholar
• Hinwood M, Tynan RJ, Charnley JL, Beynon SB, Day TA, Walker FR. (2013). Chronic stress induced remodeling of the prefrontal cortex: structural re-organization of microglia and the inhibitory effect of minocycline. Cereb Cortex 23(8):1784–97
   PubMed Web of Science ®Google Scholar
• Jiao J, Xue B, Zhang L, Gong Y, Li K, Wang H, Jing L, Xie J, Wang X. (2008). Triptolide inhibits amyloid-beta1-42-induced TNF-alpha and IL-1beta production in cultured rat microglia. J Neuroimmunol 205:32–6
   PubMed Web of Science ®Google Scholar
• Keblesh JP, Dou H, Gendelman HE, Xiong H. (2009). 4-Aminopyridine improves spatial memory in a murine model of HIV-1 encephalitis. J Neuroimmune Pharmacol 4:317–27
   PubMed Web of Science ®Google Scholar
• Kelly MP, Adamowicz W, Bove S, Hartman AJ, Mariga A, Pathak G, Reinhart V, et al. (2014). Select 3′,5′-cyclic nucleotide phosphodiesterases exhibit altered expression in the aged rodent brain. Cell Signal 26:383–97
   PubMed Web of Science ®Google Scholar
• Kobayashi K, Imagama S, Ohgomori T, Hirano K, Uchimura K, Sakamoto K, Hirakawa A, et al. (2013). Minocycline selectively inhibits M1 polarization of microglia. Cell Death Dis 4:e525
   PubMed Web of Science ®Google Scholar
• Kohman RA, Bhattacharya TK, Kilby C, Bucko P, Rhodes JS. (2013). Effects of minocycline on spatial learning hippocampal neurogenesis and microglia in aged and adult mice. Behav Brain Res 242:17–24
   PubMed Web of Science ®Google Scholar
• Kopp BL, Wick D, Herman JP. (2013). Differential effects of homotypic vs. heterotypic chronic stress regimens on microglial activation in the prefrontal cortex. Physiol Behav 122:246–52
   PubMed Web of Science ®Google Scholar
• Kwon MS, Seo YJ, Lee JK, Lee HK, Jung JS, Jang JE, Park SH, Suh HW. (2008). The repeated immobilization stress increases IL-1beta immunoreactivities in only neuron, but not astrocytes or microglia in hippocampal CA1 region, striatum and paraventricular nucleus. Neurosci Lett 430(3):258–63
   PubMed Web of Science ®Google Scholar
• Lai AY, Swayze RD, El-Husseini A, Song C. (2006). Interleukin-1 beta modulates AMPA receptor expression and phosphorylation in hippocampal neurons. J Neuroimmunol 175:97–106
   PubMed Web of Science ®Google Scholar
• Lee HK, Takamiya K, Han JS, Man H, Kim CH, Rumbaugh G, Yu S, et al. (2003). Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112:631–43
   PubMed Web of Science ®Google Scholar
• Lisman J, Raghavachari S. (2006). A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE 2006:re11
   PubMedGoogle Scholar
• Liu M, Cai T, Zhao F, Zheng G, Wang Q, Chen Y, Huang C, Luo W, Chen J. (2009). Effect of microglia activation on dopaminergic neuronal injury induced by manganese, and its possible mechanism. Neurotox Res 16:42–9
   PubMed Web of Science ®Google Scholar
• Lopez JF, Akil H, Watson SJ. (1999). Neural circuits mediating stress. Biol Psychiatr 46:1461–71
   PubMed Web of Science ®Google Scholar
• Maes M, Song C, Lin A, De Jongh R, Van Gastel A, Kenis G, Bosmans E, et al. (1998). The effects of psychological stress on humans: increased production of pro-inflammatory cytokines and a Th1-like response in stress-induced anxiety. Cytokine 10:313–18
   PubMed Web of Science ®Google Scholar
• McEwen BS, Sapolsky RM. (1995). Stress and cognitive function. Curr Opin Neurobiol 5:205–16
   PubMed Web of Science ®Google Scholar
• Miller AH, Maletic V, Raison CL. (2009). Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatr 65:732–41
   PubMed Web of Science ®Google Scholar
• Nadel L, MacDonald L. (1980). Hippocampus: cognitive map or working memory? Behav Neural Biol 29:405–9
   PubMedGoogle Scholar
• Nair A, Bonneau RH. (2006). Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J Neuroimmunol 171:72–85
   PubMed Web of Science ®Google Scholar
• O'Connor KA, Johnson JD, Hansen MK, Wieseler Frank JL, Maksimova E, Watkins LR, Maier SF. (2003). Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res 991:123–32
   PubMed Web of Science ®Google Scholar
• Ossowska G, Danilczuk Z, Klenk-Majewska B, Czajkowski L, Zebrowska-Lupina I. (2004). Antidepressants in chronic unpredictable mild stress (CUMS)-induced deficit of fighting behavior. Pol J Pharmacol 56:305–11
   PubMedGoogle Scholar
• Parkhurst CN, Gan WB. (2010). Microglia dynamics and function in the CNS. Curr Opin Neurobiol 20:595–600
   PubMed Web of Science ®Google Scholar
• Perry VH, Nicoll JA, Holmes C. (2010). Microglia in neurodegenerative disease. Nat Rev Neurol 6:193–201
   PubMed Web of Science ®Google Scholar
• Poucet B, Alvernhe A, Hok V, Renaudineau S, Sargolini F, Save E. (2010). The hippocampus and the neural code of spatial memory. Biol Aujourdhui 204:103–12
   PubMedGoogle Scholar
• Riedel G, Wetzel W, Reymann KG. (1996). Comparing the role of metabotropic glutamate receptors in long-term potentiation and in learning and memory. Prog Neuropsychopharmacol Biol Psychiatr 20:761–89
   PubMed Web of Science ®Google Scholar
• Rolls ET. (2010). A computational theory of episodic memory formation in the hippocampus. Behav Brain Res 215:180–96
   PubMed Web of Science ®Google Scholar
• Sama DM, Mohmmad Abdul H, Furman JL, Artiushin IA, Szymkowski DE, Scheff SW, Norris CM. (2012). Inhibition of soluble tumor necrosis factor ameliorates synaptic alterations and Ca2+ dysregulation in aged rats. PLoS one 7:e38170
   PubMed Web of Science ®Google Scholar
• Sanderson DJ, Good MA, Seeburg PH, Sprengel R, Rawlins JN, Bannerman DM. (2008). The role of the GluR-A (GluR1) AMPA receptor subunit in learning and memory. Prog Brain Res 169:159–78
   PubMed Web of Science ®Google Scholar
• Shah PJ, Ebmeier KP, Glabus MF, Goodwin GM. (1998). Cortical grey matter reductions associated with treatment-resistant chronic unipolar depression. Controlled magnetic resonance imaging study. Br J Psychiatr 172:527–32
   PubMed Web of Science ®Google Scholar
• Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW. (1996). Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci USA 93:3908–13
   PubMed Web of Science ®Google Scholar
• Sugama S. (2009). Stress-induced microglial activation may facilitate the progression of neurodegenerative disorders. Med Hypotheses 73(6):1031–4
   PubMed Web of Science ®Google Scholar
• Tanaka S, Kondo H, Kanda K, Ashino T, Nakamachi T, Sekikawa K, Iwakura Y, et al. (2011). Involvement of interleukin-1 in lipopolysaccaride-induced microglial activation and learning and memory deficits. J Neurosci Res 89:506–14
   PubMed Web of Science ®Google Scholar
• Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J. (2001). Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21(8):2580–8
   PubMed Web of Science ®Google Scholar
• Tomas-Camardiel M, Rite I, Herrera AJ, de Pablos RM, Cano J, Machado A, Venero JL. (2004). Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxynitrite-mediated nitration of proteins, disruption of the blood-brain barrier, and damage in the nigral dopaminergic system. Neurobiol Dis 16:190–201
   PubMed Web of Science ®Google Scholar
• van Rossum D, Hanisch UK. (2004). Microglia. Metab Brain Dis 19:393–411
   PubMed Web of Science ®Google Scholar
• Vilhardt F. (2005). Microglia: phagocyte and glia cell. Int J Biochem Cell Biol 37:17–21
   PubMed Web of Science ®Google Scholar
• Walker FR, Nilsson M, Jones K. (2013). Acute and chronic stress-induced disturbances of microglial plasticity, phenotype and function. Curr Drug Targets 14(11):1262–76
   PubMed Web of Science ®Google Scholar
• Wang J, Ben Hamida S, Darcq E, Zhu W, Gibb SL, Lanfranco MF, Carnicella S, Ron D. (2012). Ethanol-mediated facilitation of AMPA receptor function in the dorsomedial striatum: implications for alcohol drinking behavior. J Neurosci: The official journal of the Society for Neuroscience 32:15124–32
   PubMed Web of Science ®Google Scholar
• Wei F, Wang GD, Kerchner GA, Kim SJ, Xu HM, Chen ZF, Zhuo M. (2001). Genetic enhancement of inflammatory pain by forebrain NR2B overexpression. Nat Neurosci 4:164–9
   PubMed Web of Science ®Google Scholar
• Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J. (1999). A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci USA 96:13496–500
   PubMed Web of Science ®Google Scholar
• Zhang M, Zheng C, Quan M, An L, Yang Z, Zhang T. (2011). Directional indicator on neural oscillations as a measure of synaptic plasticity in chronic unpredictable stress rats. Neurosignals 19:189–97
   PubMedGoogle Scholar
• Zhao F, Cai T, Liu M, Zheng G, Luo W, Chen J. (2009). Manganese induces dopaminergic neurodegeneration via microglial activation in a rat model of manganism. Toxicol Sci 107:156–64
   PubMed Web of Science ®Google Scholar
• Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, et al. (2005). Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 47:859–72
   PubMed Web of Science ®Google Scholar