Activated Microglia-Induced Deficits in Excitatory Synapses Through IL-1β: Implications for Cognitive Impairment in Sepsis

Molecular Neurobiology

Volumn 52, Issue 1, 2015, Pages 653-663

  Moraes, Carolina A ^a,b   Santos, Gabriel ^a   Spohr, Tania Cristina Leitede Sampaioe ^a   D’Avila, Joana C ^b   Lima, Flávia Regina Souza ^a   Benjamim, Claudia Farias ^a   Bozza, Fernando A ^b,c   Gomes, Flávia Carvalho Alcantara ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b Funda??o Oswaldo Cruz   (Brazil)

^c D OR INSTITUTE FOR RESEARCH AND EDUCATION IDOR   (Brazil)

Author keywords

Astrocyte; Cognitive deficit; Microglia; Sepsis; Synapse

Indexed keywords

ALLOGRAFT INFLAMMATORY FACTOR 1; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; POSTSYNAPTIC DENSITY PROTEIN 95; SYNAPTOPHYSIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; LIPOPOLYSACCHARIDE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL ACTIVATION; CELL SIZE; CELL STRUCTURE; COGNITIVE DEFECT; CONTROLLED STUDY; CYTOKINE RELEASE; EMBRYO; IMMUNOREACTIVITY; IN VITRO STUDY; MEMORY DISORDER; MICROGLIA; MOUSE; NEWBORN; NONHUMAN; PROTEIN LOCALIZATION; SEPSIS; SHORT TERM MEMORY; SIGNAL TRANSDUCTION; SYNAPSE; ANIMAL; BRAIN CORTEX; CELL CULTURE; COGNITION DISORDERS; COMPLICATION; DRUG EFFECTS; GLIOSIS; HIPPOCAMPUS; MEMORY DISORDERS; METABOLISM; NERVE CELL; PATHOLOGY;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; COGNITION DISORDERS; GLIOSIS; HIPPOCAMPUS; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MEMORY DISORDERS; MICE; MICROGLIA; NEURONS; SEPSIS; SYNAPSES;

EID: 84937975064     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-014-8868-5     Document Type: Article

References (44)

1. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29:1303–1310
2. Iwashyna TJ, Ely EW, Smith DM, Langa KM (2010) Long-term cognitive impairment and functional disability among survivors of severe sepsis. JAMA 16:1787–1794
3. Hopkins RO, Weaver LK, Collingridge D, Parkinson RB, Chan KJ, Orme JF Jr (2005) Two-year cognitive, emotional, and quality-of-life outcomes in acute respiratory distress syndrome. Am J Respir Crit Care Med 171:340–347
4. Girard TD, Jackson JC, Pandharipande PP, Pun BT, Thompson JL, Shintani AK, Gordon SM, Canonico AE, Dittus RS, Bernard GR, Ely EW (2010) Delirium as a predictor of long-term cognitive impairment in survivors of critical illness. Crit Care Med 38:1513–1520
5. Wilcox ME, Brummel NE, Archer K, Ely EW, Jackson JC, Hopkins RO (2013) Cognitive dysfunction in ICU patients: risk factors, predictors, and rehabilitation interventions. Crit Care Med 41:S81–S98
6. Polito A, Eischwald F, Maho AL, Polito A, Azabou E, Annane D, Chrétien F, Stevens RD, Carlier R, Sharshar T (2013) Pattern of brain injury in the acute setting of human septic shock. Crit Care 17:R204
7. Gofton TE, Young GB (2012) Sepsis-associated encephalopathy. Nat Rev Neurol 10:557–566
8. Bozza FA, D’Avila JC, Ritter C, Sonneville R, Sharshar T, Dal-Pizzol F (2013) Bioenergetics, mitochondrial dysfunction, and oxidative stress in the pathophysiology of septic encephalopathy. Shock 1:10–16
9. Tuon L, Comim CM, Petronilho F, Barichello T, Izquierdo I, Quevedo J, Dal-Pizzol F (2008) Time-dependent behavioral recovery after sepsis in rats. Intensive Care Med 34:1724–1731
10. Hernandes MS, D’Avila JC, Trevelin SC, Reis PA, Kinjo ER, Lopes LR, Castro-Faria-Neto HC, Cunha FQ, Britto LR, Bozza FA (2014) The role of Nox2-derived ROS in the development of cognitive impairment after sepsis. J Neuroinflammation 11:36
11. Ben Achour S, Pascual O (2010) Glia: the many ways to modulate synaptic plasticity. Neurochem Int 57:440–445
12. Tremblay ME (2011) The role of microglia at synapses in the healthy CNS: novel insights from recent imaging studies. Neuron Glia Biol 1:67–76
13. Clarke LE, Barres BA (2013) Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 14:311–321
14. Yirmiya R, Goshen I (2011) Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 25:181–213
15. Hanisch UK (2002) Microglia as a source and target of cytokines. Glia 40:140–155
16. Hamby ME, Sofroniew MV (2010) Reactive astrocytes as therapeutic targets for CNS disorders. Neurotherapeutics 7:494–506
17. Bertaina-Anglade V, Enjuanes E, Morillon D, Drieu la Rochelle C (2006) The object recognition task in rats and mice: a simple and rapid model in safety pharmacology to detect amnesic properties of a new chemical entity. J Pharmacol Toxicol Methods 54:99–105
18. Diniz LP, Almeida JC, Tortelli V, Vargas Lopes C, Setti-Perdigão P, Stipursky J, Kahn SA, Romão LF, de Miranda J, Alves-Leon SV, de Souza JM, Castro NG, Panizzutti R, Gomes FC (2012) Astrocyte-induced synaptogenesis is mediated by transforming growth factor β signaling through modulation of D-serine levels in cerebral cortex neurons. J Biol Chem 49:41432–41445
19. Lima FR, Gervais A, Colin C, Izembart M, Neto VM, Mallat M (2001) Regulation of microglial development: a novel role for thyroid hormone. J Neurosci 6:2028–2038
20. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312–318
21. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120:421–433
22. Bibb JA, Mayford MR, Tsien JZ, Alberini CM (2010) Cognition enhancement strategies. J Neurosci 30:14987–14992
23. De Felice FG, Wasilewska-Sampaio AP, Barbosa AC, Gomes FC, Klein WL, Ferreira ST (2007) Cyclic AMP enhancers and abeta oligomerization blockers as potential therapeutic agents in Alzheimer’r disease. Curr Alzheimer Res 4:263–271
24. Morfini GA, Burns M, Binder LI, Kanaan NM, LaPointe N, Bosco DA, Brown RH Jr, Brown H, Tiwari A, Hayward L, Edgar J, Nave KA, Garberrn J, Atagi Y, Song Y, Pigino G, Brady ST (2009) Axonal transport defects in neurodegenerative diseases. J Neurosci 29:12776–12786
25. Holtzman DM, Herz J, Bu G (2012) Apolipoprotein e and apolipoprotein e receptors: normal biology and roles in Alzheimer disease. Cold Spring Harb Perspect Med 2:a6312
26. Imamura Y, Wang H, Matsumoto N, Muroya T, Shimazaki J, Ogura H, Shimazu T (2011) Interleukin-1β causes long-term potentiation deficiency in a mouse model of septic encephalopathy. Neuroscience 187:63–69
27. Di Filippo M, Chiasserini D, Gardoni F, Viviani B, Tozzi A, Giampà C, Costa C, Tantucci M, Zianni E, Boraso M, Siliquini S, de Iure A, Ghiglieri V, Colcelli E, Baker D, Sarchielli P, Fusco FR, Di Luca M, Calabresi P (2013) Effects of central and peripheral inflammation on hippocampal synaptic plasticity. Neurobiol Dis 52:229–236
28. Mallat M, Chamak B (1994) Brain macrophages: neurotoxic or neurotrophic effector cells? J Leukoc Biol 56:416–422
29. Bialas AR, Stevens B (2013) TGF-β signaling regulates neuronal C1q expression and developmental synaptic refinement. Nat Neurosci 16:1773–1782
30. Lim SH, Park E, You B, Jung Y, Park AR, Park SG, Lee JR (2013) Neuronal synapse formation induced by microglia and interleukin 10. PLoS One 8:e81218
31. Stipursky J, Spohr TC, Sousa VO, Gomes FC (2012) Neuron-astroglial interactions in cell-fate commitment and maturation in the central nervous system. Neurochem Res 37:2402–2418
32. Morris GP, Clark IA, Zinn R, Vissel B (2013) Microglia: a new frontier for synaptic plasticity, learning and memory, and neurodegenerative disease research. Neurobiol Learn Mem 105:40–53
33. Šišková Z, Tremblay MÈ (2013) Microglia and synapse: interactions in health and neurodegeneration. Neural Plast 2013:425845
34. Azevedo EP, Ledo JH, Barbosa G, Sobrinho M, Diniz L, Fonseca AC, Gomes FC, Romão L, Lima FR, Palhano FL, Ferreira ST, Foguel D (2013) Activated microglia mediate synapse loss and short-term memory deficits in a mouse model of transthyretin-related oculoleptomeningeal amyloidosis. Cell Death Dis 4:e789
35. Hama H, Hara C, Yamaguchi K, Miyawaki A (2004) PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes. Neuron 41:405–415
36. Mauch DH, Nägler K, Schumacher S, Göritz C, Müller EC, Otto A, Pfrieger FW (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294:1354–1357
37. Kucukdereli H, Allen NJ, Lee AT, Feng A, Ozlu MI, Conatser LM, Chakraborty C, Workman G, Weaver M, Sage EH, Barres BA, Eroglu C (2011) Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC. Proc Natl Acad Sci USA 108:E440–E449
38. Allen NJ, Bennett ML, Foo LC, Wang GX, Chakraborty C, Smith SJ, Barres BA (2012) Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 486:410–414
39. Parkhurst CN, Yang G, Ninan I, Savas JN, Yates JR, Lafaille JJ, Hempstead BL, Littman DR, Gan WB (2013) Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 7:1596–1609
40. Welser-Alves JV, Milner R (2013) Microglia are the major source of TNF-α and TGF-β1 in postnatal glial cultures; regulation by cytokines, lipopolysaccharide, and vitronectin. Neurochem Int 1:47–53
41. Mishra A, Kim HJ, Shin AH, Thayer SA (2012) Synapse loss induced by interleukin-1β requires pre- and post-synaptic mechanisms. J Neuroimmune Pharmacol 3:571–578
42. A receptor cell-surface expression by a phosphatidylinisitol 3-kinase/Akt pathway: relevance to sepsis associated encephalopathy. J Biol Chem 281:14632–14643
43. Terrando N, Rei Fidalgo A, Vizcaychipi M, Cibelli M (2010) The impact os IL-1 modulation on the development of lipopolysaccharide-induce cognitive dysfunction. Crit Care 14:R88
44. Mina F, Comim CM, Dominguini D, Cassol-Jr OJ, Dall Igna DM, Ferreira GK, Silva MC, Galant LS, Streck EL, Quevedo J, Dal-Pizzol F (2013) IL1-β involvement in cognitive impairment after sepsis. Mol Neurobiol 49:1069–1076