How dependent is synaptic plasticity on microglial phenotype?

Neuropharmacology

Volumn 96, Issue PA, 2015, Pages 3-10

  Jones, Raasay S ^a   Lynch, Marina A ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Age; Alzheimer's disease; Astrocytes; Inflammatory cytokines; Microglia; Neuroinflammation; Neuronal function

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; B7 ANTIGEN; BRAIN DERIVED NEUROTROPHIC FACTOR; CD11B ANTIGEN; CD200 ANTIGEN; CD200 RECEPTOR; CD22 ANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; CD45 ANTIGEN; CD47 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; FC RECEPTOR; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; REGULATOR PROTEIN; SIGNAL REGULATORY PROTEIN 1ALPHA; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; AMYLOID BETA PROTEIN; AUTACOID; CYTOKINE;

ALZHEIMER DISEASE; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL MOTILITY; CHEMOTAXIS; CYTOKINE PRODUCTION; CYTOTOXICITY; DENTATE GYRUS; ENZYME SYNTHESIS; HIPPOCAMPAL CA1 REGION; HOMEOSTASIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LONG TERM POTENTIATION; MACROPHAGE; MICROGLIA; MICROGLIAL ACTIVATION; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; COMPLICATION; DISEASE MODEL; ENCEPHALITIS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ASTROCYTES; CYTOKINES; DISEASE MODELS, ANIMAL; ENCEPHALITIS; HUMANS; INFLAMMATION MEDIATORS; LONG-TERM POTENTIATION; MICROGLIA; PHENOTYPE;

EID: 84930926617     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.08.012     Document Type: Review

References (130)

1. S. Adams, L.J. van der Laan, E. Vernon-Wilson, C. Renardel de Lavalette, E.A. Dopp, C.D. Dijkstra, D.L. Simmons, and T.K. van den Berg Signal-regulatory protein is selectively expressed by myeloid and neuronal cells J. Immunol. 161 1998 1853 1859
2. H. Akiyama, S. Barger, S. Barnum, B. Bradt, J. Bauer, G.M. Cole, N.R. Cooper, P. Eikelenboom, M. Emmerling, B.L. Fiebich, C.E. Finch, S. Frautschy, W.S. Griffin, H. Hampel, M. Hull, G. Landreth, L. Lue, R. Mrak, I.R. Mackenzie, P.L. McGeer, M.K. O'Banion, J. Pachter, G. Pasinetti, C. Plata-Salaman, J. Rogers, R. Rydel, Y. Shen, W. Streit, R. Strohmeyer, I. Tooyoma, F.L. Van Muiswinkel, R. Veerhuis, D. Walker, S. Webster, B. Wegrzyniak, G. Wenk, and T. Wyss-Coray Inflammation and Alzheimer's disease Neurobiol. Aging 21 2000 383 421
3. R.M. Barrientos, E.A. Higgins, J.C. Biedenkapp, D.B. Sprunger, K.J. Wright-Hardesty, L.R. Watkins, J.W. Rudy, and S.F. Maier Peripheral infection and aging interact to impair hippocampal memory consolidation Neurobiol. Aging 27 2006 723 732
4. F.P. Bellinger, S. Madamba, and G.R. Siggins Interleukin 1 beta inhibits synaptic strength and long-term potentiation in the rat CA1 hippocampus Brain Res. 628 1993 227 234
5. E.N. Benveniste, V.T. Nguyen, and D.R. Wesemann Molecular regulation of CD40 gene expression in macrophages and microglia Brain Behav. Immun. 18 2004 7 12
6. S. Bhatia, M. Edidin, S.C. Almo, and S.G. Nathenson B7-1 and B7-2: similar costimulatory ligands with different biochemical, oligomeric and signaling properties Immunol. Lett. 104 2006 70 75
7. K. Biber, H. Neumann, K. Inoue, and H.W. Boddeke Neuronal 'On' and 'Off' signals control microglia Trends Neurosci. 30 2007 596 602
8. I. Blasko, R. Veerhuis, M. Stampfer-Kountchev, M. Saurwein-Teissl, P. Eikelenboom, and B. Grubeck-Loebenstein Costimulatory effects of interferon-gamma and interleukin-1beta or tumor necrosis factor alpha on the synthesis of Abeta1-40 and Abeta1-42 by human astrocytes Neurobiol. Dis. 7 2000 682 689
9. D. Boche, and J.A. Nicoll The role of the immune system in clearance of Abeta from the brain Brain Pathol. 18 2008 267 278
10. N. Braidy, P. Munoz, A.G. Palacios, G. Castellano-Gonzalez, N.C. Inestrosa, R.S. Chung, P. Sachdev, and G.J. Guillemin Recent rodent models for Alzheimer's disease: clinical implications and basic research J. Neural Transm. 119 2012 173 195
11. A.E. Cardona, E.P. Pioro, M.E. Sasse, V. Kostenko, S.M. Cardona, I.M. Dijkstra, D. Huang, G. Kidd, S. Dombrowski, R. Dutta, J.C. Lee, D.N. Cook, S. Jung, S.A. Lira, D.R. Littman, and R.M. Ransohoff Control of microglial neurotoxicity by the fractalkine receptor Nat. Neurosci. 9 2006 917 924
12. D. Carnevale, R. De Simone, and L. Minghetti Microglia-neuron interaction in inflammatory and degenerative diseases: role of cholinergic and noradrenergic systems CNS Neurol. Disord. Drug Targets 6 2007 388 397
13. P.F. Chapman, G.L. White, M.W. Jones, D. Cooper-Blacketer, V.J. Marshall, M. Irizarry, L. Younkin, M.A. Good, T.V. Bliss, B.T. Hyman, S.G. Younkin, and K.K. Hsiao Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice Nat. Neurosci. 2 1999 271 276
14. H. Chen, E. Jacobs, M.A. Schwarzschild, M.L. McCullough, E.E. Calle, M.J. Thun, and A. Ascherio Nonsteroidal antiinflammatory drug use and the risk for Parkinson's disease Ann. Neurol. 58 2005 963 967
15. J. Chen, J.B. Buchanan, N.L. Sparkman, J.P. Godbout, G.G. Freund, and R.W. Johnson Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system Brain Behav. Immun. 22 2008 301 311
16. K. Chen, J. Huang, W. Gong, L. Zhang, P. Yu, and J.M. Wang CD40/CD40L dyad in the inflammatory and immune responses in the central nervous system Cell. Mol. Immunol. 3 2006 163 169
17. J.D. Cherry, J.A. Olschowka, and M.K. O'Banion Neuroinflammation and M2 microglia: the good, the bad, and the inflamed J. Neuroinflammation 11 2014 98
18. V. Chhor, T. Le Charpentier, S. Lebon, M.V. Ore, I.L. Celador, J. Josserand, V. Degos, E. Jacotot, H. Hagberg, K. Savman, C. Mallard, P. Gressens, and B. Fleiss Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia in vitro Brain Behav. Immun. 32 2013 70 85
19. R.M. Clarke, A. Lyons, F. O'Connell, B.F. Deighan, C.E. Barry, N.G. Anyakoha, A. Nicolaou, and M.A. Lynch A pivotal role for interleukin-4 in atorvastatin-associated neuroprotection in rat brain J. Biol. Chem. 283 2008 1808 1817
20. R.M. Clarke, F. O'Connell, A. Lyons, and M.A. Lynch The HMG-CoA reductase inhibitor, atorvastatin, attenuates the effects of acute administration of amyloid-beta1-42 in the rat hippocampus in vivo Neuropharmacology 52 2007 136 145
21. C.A. Colton, and D.M. Wilcock Assessing activation states in microglia CNS Neurol. Disord. Drug Targets 9 2010 174 191
22. C.K. Combs, J.C. Karlo, S.C. Kao, and G.E. Landreth Beta-amyloid stimulation of microglia and monocytes results in TNF alpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis J. Neurosci. 21 2001 1179 1188
23. R. Corti, R. Hutter, J.J. Badimon, and V. Fuster Evolving concepts in the triad of atherosclerosis, inflammation and thrombosis J. Thromb. Thrombolysis 17 2004 35 44
24. D.A. Costello, A. Lyons, S. Denieffe, T.C. Browne, F.F. Cox, and M.A. Lynch Long term potentiation is impaired in membrane glycoprotein CD200-deficient mice: a role for Toll-like receptor activation J. Biol. Chem. 286 2011 34722 34732
25. T.R. Cowley, J. O'Sullivan, C. Blau, B.F. Deighan, R. Jones, C. Kerskens, J.C. Richardson, D. Virley, N. Upton, and M.A. Lynch Rosiglitazone attenuates the age-related changes in astrocytosis and the deficit in LTP Neurobiol. Aging 33 2012 162 175
26. F.F. Cox, V. Berezin, E. Bock, and M.A. Lynch The neural cell adhesion molecule-derived peptide, FGL, attenuates lipopolysaccharide-induced changes in glia in a CD200-dependent manner Neuroscience 235 2013 141 148
27. F.F. Cox, D. Carney, A.M. Miller, and M.A. Lynch CD200 fusion protein decreases microglial activation in the hippocampus of aged rats Brain Behav. Immun. 26 2012 789 796
28. W.K. Cullen, Y.H. Suh, R. Anwyl, and M.J. Rowan Block of LTP in rat hippocampus in vivo by beta-amyloid precursor protein fragments Neuroreport 8 1997 3213 3217
29. A.J. Cunningham, C.A. Murray, L.A. O'Neill, M.A. Lynch, and J.J. O'Connor Interleukin-1 beta (IL-1 beta) and tumour necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro Neurosci. Lett. 203 1996 17 20
30. L.F. Eng, R.S. Ghirnikar, and Y.L. Lee Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000) Neurochem. Res. 25 2000 1439 1451
31. E. Esposito, V. Di Matteo, A. Benigno, M. Pierucci, G. Crescimanno, and G. Di Giovanni Non-steroidal anti-inflammatory drugs in Parkinson's disease Exp. Neurol. 205 2007 295 312
32. S.A. Frautschy, W. Hu, P. Kim, S.A. Miller, T. Chu, M.E. Harris-White, and G.M. Cole Phenolic anti-inflammatory antioxidant reversal of Abeta-induced cognitive deficits and neuropathology Neurobiol. Aging 22 2001 993 1005
33. D.B. Freir, C. Holscher, and C.E. Herron Blockade of long-term potentiation by beta-amyloid peptides in the CA1 region of the rat hippocampus in vivo J. Neurophysiol. 85 2001 708 713
34. S. Fuller, M. Steele, and G. Munch Activated astroglia during chronic inflammation in Alzheimer's disease - do they neglect their neurosupportive roles? Mutat. Res. 690 1-2 2009 40 49
35. E. Gahtan, and J.B. Overmier Performance more than working memory disrupted by acute systemic inflammation in rats in appetitive tasks Physiol. Behav. 73 1-2 2001 201 210
36. J.J. Gallagher, M.E. Finnegan, B. Grehan, J. Dobson, J.F. Collingwood, and M.A. Lynch Modest amyloid deposition is associated with iron dysregulation, microglial activation, and oxidative stress J. Alzheimers Dis. 28 2012 147 161
37. J.J. Gallagher, A.M. Minogue, and M.A. Lynch Impaired performance of female APP/PS1 mice in the Morris water maze is coupled with increased Abeta accumulation and microglial activation Neurodegener. Dis. 11 2013 33 41
38. M. Gibertini Cytokines and cognitive behavior Neuroimmunomodulation 5 3-4 1998 160 165
39. F. Ginhoux, M. Greter, M. Leboeuf, S. Nandi, P. See, S. Gokhan, M.F. Mehler, S.J. Conway, L.G. Ng, E.R. Stanley, I.M. Samokhvalov, and M. Merad Fate mapping analysis reveals that adult microglia derive from primitive macrophages Science 330 2010 841 845
40. S. Gordon Alternative activation of macrophages Nat. Rev. Immunol. 3 2003 23 35
41. S.A. Grathwohl, R.E. Kalin, T. Bolmont, S. Prokop, G. Winkelmann, S.A. Kaeser, J. Odenthal, R. Radde, T. Eldh, S. Gandy, A. Aguzzi, M. Staufenbiel, P.M. Mathews, H. Wolburg, F.L. Heppner, and M. Jucker Formation and maintenance of Alzheimer's disease beta-amyloid plaques in the absence of microglia Nat. Neurosci. 12 2009 1361 1363
42. R.J. Greenwald, G.J. Freeman, and A.H. Sharpe The B7 family revisited Annu Rev. Immunol. 23 2005 515 548
43. M.M. Halassa, T. Fellin, and P.G. Haydon The tripartite synapse: roles for gliotransmission in health and disease Trends Mol. Med. 13 2007 54 63
44. U.K. Hanisch Functional diversity of microglia - how heterogeneous are they to begin with? Front. Cell. Neurosci. 7 2013 65
45. J.K. Harrison, Y. Jiang, S. Chen, Y. Xia, D. Maciejewski, R.K. McNamara, W.J. Streit, M.N. Salafranca, S. Adhikari, D.A. Thompson, P. Botti, K.B. Bacon, and L. Feng Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia Proc. Natl. Acad. Sci. U. S. A. 95 1998 10896 10901
46. A.D. Hart, A. Wyttenbach, V.H. Perry, and J.L. Teeling Age related changes in microglial phenotype vary between CNS regions: grey versus white matter differences Brain Behav. Immun. 26 2012 754 765
47. M.T. Heneka, and M.K. O'Banion Inflammatory processes in Alzheimer's disease J. Neuroimmunol. 184 2007 69 91
48. K. Hensley Neuroinflammation in Alzheimer's disease: mechanisms, pathologic consequences, and potential for therapeutic manipulation J. Alzheimers Dis. 21 2010 1 14
49. S.E. Hickman, E.K. Allison, and J. El Khoury Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice J. Neurosci. 28 2008 8354 8360
50. E. Hjorth, M. Zhu, V.C. Toro, I. Vedin, J. Palmblad, T. Cederholm, Y. Freund-Levi, G. Faxen-Irving, L.O. Wahlund, H. Basun, M. Eriksdotter, and M. Schultzberg Omega-3 fatty acids enhance phagocytosis of Alzheimer's disease-related amyloid-beta42 by human microglia and decrease inflammatory markers J. Alzheimers Dis. 35 2013 697 713
51. A. Itoh, T. Akaike, M. Sokabe, A. Nitta, R. Iida, A. Olariu, K. Yamada, and T. Nabeshima Impairments of long-term potentiation in hippocampal slices of beta-amyloid-infused rats Eur. J. Pharmacol. 382 1999 167 175
52. M.C. Janelsins, M.A. Mastrangelo, K.M. Park, K.L. Sudol, W.C. Narrow, S. Oddo, F.M. LaFerla, L.M. Callahan, H.J. Federoff, and W.J. Bowers Chronic neuron-specific tumor necrosis factor-alpha expression enhances the local inflammatory environment ultimately leading to neuronal death in 3× Tg-AD mice Am. J. Pathol. 173 2008 1768 1782
53. H. Katsuki, S. Nakai, Y. Hirai, K. Akaji, Y. Kiso, and M. Satoh Interleukin-1 beta inhibits long-term potentiation in the CA3 region of mouse hippocampal slices Eur. J. Pharmacol. 181 1990 323 326
54. A. Kelly, A. Lynch, E. Vereker, Y. Nolan, P. Queenan, E. Whittaker, L.A. O'Neill, and M.A. Lynch The anti-inflammatory cytokine, interleukin (IL)-10, blocks the inhibitory effect of IL-1 beta on long term potentiation. A role for JNK J. Biol. Chem. 276 2001 45564 45572
55. L. Kelly, B. Grehan, A.D. Chiesa, S.M. O'Mara, E. Downer, G. Sahyoun, K.A. Massey, A. Nicolaou, and M.A. Lynch The polyunsaturated fatty acids, EPA and DPA exert a protective effect in the hippocampus of the aged rat Neurobiol. Aging 32 2318 2011 e2311 2315
56. R.J. Kelly, A.M. Minogue, A. Lyons, R.S. Jones, T.C. Browne, D.A. Costello, S. Denieffe, C. O'Sullivan, T.J. Connor, and M.A. Lynch Glial activation in Abeta PP/PS1 mice is associated with infiltration of IFN gamma-producing cells J. Alzheimers Dis. 37 2013 63 75
57. I. Klyubin, D.M. Walsh, W.K. Cullen, J.V. Fadeeva, R. Anwyl, D.J. Selkoe, and M.J. Rowan Soluble arctic amyloid beta protein inhibits hippocampal long-term potentiation in vivo Eur. J. Neurosci. 19 2004 2839 2846
58. J. Koenigsknecht, and G. Landreth Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism J. Neurosci. 24 2004 9838 9846
59. J. Koenigsknecht-Talboo, and G.E. Landreth Microglial phagocytosis induced by fibrillar beta-amyloid and IgGs are differentially regulated by proinflammatory cytokines J. Neurosci. 25 2005 8240 8249
60. J. Koenigsknecht-Talboo, M. Meyer-Luehmann, M. Parsadanian, M. Garcia-Alloza, M.B. Finn, B.T. Hyman, B.J. Bacskai, and D.M. Holtzman Rapid microglial response around amyloid pathology after systemic anti-Abeta antibody administration in PDAPP mice J. Neurosci. 28 2008 14156 14164
61. R.M. Koffie, B.T. Hyman, and T.L. Spires-Jones Alzheimer's disease: synapses gone cold Mol. Neurodegener. 6 2011 63
62. L. Launer Nonsteroidal anti-inflammatory drug use and the risk for Alzheimer's disease: dissecting the epidemiological evidence Drugs 63 2003 731 739
63. L.J. Lawson, V.H. Perry, P. Dri, and S. Gordon Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain Neuroscience 39 1990 151 170
64. M. Lee, C. Schwab, and P.L. McGeer Astrocytes are GABAergic cells that modulate microglial activity Glia 59 2011 152 165
65. C. Li, A. Ebrahimi, and H. Schluesener Drug pipeline in neurodegeneration based on transgenic mice models of Alzheimer's disease Ageing Res. Rev. 12 2013 116 140
66. D.J. Loane, B.A. Stoica, A. Pajoohesh-Ganji, K.R. Byrnes, and A.I. Faden Activation of metabotropic glutamate receptor 5 modulates microglial reactivity and neurotoxicity by inhibiting NADPH oxidase J. Biol. Chem. 284 2009 15629 15639
67. C.M. Long-Smith, A.M. Sullivan, and Y.M. Nolan The influence of microglia on the pathogenesis of Parkinson's disease Prog. Neurobiol. 89 2009 277 287
68. A.M. Lynch, D.J. Loane, A.M. Minogue, R.M. Clarke, D. Kilroy, R.E. Nally, O.J. Roche, F. O'Connell, and M.A. Lynch Eicosapentaenoic acid confers neuroprotection in the amyloid-beta challenged aged hippocampus Neurobiol. Aging 28 2007 845 855
69. M.A. Lynch The multifaceted profile of activated microglia Mol. Neurobiol. 40 2009 139 156
70. M.A. Lynch Age-related neuroinflammatory changes negatively impact on neuronal function Front. Aging Neurosci. 1 2010 6
71. M.A. Lynch The impact of neuroimmune changes on development of amyloid pathology; relevance to Alzheimer's disease Immunology 141 3 2013 292 301
72. A. Lyons, E.J. Downer, D.A. Costello, N. Murphy, and M.A. Lynch Dok2 mediates the CD200Fc attenuation of Abeta-induced changes in glia J. Neuroinflammation 9 2012 107
73. A. Lyons, E.J. Downer, S. Crotty, Y.M. Nolan, K.H. Mills, and M.A. Lynch CD200 ligand receptor interaction modulates microglial activation in vivo and in vitro: a role for IL-4 J. Neurosci. 27 2007 8309 8313
74. A. Lyons, R.J. Griffin, C.E. Costelloe, R.M. Clarke, and M.A. Lynch IL-4 attenuates the neuroinflammation induced by amyloid-beta in vivo and in vitro J. Neurochem. 101 2007 771 781
75. A. Lyons, A.M. Lynch, E.J. Downer, R. Hanley, J.B. O'Sullivan, A. Smith, and M.A. Lynch Fractalkine-induced activation of the phosphatidylinositol-3 kinase pathway attentuates microglial activation in vivo and in vitro J. Neurochem. 110 2009 1547 1556
76. A. Lyons, K. McQuillan, B.F. Deighan, J.A. O'Reilly, E.J. Downer, A.C. Murphy, M. Watson, A. Piazza, F. O'Connell, R. Griffin, K.H. Mills, and M.A. Lynch Decreased neuronal CD200 expression in IL-4-deficient mice results in increased neuroinflammation in response to lipopolysaccharide Brain Behav. Immun. 23 2009 1020 1027
77. F.O. Maher, R.M. Clarke, A. Kelly, R.E. Nally, and M.A. Lynch Interaction between interferon gamma and insulin-like growth factor-1 in hippocampus impacts on the ability of rats to sustain long-term potentiation J. Neurochem. 96 2006 1560 1571
78. S.F. Maier, and L.R. Watkins Intracerebroventricular interleukin-1 receptor antagonist blocks the enhancement of fear conditioning and interference with escape produced by inescapable shock Brain Res. 695 2 1995 279 282
79. S. Mandrekar-Colucci, J.C. Karlo, and G.E. Landreth Mechanisms underlying the rapid peroxisome proliferator-activated receptor-gamma-mediated amyloid clearance and reversal of cognitive deficits in a murine model of Alzheimer's disease J. Neurosci. 32 2012 10117 10128
80. C. Marchetti, and H. Marie Hippocampal synaptic plasticity in Alzheimer's disease: what have we learned so far from transgenic models? Rev. Neurosci. 22 2011 373 402
81. M.A. Mastrangelo, and W.J. Bowers Detailed immunohistochemical characterization of temporal and spatial progression of Alzheimer's disease-related pathologies in male triple-transgenic mice BMC Neurosci. 9 2008 81
82. E.G. McGeer, and P.L. McGeer Inflammatory processes in Alzheimer's disease Prog. Neuropsychopharmacol. Biol. Psychiatry 27 2003 741 749
83. P.L. McGeer, and E.G. McGeer Glial reactions in Parkinson's disease Mov. Disord. 23 2008 474 483
84. R.M. McManus, S.C. Higgins, K.H. Mills, and M.A. Lynch Respiratory infection promotes T cell infiltration and amyloid-beta deposition in APP/PS1 mice Neurobiol. Aging 35 2014 109 121
85. K. McQuillan, M.A. Lynch, and K.H. Mills Activation of mixed glia by Abeta-specific Th1 and Th17 cells and its regulation by Th2 cells Brain Behav. Immun. 24 2010 598 607
86. K.J. Min, M.S. Yang, S.U. Kim, I. Jou, and E.H. Joe Astrocytes induce hemeoxygenase-1 expression in microglia: a feasible mechanism for preventing excessive brain inflammation J. Neurosci. 26 2006 1880 1887
87. A.M. Minogue, R.S. Jones, R.J. Kelly, C.L. McDonald, T.J. Connor, and M.A. Lynch Age-associated dysregulation of microglial activation is coupled with enhanced blood-brain barrier permeability and pathology in APP/PS1 mice Neurobiol. Aging 35 2014 1442 1452
88. A.M. Minogue, A.M. Lynch, D.J. Loane, C.E. Herron, and M.A. Lynch Modulation of amyloid-beta-induced and age-associated changes in rat hippocampus by eicosapentaenoic acid J. Neurochem. 103 2007 914 926
89. A.M. Minogue, A.W. Schmid, M.P. Fogarty, A.C. Moore, V.A. Campbell, C.E. Herron, and M.A. Lynch Activation of the c-Jun N-terminal kinase signaling cascade mediates the effect of amyloid-beta on long term potentiation and cell death in hippocampus: a role for interleukin-1beta? J. Biol. Chem. 278 2003 27971 27980
90. M. Mittelbronn, K. Dietz, H.J. Schluesener, and R. Meyermann Local distribution of microglia in the normal adult human central nervous system differs by up to one order of magnitude Acta Neuropathol. 101 2001 249 255
91. M. Moore, A. Piazza, Y. Nolan, and M.A. Lynch Treatment with dexamethasone and vitamin D3 attenuates neuroinflammatory age-related changes in rat hippocampus Synapse 61 2007 851 861
92. S.C. Morgan, D.L. Taylor, and J.M. Pocock Microglia release activators of neuronal proliferation mediated by activation of mitogen-activated protein kinase, phosphatidylinositol-3-kinase/Akt and delta-notch signalling cascades J. Neurochem. 90 2004 89 101
93. D.M. Mosser The many faces of macrophage activation J. Leukoc. Biol. 73 2003 209 212
94. R.T. Mott, G. Ait-Ghezala, T. Town, T. Mori, M. Vendrame, J. Zeng, J. Ehrhart, M. Mullan, and J. Tan Neuronal expression of CD22: novel mechanism for inhibiting microglial proinflammatory cytokine production Glia 46 2004 369 379
95. C.A. Murray, and M.A. Lynch Evidence that increased hippocampal expression of the cytokine interleukin-1 beta is a common trigger for age- and stress-induced impairments in long-term potentiation J. Neurosci. 18 1998 2974 2981
96. A. Nagai, S. Mishima, Y. Ishida, H. Ishikura, T. Harada, S. Kobayashi, and S.U. Kim Immortalized human microglial cell line: phenotypic expression J. Neurosci. Res. 81 2005 342 348
97. S. Nakamura, N. Murayama, T. Noshita, H. Annoura, and T. Ohno Progressive brain dysfunction following intracerebroventricular infusion of beta(1-42)-amyloid peptide Brain Res. 912 2001 128 136
98. V.T. Nguyen, and E.N. Benveniste IL-4-activated STAT-6 inhibits IFN-gamma-induced CD40 gene expression in macrophages/microglia J. Immunol. 165 2000 6235 6243
99. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo Science 308 2005 1314 1318
100. A. Nitta, T. Fukuta, T. Hasegawa, and T. Nabeshima Continuous infusion of beta-amyloid protein into the rat cerebral ventricle induces learning impairment and neuronal and morphological degeneration Jpn. J. Pharmacol. 73 1997 51 57
101. Y. Nolan, F.O. Maher, D.S. Martin, R.M. Clarke, M.T. Brady, A.E. Bolton, K.H. Mills, and M.A. Lynch Role of interleukin-4 in regulation of age-related inflammatory changes in the hippocampus J. Biol. Chem. 280 2005 9354 9362
102. M.S. Oitzl, H. van Oers, B. Schöbitz, and E.R. de Kloet Interleukin-1 beta, but not interleukin-6, impairs spatial navigation learning Brain Res. 613 1 1993 160 163
103. J.A. O'Reilly, and M. Lynch Rosiglitazone improves spatial memory and decreases insoluble Abeta(1-42) in APP/PS1 mice J. Neuroimmune Pharmacol. 7 2012 140 144
104. S. Oddo, A. Caccamo, J.D. Shepherd, M.P. Murphy, T.E. Golde, R. Kayed, R. Metherate, M.P. Mattson, Y. Akbari, and F.M. LaFerla Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction Neuron 39 2003 409 421
105. T. Ondrejcak, I. Klyubin, N.W. Hu, A.E. Barry, W.K. Cullen, and M.J. Rowan Alzheimer's disease amyloid beta-protein and synaptic function Neuromolecular Med. 12 2010 13 26
106. Y. Ouchi, S. Yagi, M. Yokokura, and M. Sakamoto Neuroinflammation in the living brain of Parkinson's disease Park. Relat. Disord. 15 Suppl. 3 2009 S200 S204
107. X.D. Pan, Y.G. Zhu, N. Lin, J. Zhang, Q.Y. Ye, H.P. Huang, and X.C. Chen Microglial phagocytosis induced by fibrillar beta-amyloid is attenuated by oligomeric beta-amyloid: implications for Alzheimer's disease Mol. Neurodegener. 6 2011 45
108. O. Pascual, S. Ben Achour, P. Rostaing, A. Triller, and A. Bessis Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission Proc. Natl. Acad. Sci. U. S. A. 109 2012 E197 E205
109. C.R. Pugh, K. Kumagawa, M. Fleshner, L.R. Watkins, S.F. Maier, and J.W. Rudy Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain Behav Immun. 12 3 1998 212 229
110. C.R. Pugh, K.T. Nguyen, J.L. Gonyea, M. Fleshner, L.R. Wakins, S.F. Maier, and J.W. Rudy Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation Behav. Brain Res. 106 1-2 1999 109 118
111. C.R. Pugh, J.D. Johnson, D. Martin, J.W. Rudy, S.F. Maier, and L.R. Watkins Human immunodeficiency virus-1 coat protein gp120 impairs contextual fear conditioning: a potential role in AIDS related learning and memory impairments Brain Res. 861 1 2000 8 15
112. H. Qin, C.A. Wilson, S.J. Lee, X. Zhao, and E.N. Benveniste LPS induces CD40 gene expression through the activation of NF-kappaB and STAT-1alpha in macrophages and microglia Blood 106 2005 3114 3122
113. L. Ren, B. Lubrich, K. Biber, and P.J. Gebicke-Haerter Differential expression of inflammatory mediators in rat microglia cultured from different brain regions Brain Res. Mol. Brain Res. 65 1999 198 205
114. J.B. Rich, D.X. Rasmusson, M.F. Folstein, K.A. Carson, C. Kawas, and J. Brandt Nonsteroidal anti-inflammatory drugs in Alzheimer's disease Neurology 45 1995 51 55
115. D.A. Solovjov, E. Pluskota, and E.F. Plow Distinct roles for the alpha and beta subunits in the functions of integrin alphaMbeta2 J. Biol. Chem. 280 2005 1336 1345
116. M. Stein, S. Keshav, N. Harris, and S. Gordon Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation J. Exp. Med. 176 1992 287 292
117. W.J. Streit, S.A. Walter, and N.A. Pennell Reactive microgliosis Prog. Neurobiol. 57 1999 563 581
118. J. Tan, T. Town, T. Mori, D. Obregon, Y. Wu, A. DelleDonne, A. Rojiani, F. Crawford, R.A. Flavell, and M. Mullan CD40 is expressed and functional on neuronal cells EMBO J. 21 2002 643 652
119. F. Trinchese, S. Liu, F. Battaglia, S. Walter, P.M. Mathews, and O. Arancio Progressive age-related development of Alzheimer-like pathology in APP/PS1 mice Ann. Neurol. 55 2004 801 814
120. S.C. Vlad, D.R. Miller, N.W. Kowall, and D.T. Felson Protective effects of NSAIDs on the development of Alzheimer disease Neurology 70 2008 1672 1677
121. R. von Bernhardi, and G. Ramirez Microglia-astrocyte interaction in Alzheimer's disease: friends or foes for the nervous system? Biol. Res. 34 2001 123 128
122. H. Wake, A.J. Moorhouse, S. Jinno, S. Kohsaka, and J. Nabekura Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals J. Neurosci. 29 2009 3974 3980
123. D.M. Walsh, I. Klyubin, J.V. Fadeeva, W.K. Cullen, R. Anwyl, M.S. Wolfe, M.J. Rowan, and D.J. Selkoe Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo Nature 416 2002 535 539
124. C. Weber, W. Erl, K.S. Weber, and P.C. Weber HMG-CoA reductase inhibitors decrease CD11b expression and CD11b-dependent adhesion of monocytes to endothelium and reduce increased adhesiveness of monocytes isolated from patients with hypercholesterolemia J. Am. Coll. Cardiol. 30 1997 1212 1217
125. D.M. Wilcock, G. DiCarlo, D. Henderson, J. Jackson, K. Clarke, K.E. Ugen, M.N. Gordon, and D. Morgan Intracranially administered anti-Abeta antibodies reduce beta-amyloid deposition by mechanisms both independent of and associated with microglial activation J. Neurosci. 23 2003 3745 3751
126. D.M. Wilcock, A. Rojiani, A. Rosenthal, S. Subbarao, M.J. Freeman, M.N. Gordon, and D. Morgan Passive immunotherapy against Abeta in aged APP-transgenic mice reverses cognitive deficits and depletes parenchymal amyloid deposits in spite of increased vascular amyloid and microhemorrhage J. Neuroinflammation 1 2004 24
127. S.A. Wolf, U. Gimsa, I. Bechmann, and R. Nitsch Differential expression of costimulatory molecules B7-1 and B7-2 on microglial cells induced by Th1 and Th2 cells in organotypic brain tissue Glia 36 2001 414 420
128. K. Yamada, T. Tanaka, D. Han, K. Senzaki, T. Kameyama, and T. Nabeshima Protective effects of idebenone and alpha-tocopherol on beta-amyloid-(1-42)-induced learning and memory deficits in rats: implication of oxidative stress in beta-amyloid-induced neurotoxicity in vivo Eur. J. Neurosci. 11 1999 83 90
129. A. Zameer, and S.A. Hoffman Increased ICAM-1 and VCAM-1 expression in the brains of autoimmune mice J. Neuroimmunol. 142 2003 67 74
130. J. Zhao, T. O'Connor, and R. Vassar The contribution of activated astrocytes to Abeta production: implications for Alzheimer's disease pathogenesis J. Neuroinflammation 8 2011 150