Neuroinflammation in the normal aging hippocampus

Neuroscience

Volumn 309, Issue , 2015, Pages 84-99

  Barrientos, R M ^a   Kitt, M M ^a   Watkins, L R ^a   Maier, S F ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Danger signals; Memory impairments; Microglial priming; Neuroendocrine dysregulation; Neuroinflammation; Normal aging

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; ALPHA TOCOPHEROL; ARACHIDONIC ACID; ASCORBIC ACID; BLUEBERRY EXTRACT; BRAIN DERIVED NEUROTROPHIC FACTOR; CD200 RECEPTOR; CELL PROTEIN; CELL RECEPTOR; CENTRAL NERVOUS SYSTEM AGENTS; COLECALCIFEROL; COMPLEMENT COMPONENT C3 RECEPTOR; CORTICOSTERONE; CRYOPYRIN; EXCITATORY AMINO ACID TRANSPORTER; FRACTALKINE; GLUCOCORTICOID RECEPTOR; INTERLEUKIN 1 RECEPTOR A; INTERLEUKIN 1BETA; INTERLEUKIN 6; MINOCYCLINE; NEUROTROPHIN RECEPTOR P75; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PROTEIN ARC; RESVERATROL; SYNAPTOPHYSIN; THIOCTIC ACID; UNCLASSIFIED DRUG; UNINDEXED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1;

AGING; ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; B LYMPHOCYTE; CELL ACTIVATION; DIET SUPPLEMENTATION; DISEASE PREDISPOSITION; DRUG HALF LIFE; ENZYME ACTIVITY; EXERCISE; FRUIT; GENE EXPRESSION; HIPPOCAMPUS; HUMAN; IMMUNE SYSTEM; IMMUNOPHENOTYPING; INFECTION; LONG TERM MEMORY; LONG TERM POTENTIATION; LYMPHOCYTE PROLIFERATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMORY DISORDER; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PATHOPHYSIOLOGY; POSTOPERATIVE COGNITIVE DECLINE; POSTOPERATIVE COMPLICATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SENSITIZATION; SPINACH; T LYMPHOCYTE; TRAUMATIC BRAIN INJURY; ANIMAL; DRUG EFFECTS; IMMUNOLOGY; IMMUNOMODULATION; MEMORY; PHYSIOLOGY; PSYCHOLOGY;

AGING; ANIMALS; HIPPOCAMPUS; HUMANS; MEMORY; MICROGLIA; NEUROIMMUNOMODULATION;

EID: 84945445235     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.03.007     Document Type: Review

References (226)

1. Abraham J., Johnson R.W. Central inhibition of interleukin-1beta ameliorates sickness behavior in aged mice. Brain Behav Immun 2009, 23:396-401.
2. Abraham J., Johnson R.W. Consuming a diet supplemented with resveratrol reduced infection-related neuroinflammation and deficits in working memory in aged mice. Rejuvenation Res 2009, 12:445-453.
3. Abraham J., Jang S., Godbout J.P., Chen J., Kelley K.W., Dantzer R., Johnson R.W. Aging sensitizes mice to behavioral deficits induced by central HIV-1 gp120. Neurobiol Aging 2008, 29:614-621.
4. Akana S.F., Strack A.M., Hanson E.S., Horsley C.J., Milligan E.D., Bhatnagar S., Dallman M.F. Interactions among chronic cold, corticosterone and puberty on energy intake and deposition. Stress 1999, 3:131-146.
5. 2014 Alzheimer's disease facts and figures. Alzheimers Dement 2014, 10:e47-e92. Alzheimer's Association.
6. Anttila S.K. Diseases and symptoms as predictors of hospital care in an aged population. A prospective register-based study. Scand J Soc Med 1992, 20:79-84.
7. Bachstetter A.D., Morganti J.M., Jernberg J., Schlunk A., Mitchell S.H., Brewster K.W., Hudson C.E., Cole M.J., Harrison J.K., Bickford P.C., Gemma C. Fractalkine and CX 3 CR1 regulate hippocampal neurogenesis in adult and aged rats. Neurobiol Aging 2011, 32:2030-2044.
8. Ban E., Milon G., Prudhomme N., Fillion G., Haour F. Receptors for interleukin-1 (alpha and beta) in mouse brain: mapping and neuronal localization in hippocampus. Neuroscience 1991, 43:21-30.
9. Ban E., Marquette C., Sarrieau A., Fitzpatrick F., Fillion G., Milon G., Rostene W., Haour F. Regulation of interleukin-1 receptor expression in mouse brain and pituitary by lipopolysaccharide and glucocorticoids. Neuroendocrinology 1993, 58:581-587.
10. Banks W.A., Kastin A.J., Brennan J.M., Vallance K.L. Adsorptive endocytosis of HIV-1gp120 by blood-brain barrier is enhanced by lipopolysaccharide. Exp Neurol 1999, 156:165-171.
11. Bao T.H., Miao W., Han J.H., Yin M., Yan Y., Wang W.W., Zhu Y.H. Spontaneous running wheel improves cognitive functions of mouse associated with miRNA expressional alteration in hippocampus following traumatic brain injury. J Mol Neurosci 2014, 54:622-629.
12. Barrientos R.M. Voluntary exercise as an anti-neuroinflammatory therapeutic. Brain Behav Immun 2011, 25:1061-1062.
13. Barrientos R.M., Higgins E.A., Sprunger D.B., Watkins L.R., Rudy J.W., Maier S.F. Memory for context is impaired by a post context exposure injection of interleukin-1 beta into dorsal hippocampus. Behav Brain Res 2002, 134:291-298.
14. Barrientos R.M., O'Reilly R.C., Rudy J.W. Memory for context is impaired by injecting anisomycin into dorsal hippocampus following context exploration. Behav Brain Res 2002, 134:299-306.
15. Barrientos R.M., Sprunger D.B., Campeau S., Higgins E.A., Watkins L.R., Rudy J.W., Maier S.F. Brain-derived neurotrophic factor mRNA downregulation produced by social isolation is blocked by intrahippocampal interleukin-1 receptor antagonist. Neuroscience 2003, 121:847-853.
16. Barrientos R.M., Sprunger D.B., Campeau S., Watkins L.R., Rudy J.W., Maier S.F. BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1beta administration. J Neuroimmunol 2004, 155:119-126.
17. Barrientos R.M., Higgins E.A., Biedenkapp J.C., Sprunger D.B., Wright-Hardesty K.J., Watkins L.R., Rudy J.W., Maier S.F. Peripheral infection and aging interact to impair hippocampal memory consolidation. Neurobiol Aging 2006, 27:723-732.
18. Barrientos R.M., Frank M.G., Hein A.M., Higgins E.A., Watkins L.R., Rudy J.W., Maier S.F. Time course of hippocampal IL-1 beta and memory consolidation impairments in aging rats following peripheral infection. Brain Behav Immun 2009, 23:46-54.
19. Barrientos R.M., Watkins L.R., Rudy J.W., Maier S.F. Characterization of the sickness response in young and aging rats following E. coli infection. Brain Behav Immun 2009, 23:450-454.
20. Barrientos R.M., Frank M.G., Watkins L.R., Maier S.F. Memory impairments in healthy aging: role of aging-induced microglial sensitization. Aging Dis 2010, 1:212-231.
21. Barrientos R.M., Frank M.G., Crysdale N.Y., Chapman T.R., Ahrendsen J.T., Day H.E., Campeau S., Watkins L.R., Patterson S.L., Maier S.F. Little exercise, big effects: reversing aging and infection-induced memory deficits, and underlying processes. J Neurosci 2011, 31:11578-11586.
22. Barrientos R.M., Hein A.M., Frank M.G., Watkins L.R., Maier S.F. Intracisternal interleukin-1 receptor antagonist prevents postoperative cognitive decline and neuroinflammatory response in aged rats. J Neurosci 2012, 32:14641-14648.
23. Barrientos R.M., Thompson V.M., Arnold T.H., Frank M.G., Watkins L.R., Maier S.F. The role of hepatic and splenic macrophages in E. coli-induced memory impairments in aged rats. Brain Behav Immun 2015, 43:60-67.
24. Barrientos R.M., Thompson V.M., Kitt M.M., Amat J., Hale M.W., Frank M.G., Crysdale N.Y., Stamper C.E., Hennessey P.A., Watkins L.R., Spencer R.L., Lowry C.A., Maier S.F. Greater glucocorticoid receptor activation in hippocampus of aged rats sensitizes microglia. Neurobiol Aging 2015, 36:1483-1495.
25. Bauernfeind F., Ablasser A., Bartok E., Kim S., Schmid-Burgk J., Cavlar T., Hornung V. Inflammasomes: current understanding and open questions. Cell Mol Life Sci 2011, 68:765-783.
26. Bedford P.D. Adverse cerebral effects of anaesthesia on old people. Lancet 1955, 269:259-263.
27. Bellinger F.P., Madamba S., Siggins G.R. Interleukin-1 Beta inhibits synaptic strength and long-term potentiation in the rat CA1 hippocampus. Brain Res 1993, 628:227-234.
28. Berg B.M., Godbout J.P., Chen J., Kelley K.W., Johnson R.W. Alpha-tocopherol and selenium facilitate recovery from lipopolysaccharide-induced sickness in aged mice. J Nutr 2005, 135:1157-1163.
29. Bergles D.E., Jahr C.E. Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J Neurosci 1998, 18:7709-7716.
30. Bilbo S.D., Biedenkapp J.C., Der-Avakian A., Watkins L.R., Rudy J.W., Maier S.F. Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition. J Neurosci 2005, 25:8000-8009.
31. Bilbo S.D., Barrientos R.M., Eads A.S., Northcutt A., Watkins L.R., Rudy J.W., Maier S.F. Early-life infection leads to altered BDNF and IL-1beta mRNA expression in rat hippocampus following learning in adulthood. Brain Behav Immun 2008, 22:451-455.
32. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
33. Bramham C.R., Worley P.F., Moore M.J., Guzowski J.F. The immediate early gene arc/arg3.1: regulation, mechanisms, and function. J Neurosci 2008, 28:11760-11767.
34. Brothers H.M., Bardou I., Hopp S.C., Kaercher R.M., Corona A.W., Fenn A.M., Godbout J.P., Wenk G.L. Riluzole partially rescues age-associated, but not LPS-induced, loss of glutamate transporters and spatial memory. J Neuroimmune Pharmacol 2013, 8:1098-1105.
35. Buchanan J.B., Sparkman N.L., Chen J., Johnson R.W. Cognitive and neuroinflammatory consequences of mild repeated stress are exacerbated in aged mice. Psychoneuroendocrinology 2008, 33:755-765.
36. Busillo J.M., Azzam K.M., Cidlowski J.A. Glucocorticoids sensitize the innate immune system through regulation of the NLRP3 inflammasome. J Biol Chem 2011, 286:38703-38713.
37. Cacabelos R., Alvarez X.A., Fernandez-Novoa L., Franco A., Mangues R., Pellicer A., Nishimura T. Brain interleukin-1 beta in Alzheimer's disease and vascular dementia. Methods Find Exp Clin Pharmacol 1994, 16:141-151.
38. Campbell S.J., Hughes P.M., Iredale J.P., Wilcockson D.C., Waters S., Docagne F., Perry V.H., Anthony D.C. CINC-1 is an acute-phase protein induced by focal brain injury causing leukocyte mobilization and liver injury. FASEB J 2003, 17:1168-1170.
39. Campbell S.J., Perry V.H., Pitossi F.J., Butchart A.G., Chertoff M., Waters S., Dempster R., Anthony D.C. Central nervous system injury triggers hepatic CC and CXC chemokine expression that is associated with leukocyte mobilization and recruitment to both the central nervous system and the liver. Am J Pathol 2005, 166:1487-1497.
40. Campbell S.J., Deacon R.M., Jiang Y., Ferrari C., Pitossi F.J., Anthony D.C. Overexpression of IL-1beta by adenoviral-mediated gene transfer in the rat brain causes a prolonged hepatic chemokine response, axonal injury and the suppression of spontaneous behaviour. Neurobiol Dis 2007, 27:151-163.
41. Campbell S.J., Jiang Y., Davis A.E., Farrands R., Holbrook J., Leppert D., Anthony D.C. Immunomodulatory effects of etanercept in a model of brain injury act through attenuation of the acute-phase response. J Neurochem 2007, 103:2245-2255.
42. Cao X.Z., Ma H., Wang J.K., Liu F., Wu B.Y., Tian A.Y., Wang L.L., Tan W.F. Postoperative cognitive deficits and neuroinflammation in the hippocampus triggered by surgical trauma are exacerbated in aged rats. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:1426-1432.
43. Cartford M.C., Gemma C., Bickford P.C. Eighteen-month-old Fischer 344 rats fed a spinach-enriched diet show improved delay classical eyeblink conditioning and reduced expression of tumor necrosis factor alpha (TNFalpha) and TNFbeta in the cerebellum. J Neurosci 2002, 22:5813-5816.
44. Chao P.K., Lu K.T., Jhu J.Y., Wo Y.Y., Huang T.C., Ro L.S., Yang Y.L. Indomethacin protects rats from neuronal damage induced by traumatic brain injury and suppresses hippocampal IL-1beta release through the inhibition of Nogo-A expression. J Neuroinflammation 2012, 9:121.
45. Chapman T.R., Barrientos R.M., Ahrendsen J.T., Maier S.F., Patterson S.L. Synaptic correlates of increased cognitive vulnerability with aging: peripheral immune challenge and aging interact to disrupt theta-burst late-phase long-term potentiation in hippocampal area CA1. J Neurosci 2010, 30:7598-7603.
46. Chapman T.R., Barrientos R.M., Ahrendsen J.T., Hoover J.M., Maier S.F., Patterson S.L. Aging and infection reduce expression of specific brain-derived neurotrophic factor mRNAs in hippocampus. Neurobiol Aging 2012, 33:832.e1-832.e14.
47. Chen J., Buchanan J.B., Sparkman N.L., Godbout J.P., Freund G.G., Johnson R.W. Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system. Brain Behav Immun 2008, 22:301-311.
48. Cibelli M., Fidalgo A.R., Terrando N., Ma D., Monaco C., Feldmann M., Takata M., Lever I.J., Nanchahal J., Fanselow M.S., Maze M. Role of interleukin-1beta in postoperative cognitive dysfunction. Ann Neurol 2010, 68:360-368.
49. Colton C.A. Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 2009, 4:399-418.
50. Coogan A., O'Connor J.J. Inhibition of NMDA receptor-mediated synaptic transmission in the rat dentate gyrus in vitro by IL-1 beta. NeuroReport 1997, 8:2107-2110.
51. Coogan A.N., O'Neill L.A., O'Connor J.J. The P38 mitogen-activated protein kinase inhibitor SB203580 antagonizes the inhibitory effects of interleukin-1beta on long-term potentiation in the rat dentate gyrus in vitro. Neuroscience 1999, 93:57-69.
52. Corona A.W., Huang Y., O'Connor J.C., Dantzer R., Kelley K.W., Popovich P.G., Godbout J.P. Fractalkine receptor (CX3CR1) deficiency sensitizes mice to the behavioral changes induced by lipopolysaccharide. J Neuroinflammation 2010, 7:93.
53. Cortese G.P., Barrientos R.M., Maier S.F., Patterson S.L. Aging and a peripheral immune challenge interact to reduce mature brain-derived neurotrophic factor and activation of TrkB, PLC{gamma}1, and ERK in hippocampal synaptoneurosomes. J Neurosci 2011, 31:4274-4279.
54. Cotman C.W., Berchtold N.C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 2002, 25:295-301.
55. Craft S., Foster T.C., Landfield P.W., Maier S.F., Resnick S.M., Yaffe K. Session III: mechanisms of age-related cognitive change and targets for intervention: inflammatory, oxidative, and metabolic processes. J Gerontol A Biol Sci Med Sci 2012, 67:754-759.
56. Cullinan E.B., Kwee L., Nunes P., Shuster D.J., Ju G., McIntyre K.W., Chizzonite R.A., Labow M.A. IL-1 receptor accessory protein is an essential component of the IL-1 receptor. J Immunol 1998, 161:5614-5620.
57. Cunningham A.J., Murray C.A., O'Neil L.A.J., Lynch M.A., O'Connor J.J. Interleukin-1 (IL-1) and tumor necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro. Neurosci Lett 1996, 203:17-20.
58. Cunningham C., Wilcockson D.C., Campion S., Lunnon K., Perry V.H. Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 2005, 25:9275-9284.
59. Curran B.P., Murray H.J., O'Connor J.J. A role for c-Jun N-terminal kinase in the inhibition of long-term potentiation by interleukin-1beta and long-term depression in the rat dentate gyrus in vitro. Neuroscience 2003, 118:347-357.
60. Danbolt N.C. Glutamate uptake. Prog Neurobiol 2001, 65:1-105.
61. de Pablos R.M., Villaran R.F., Arguelles S., Herrera A.J., Venero J.L., Ayala A., Cano J., Machado A. Stress increases vulnerability to inflammation in the rat prefrontal cortex. J Neurosci 2006, 26:5709-5719.
62. DeKosky S.T., Goss J.R., Miller P.D., Styren S.D., Kochanek P.M., Marion D. Upregulation of nerve growth factor following cortical trauma. Exp Neurol 1994, 130:173-177.
63. Dinarello C.A., Cannon J.G., Wolff S.M. New concepts on the pathogenesis of fever. Rev Infect Dis 1988, 10:168-189.
64. Dinkel K., MacPherson A., Sapolsky R.M. Novel glucocorticoid effects on acute inflammation in the CNS. J Neurochem 2003, 84:705-716.
65. Ericsson A., Kovacs K.J., Sawchenko P.E. A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons. J Neurosci 1994, 14:897-913.
66. Espinosa-Oliva A.M., de Pablos R.M., Villaran R.F., Arguelles S., Venero J.L., Machado A., Cano J. Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol Aging 2011, 32:85-102.
67. Frank M.G., Barrientos R.M., Biedenkapp J.C., Rudy J.W., Watkins L.R., Maier S.F. MRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol Aging 2006, 27:717-722.
68. Frank M.G., Barrientos R.M., Hein A.M., Biedenkapp J.C., Watkins L.R., Maier S.F. IL-1RA blocks E. coli-induced suppression of Arc and long-term memory in aged F344xBN F1 rats. Brain Behav Immun 2010, 24:254-262.
69. Frank M.G., Barrientos R.M., Watkins L.R., Maier S.F. Aging sensitizes rapidly isolated hippocampal microglia to LPS ex vivo. J Neuroimmunol 2010, 226:181-184.
70. 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.
71. Frank M.G., Barrientos R.M., Thompson B.M., Weber M.D., Watkins L.R., Maier S.F. IL-1RA injected intra-cisterna magna confers extended prophylaxis against lipopolysaccharide-induced neuroinflammatory and sickness responses. J Neuroimmunol 2012, 252:33-39.
72. 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.
73. Garcia-Mesa Y., Lopez-Ramos J.C., Gimenez-Llort L., Revilla S., Guerra R., Gruart A., Laferla F.M., Cristofol R., Delgado-Garcia J.M., Sanfeliu C. Physical exercise protects against Alzheimer's disease in 3xTg-AD mice. J Alzheimers Dis 2011, 24:421-454.
74. Garcia-Mesa Y., Pareja-Galeano H., Bonet-Costa V., Revilla S., Gomez-Cabrera M.C., Gambini J., Gimenez-Llort L., Cristofol R., Vina J., Sanfeliu C. Physical exercise neuroprotects ovariectomized 3xTg-AD mice through BDNF mechanisms. Psychoneuroendocrinology 2014, 45:154-166.
75. Gaykema R.P.A., Goehler L.E., Tilders F.J.H., Bol J.G.J.M., McGorry M., Fleshner M., Maier S.F., Watkins L.R. Bacterial endotoxin induces Fos immunoreactivity in primary afferent neurons of the vagus nerve. NeuroImmunoModulation 1998, 5:234-240.
76. Gemma C., Mesches M.H., Sepesi B., Choo K., Holmes D.B., Bickford P.C. Diets enriched in foods with high antioxidant activity reverse age-induced decreases in cerebellar beta-adrenergic function and increases in proinflammatory cytokines. J Neurosci 2002, 22:6114-6120.
77. Gibbons T.E., Pence B.D., Petr G., Ossyra J.M., Mach H.C., Bhattacharya T.K., Perez S., Martin S.A., McCusker R.H., Kelley K.W., Rhodes J.S., Johnson R.W., Woods J.A. Voluntary wheel running, but not a diet containing (-)-epigallocatechin-3-gallate and beta-alanine, improves learning, memory and hippocampal neurogenesis in aged mice. Behav Brain Res 2014, 272:131-140.
78. Gibertini M., Newton C., Friedman H., Klein T.W. Spatial learning impairment in mice infected with Legionella pneumophila or administered exogenous interleukin-1-beta. Brain Behav Immun 1995, 9:113-128.
79. Godbout J.P., Berg B.M., Kelley K.W., Johnson R.W. Alpha-tocopherol reduces lipopolysaccharide-induced peroxide radical formation and interleukin-6 secretion in primary murine microglia and in brain. J Neuroimmunol 2004, 149:101-109.
80. Godbout J.P., Chen J., Abraham J., Richwine A.F., Berg B.M., Kelley K.W., Johnson R.W. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J 2005, 19:1329-1331.
81. Godbout J.P., Moreau M., Lestage J., Chen J., Sparkman N.L., OC J., Castanon N., Kelley K.W., Dantzer R., Johnson R.W. Aging exacerbates depressive-like behavior in mice in response to activation of the peripheral innate immune system. Neuropsychopharmacology 2008, 33:2341-2351.
82. Goehler L.E., Relton J.K., Dripps D., Kiechle R., Tartaglia N., Maier S.F., Watkins L.R. Vagal paraganglia bind biotinylated interleukin-1 receptor antagonist: a possible mechanism for immune-to-brain communication. Brain Res Bull 1997, 43:357-364.
83. Granowitz E.V., Porat R., Mier J.W., Pribble J.P., Stiles D.M., Bloedow D.C., Catalano M.A., Wolff S.M., Dinarello C.A. Pharmacokinetics, safety and immunomodulatory effects of human recombinant interleukin-1 receptor antagonist in healthy humans. Cytokine 1992, 4:353-360.
84. Griffin R., Nally R., Nolan Y., McCartney Y., Linden J., Lynch M.A. The age-related attenuation in long-term potentiation is associated with microglial activation. J Neurochem 2006, 99:1263-1272.
85. Griffiths M.R., Gasque P., Neal J.W. The multiple roles of the innate immune system in the regulation of apoptosis and inflammation in the brain. J Neuropathol Exp Neurol 2009, 68:217-226.
86. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., Barnes C.A. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 2000, 20:3993-4001.
87. Hall J., Thomas K.L., Everitt B.J. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 2000, 3:533-535.
88. Hanamsagar R., Hanke M.L., Kielian T. Toll-like receptor (TLR) and inflammasome actions in the central nervous system. Trends Immunol 2012, 33:333-342.
89. Hauss-Wegrzyniak B., Dobrzanski P., Stoehr J.D., Wenk G.L. Chronic neuroinflammation in rats reproduces components of the neurobiology of Alzheimer's disease. Brain Res 1998, 780:294-303.
90. Hauss-Wegrzyniak B., Willard L.B., Del Soldato P., Pepeu G., Wenk G.L. Peripheral administration of novel anti-inflammatories can attenuate the effects of chronic inflammation within the CNS. Brain Res 1999, 815:36-43.
91. Hauss-Wegrzyniak B., Lynch M.A., Vraniak P.D., Wenk G.L. Chronic brain inflammation results in cell loss in the entorhinal cortex and impaired LTP in perforant path-granule cell synapses. Exp Neurol 2002, 176:336-341.
92. Hein A.M., Stasko M.R., Matousek S.B., Scott-McKean J.J., Maier S.F., Olschowka J.A., Costa A.C., O'Banion M.K. Sustained hippocampal IL-1beta overexpression impairs contextual and spatial memory in transgenic mice. Brain Behav Immun 2010, 24:243-253.
93. Henry C.J., Huang Y., Wynne A., Hanke M., Himler J., Bailey M.T., Sheridan J.F., Godbout J.P. Minocycline attenuates lipopolysaccharide (LPS)-induced neuroinflammation, sickness behavior, and anhedonia. J Neuroinflammation 2008, 5:15.
94. 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.
95. Hoek R.M., Ruuls S.R., Murphy C.A., Wright G.J., Goddard R., Zurawski S.M., Blom B., Homola M.E., Streit W.J., Brown M.H., Barclay A.N., Sedgwick J.D. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 2000, 290:1768-1771.
96. Holmes M.C., Carter R.N., Noble J., Chitnis S., Dutia A., Paterson J.M., Mullins J.J., Seckl J.R., Yau J.L. 11beta-hydroxysteroid dehydrogenase type 1 expression is increased in the aged mouse hippocampus and parietal cortex and causes memory impairments. J Neurosci 2010, 30:6916-6920.
97. Hovens I.B., Schoemaker R.G., van der Zee E.A., Heineman E., Nyakas C., van Leeuwen B.L. Surgery-induced behavioral changes in aged rats. Exp Gerontol 2013, 48:1204-1211.
98. Hovens I.B., Schoemaker R.G., van der Zee E.A., Absalom A.R., Heineman E., van Leeuwen B.L. Postoperative cognitive dysfunction: involvement of neuroinflammation and neuronal functioning. Brain Behav Immun 2014, 38:202-210.
99. Hovens I.B., van Leeuwen B.L., Nyakas C., Heineman E., van der Zee E.A., Schoemaker R.G. Postoperative cognitive dysfunction and microglial activation in associated brain regions in old rats. Neurobiol Learn Mem 2014, 118C:74-79.
100. Jacotte-Simancas A., Costa-Miserachs D., Coll-Andreu M., Torras-Garcia M., Borlongan C., Portell-Cortes I. Effects of voluntary physical exercise, citicoline, and combined treatment on object recognition memory, neurogenesis and neuroprotection after traumatic brain injury in rats. Journal of neurotrauma 2014.
101. Jiang Y., Deacon R., Anthony D.C., Campbell S.J. Inhibition of peripheral TNF can block the malaise associated with CNS inflammatory diseases. Neurobiol Dis 2008, 32:125-132.
102. Jin W.J., Feng S.W., Feng Z., Lu S.M., Qi T., Qian Y.N. Minocycline improves postoperative cognitive impairment in aged mice by inhibiting astrocytic activation. NeuroReport 2014, 25:1-6.
103. Johnson J.D., O'Connor K.A., Deak T., Stark M., Watkins L.R., Maier S.F. Prior stressor exposure sensitizes LPS-induced cytokine production. Brain Behav Immun 2002, 16:461-476.
104. Joseph J.A., Shukitt-Hale B., Denisova N.A., Bielinski D., Martin A., McEwen J.J., Bickford P.C. Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation. J Neurosci 1999, 19:8114-8121.
105. Jurgens H.A., Amancherla K., Johnson R.W. Influenza infection induces neuroinflammation, alters hippocampal neuron morphology, and impairs cognition in adult mice. J Neurosci 2012, 32:3958-3968.
106. Katagiri H., Tanaka K., Manabe T. Requirement of appropriate glutamate concentrations in the synaptic cleft for hippocampal LTP induction. Eur J Neurosci 2001, 14:547-553.
107. Katsuki H., Nakai S., Hirai Y., Akaji K., Kiso Y., Satoh M. Interleukin-1 B inhibits long-term potentiation in the CA3 region of mouse hippocampal slices. Eur J Pharmacol 1990, 181:323-326.
108. Katsuura G., Arimura A., Koves K., Gottschall P.E. Involvement of organum vasculosum of lamina terminalis and preoptic area in interleukin 1 beta-induced ACTH release. Am J Physiol 1990, 258:E163-E171.
109. Kelly A., Vereker E., Nolan Y., Brady M., Barry C., Loscher C.E., Mills K.H., Lynch M.A. Activation of p38 plays a pivotal role in the inhibitory effect of lipopolysaccharide and interleukin-1 beta on long term potentiation in rat dentate gyrus. J Biol Chem 2003, 278:19453-19462.
110. 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.
111. Kim S.E., Ko I.G., Kim B.K., Shin M.S., Cho S., Kim C.J., Kim S.H., Baek S.S., Lee E.K., Jee Y.S. Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp Gerontol 2010, 45:357-365.
112. Kinoshita K., Chatzipanteli K., Vitarbo E., Truettner J.s., Alonso O.F., Dietrich W.D. Interleukin-1beta messenger ribonucleic acid and protein levels after fluid-percussion brain injury in rats: importance of injury severity and brain temperature. Neurosurgery 2002, 51:195-203. discussion 203.
113. Knoblach S.M., Faden A.I. Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental traumatic brain injury. Exp Neurol 1998, 153:143-151.
114. Kohman R.A., DeYoung E.K., Bhattacharya T.K., Peterson L.N., Rhodes J.S. 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.
115. Kohman R.A., Bhattacharya T.K., Wojcik E., Rhodes J.S. Exercise reduces activation of microglia isolated from hippocampus and brain of aged mice. J Neuroinflammation 2013, 10:114.
116. Kong F., Chen S., Cheng Y., Ma L., Lu H., Zhang H., Hu W. Minocycline attenuates cognitive impairment induced by isoflurane anesthesia in aged rats. PLoS One 2013, 8:e61385.
117. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996, 19:312-318.
118. Kumar A., Stoica B.A., Sabirzhanov B., Burns M.P., Faden A.I., Loane D.J. Traumatic brain injury in aged animals increases lesion size and chronically alters microglial/macrophage classical and alternative activation states. Neurobiol Aging 2013, 34:1397-1411.
119. Lapchak P.A., Araujo D.M., Hefti F. Systemic interleukin-1 beta decreases brain-derived neurotrophic factor messenger RNA expression in the rat hippocampal formation. Neuroscience 1993, 53:297-301.
120. Lawson L.J., Perry V.H., Dri P., Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990, 39:151-170.
121. Laye S., Goujon E., Combe C., VanHoy R., Kelley K.W., Parnet P., Dantzer R. Effects of lipopolysaccharide and glucocorticoids on expression of interleukin-1 beta converting enzyme in the pituitary and brain of mice. J Neuroimmunol 1996, 68:61-66.
122. Li R.L., Zhang Z.Z., Peng M., Wu Y., Zhang J.J., Wang C.Y., Wang Y.L. Postoperative impairment of cognitive function in old mice: a possible role for neuroinflammation mediated by HMGB1, S100B, and RAGE. J Surg Res 2013, 185:815-824.
123. Li Z., Cao Y., Li L., Liang Y., Tian X., Mo N., Liu Y., Li M., Chui D., Guo X. Prophylactic angiotensin type 1 receptor antagonism confers neuroprotection in an aged rat model of postoperative cognitive dysfunction. Biochem Biophys Res Commun 2014, 449:74-80.
124. Lievens J.C., Bernal F., Forni C., Mahy N., Kerkerian-Le Goff L. Characterization of striatal lesions produced by glutamate uptake alteration: cell death, reactive gliosis, and changes in GLT1 and GADD45 mRNA expression. Glia 2000, 29:222-232.
125. Link W., Konietzko U., Kauselmann G., Krug M., Schwanke B., Frey U., Kuhl D. Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci U S A 1995, 92:5734-5738.
126. Lloyd E., Somera-Molina K., Van Eldik L.J., Watterson D.M., Wainwright M.S. Suppression of acute proinflammatory cytokine and chemokine upregulation by post-injury administration of a novel small molecule improves long-term neurologic outcome in a mouse model of traumatic brain injury. J Neuroinflammation 2008, 5:28.
127. Long J.M., Kalehua A.N., Muth N.J., Calhoun M.E., Jucker M., Hengemihle J.M., Ingram D.K., Mouton P.R. Stereological analysis of astrocyte and microglia in aging mouse hippocampus. Neurobiol Aging 1998, 19:497-503.
128. Lu K.T., Wu C.Y., Yen H.H., Peng J.H., Wang C.L., Yang Y.L. Bumetanide administration attenuated traumatic brain injury through IL-1 overexpression. Neurol Res 2007, 29:404-409.
129. Luterman J.D., Haroutunian V., Yemul S., Ho L., Purohit D., Aisen P.S., Mohs R., Pasinetti G.M. Cytokine gene expression as a function of the clinical progression of Alzheimer disease dementia. Arch Neurol 2000, 57:1153-1160.
130. Lyford G.L., Yamagata K., Kaufmann W.E., Barnes C.A., Sanders L.K., Copeland N.G., Gilbert D.J., Jenkins N.A., Lanahan A.A., Worley P.F. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 1995, 14:433-445.
131. Lynch M.A. Age-related impairment in long-term potentiation in hippocampus: a role for the cytokine, interleukin-1 beta?. Prog Neurobiol 1998, 56:571-589.
132. Lyons A., Downer E.J., Crotty S., Nolan Y.M., Mills K.H., Lynch M.A. CD200 ligand receptor interaction modulates microglial activation in vivo and in vitro: a role for IL-4. J Neurosci 2007, 27:8309-8313.
133. Ma Y.L., Wang H.L., Wu H.C., Wei C.L., Lee E.H. Brain-derived neurotrophic factor antisense oligonucleotide impairs memory retention and inhibits long-term potentiation in rats. Neuroscience 1998, 82:957-967.
134. MacPherson A., Dinkel K., Sapolsky R. Glucocorticoids worsen excitotoxin-induced expression of pro-inflammatory cytokines in hippocampal cultures. Exp Neurol 2005, 194:376-383.
135. Maier S.F. Bi-directional immune-brain communication: implications for understanding stress, pain, and cognition. Brain Behav Immun 2003, 17:69-85.
136. Maier S.F., Watkins L.R. Cytokines for psychologists: implications of bidirectional immune-to-brain communication for understanding behavior, mood, and cognition. Psychol Rev 1998, 105:83-107.
137. Maroney A.C., Glicksman M.A., Basma A.N., Walton K.M., Knight E., Murphy C.A., Bartlett B.A., Finn J.P., Angeles T., Matsuda Y., Neff N.T., Dionne C.A. Motoneuron apoptosis is blocked by CEP-1347 (KT 7515), a novel inhibitor of the JNK signaling pathway. J Neurosci 1998, 18:104-111.
138. Martin D.S., Spencer P., Horrobin D.F., Lynch M.A. Long-term potentiation in aged rats is restored when the age-related decrease in polyunsaturated fatty acid concentration is reversed. Prostaglandins Leukot Essent Fatty Acids 2002, 67:121-130.
139. Martinon F., Burns K., Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002, 10:417-426.
140. Matus-Amat P., Higgins E.A., Barrientos R.M., Rudy J.W. The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. J Neurosci 2004, 24:2431-2439.
141. McAllister T.W. Neuropsychiatric sequelae of head injuries. Psychiatr Clin North Am 1992, 15:395-413.
142. McGahon B.M., Martin D.S., Horrobin D.F., Lynch M.A. Age-related changes in LTP and antioxidant defenses are reversed by an alpha-lipoic acid-enriched diet. Neurobiol Aging 1999, 20:655-664.
143. McGahon B.M., Murray C.A., Horrobin D.F., Lynch Age-related changes in oxidative mechanisms and LTP are reversed by dietary manipulation. Neurobiol Aging 1999, 20:643-653.
144. Menard C., Quirion R. Successful cognitive aging in rats: a role for mGluR5 glutamate receptors, homer 1 proteins and downstream signaling pathways. PLoS One 2012, 7:e28666.
145. Merkley C.M., Jian C., Mosa A., Tan Y.F., Wojtowicz J.M. Homeostatic regulation of adult hippocampal neurogenesis in aging rats: long-term effects of early exercise. Front Neurosci 2014, 8:174.
146. Minogue A.M., Schmid A.W., Fogarty M.P., Moore A.C., Campbell V.A., Herron C.E., Lynch M.A. 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 2003, 278:27971-27980.
147. Mizuno M., Yamada K., Olariu A., Nawa H., Nabeshima T. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J Neurosci 2000, 20:7116-7121.
148. Moller J.T., Cluitmans P., Rasmussen L.S., Houx P., Rasmussen H., Canet J., Rabbitt P., Jolles J., Larsen K., Hanning C.D., Langeron O., Johnson T., Lauven P.M., Kristensen P.A., Biedler A., van Beem H., Fraidakis O., Silverstein J.H., Beneken J.E., Gravenstein J.S. Long-term postoperative cognitive dysfunction in the elderly ISPOCD1 study. ISPOCD investigators. International study of post-operative cognitive dysfunction. Lancet 1998, 351:857-861.
149. Monti J.M., Voss M.W., Pence A., McAuley E., Kramer A.F., Cohen N.J. History of mild traumatic brain injury is associated with deficits in relational memory, reduced hippocampal volume, and less neural activity later in life. Front Aging Neurosci 2013, 5:41.
150. Moore M.E., Piazza A., McCartney Y., Lynch M.A. Evidence that vitamin D3 reverses age-related inflammatory changes in the rat hippocampus. Biochem Soc Trans 2005, 33:573-577.
151. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
152. Moser E.I., Kropff E., Moser M.B. Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 2008, 31:69-89.
153. Munhoz C.D., Lepsch L.B., Kawamoto E.M., Malta M.B., Lima Lde S., Avellar M.C., Sapolsky R.M., Scavone C. Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-kappaB in the frontal cortex and hippocampus via glucocorticoid secretion. J Neurosci 2006, 26:3813-3820.
154. Munhoz C.D., Sorrells S.F., Caso J.R., Scavone C., Sapolsky R.M. Glucocorticoids exacerbate lipopolysaccharide-induced signaling in the frontal cortex and hippocampus in a dose-dependent manner. J Neurosci 2010, 30:13690-13698.
155. Murray C.A., Lynch M.A. Dietary supplementation with vitamin E reverses the age-related deficit in long term potentiation in dentate gyrus. J Biol Chem 1998, 273:12161-12168.
156. Murray C.A., Lynch M.A. 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 1998, 18:2974-2981.
157. Murray C.A., Clements M.P., Lynch M.A. Interleukin-1 induces lipid peroxidation and membrane changes in rat hippocampus: an age-related study. Gerontology 1999, 45:136-142.
158. Nakajima K., Tohyama Y., Kohsaka S., Kurihara T. Ceramide activates microglia to enhance the production/secretion of brain-derived neurotrophic factor (BDNF) without induction of deleterious factors in vitro. J Neurochem 2002, 80:697-705.
159. Nguyen K.T., Deak T., Owens S.M., Kohno T., Fleshner M., Watkins L.R., Maier S.F. Exposure to acute stress induces brain interleukin-1beta protein in the rat. J Neurosci 1998, 18:2239-2246.
160. Niemann C., Godde B., Voelcker-Rehage C. Not only cardiovascular, but also coordinative exercise increases hippocampal volume in older adults. Front Aging Neurosci 2014, 6:170.
161. Pang P.T., Lu B. Regulation of late-phase LTP and long-term memory in normal and aging hippocampus: role of secreted proteins tPA and BDNF. Ageing Res Rev 2004, 3:407-430.
162. Perkins A.J., Hendrie H.C., Callahan C.M., Gao S., Unverzagt F.W., Xu Y., Hall K.S., Hui S.L. Association of antioxidants with memory in a multiethnic elderly sample using the Third National Health and Nutrition Examination Survey. Am J Epidemiol 1999, 150:37-44.
163. Perrig W.J., Perrig P., Stahelin H.B. The relation between antioxidants and memory performance in the old and very old. J Am Geriatr Soc 1997, 45:718-724.
164. Perry V.H. A revised view of the central nervous system microenvironment and major histocompatibility complex class II antigen presentation. J Neuroimmunol 1998, 90:113-121.
165. Perry V.H., Matyszak M.K., Fearn S. Altered antigen expression of microglia in the aged rodent CNS. Glia 1993, 7:60-67.
166. Pita-Almenar J.D., Collado M.S., Colbert C.M., Eskin A. Different mechanisms exist for the plasticity of glutamate reuptake during early long-term potentiation (LTP) and late LTP. J Neurosci 2006, 26:10461-10471.
167. Pitossi F., del Rey A., Kabiersch A., Besedovsky H. Induction of cytokine transcripts in the central nervous system and pituitary following peripheral administration of endotoxin to mice. J Neurosci Res 1997, 48:287-298.
168. Pugh C.R., Kumagawa K., Fleshner M., Watkins L.R., Maier S.F., Rudy J.W. Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain Behav Immun 1998, 12:212-229.
169. Pugh C.R., Nguyen K.T., Gonyea J.L., Fleshner M., Wakins L.R., Maier S.F., Rudy J.W. Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation. Behav Brain Res 1999, 106:109-118.
170. Ramaiah R., Lam A.M. Postoperative cognitive dysfunction in the elderly. Anesthesiol Clin 2009, 27:485-496. table of contents.
171. Remarque E.J., Bollen E.L., Weverling-Rijnsburger A.W., Laterveer J.C., Blauw G.J., Westendorp R.G. Patients with Alzheimer's disease display a pro-inflammatory phenotype. Exp Gerontol 2001, 36:171-176.
172. Richwine A.F., Parkin A.O., Buchanan J.B., Chen J., Markham J.A., Juraska J.M., Johnson R.W. Architectural changes to CA1 pyramidal neurons in adult and aged mice after peripheral immune stimulation. Psychoneuroendocrinology 2008, 33:1369-1377.
173. Rogers J., Luber-Narod J., Styren S.D., Civin W.H. Expression of immune system-associated antigens by cells of the human central nervous system: relationship to the pathology of Alzheimer's disease. Neurobiol Aging 1988, 9:339-349.
174. Rosczyk H.A., Sparkman N.L., Johnson R.W. Neuroinflammation and cognitive function in aged mice following minor surgery. Exp Gerontol 2008, 43:840-846.
175. Rosi S., Ramirez-Amaya V., Vazdarjanova A., Worley P.F., Barnes C.A., Wenk G.L. Neuroinflammation alters the hippocampal pattern of behaviorally induced Arc expression. J Neurosci 2005, 25:723-731.
176. Rozovsky I., Finch C.E., Morgan T.E. Age-related activation of microglia and astrocytes: in vitro studies show persistent phenotypes of aging, increased proliferation, and resistance to down-regulation. Neurobiol Aging 1998, 19:97-103.
177. Rubio N. Demonstration of the presence of an interleukin-1 receptor on the surface of murine astrocytes and its regulation by cytokines and Theiler's virus. Immunology 1994, 82:178-183.
178. Rudy J.W., Barrientos R.M., O'Reilly R.C. Hippocampal formation supports conditioning to memory of a context. Behav Neurosci 2002, 116:530-538.
179. Sandhir R., Onyszchuk G., Berman N.E. Exacerbated glial response in the aged mouse hippocampus following controlled cortical impact injury. Exp Neurol 2008, 213:372-380.
180. Sapolsky R.M. Glucocorticoids, stress, and their adverse neurological effects: relevance to aging. Exp Gerontol 1999, 34:721-732.
181. Sapolsky R.M., Pulsinelli W.A. Glucocorticoids potentiate ischemic injury to neurons: therapeutic implications. Science 1985, 229:1397-1400.
182. Scheff S.W., Baldwin S.A., Brown R.W., Kraemer P.J. Morris water maze deficits in rats following traumatic brain injury: lateral controlled cortical impact. J Neurotrauma 1997, 14:615-627.
183. Seckl J.R. 11beta-Hydroxysteroid dehydrogenase in the brain: a novel regulator of glucocorticoid action?. Front Neuroendocrinol 1997, 18:49-99.
184. Seger R., Krebs E.G. The MAPK signaling cascade. FASEB J 1995, 9:726-735.
185. Selye H. Stress and disease. Science 1955, 122:625-631.
186. Senathi-Raja D., Ponsford J., Schonberger M. Impact of age on long-term cognitive function after traumatic brain injury. Neuropsychology 2010, 24:336-344.
187. Shah S.A., Prough D.S., Garcia J.M., DeWitt D.S., Hellmich H.L. Molecular correlates of age-specific responses to traumatic brain injury in mice. Exp Gerontol 2006, 41:1201-1205.
188. Sheffield L.G., Berman N.E. Microglial expression of MHC class II increases in normal aging of nonhuman primates. Neurobiol Aging 1998, 19:47-55.
189. Shukitt-Hale B., Cheng V., Joseph J.A. Effects of blackberries on motor and cognitive function in aged rats. Nutr Neurosci 2009, 12:135-140.
190. Siette J., Westbrook R.F., Cotman C., Sidhu K., Zhu W., Sachdev P., Valenzuela M.J. Age-specific effects of voluntary exercise on memory and the older brain. Biol Psychiatry 2013, 73:435-442.
191. Snigdha S., de Rivera C., Milgram N.W., Cotman C.W. Exercise enhances memory consolidation in the aging brain. Front Aging Neurosci 2014, 6:3.
192. Sparkman N.L., Johnson R.W. Neuroinflammation associated with aging sensitizes the brain to the effects of infection or stress. NeuroImmunoModulation 2008, 15:323-330.
193. Sparkman N.L., Martin L.A., Calvert W.S., Boehm G.W. Effects of intraperitoneal lipopolysaccharide on Morris maze performance in year-old and 2-month-old female C57BL/6J mice. Behav Brain Res 2005, 159:145-151.
194. Speisman R.B., Kumar A., Rani A., Foster T.C., Ormerod B.K. Daily exercise improves memory, stimulates hippocampal neurogenesis and modulates immune and neuroimmune cytokines in aging rats. Brain Behav Immun 2013, 28:25-43.
195. Steward O., Wallace C.S., Lyford G.L., Worley P.F. Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 1998, 21:741-751.
196. Sun L., Xie K., Zhang C., Song R., Zhang H. Hyperbaric oxygen preconditioning attenuates postoperative cognitive impairment in aged rats. NeuroReport 2014, 25:718-724.
197. Tafti M., Nishino S., Aldrich M.S., Liao W., Dement W.C., Mignot E. Major histocompatibility class II molecules in the CNS: increased microglial expression at the onset of narcolepsy in canine model. J Neurosci 1996, 16:4588-4595.
198. Tajiri N., Kellogg S.L., Shimizu T., Arendash G.W., Borlongan C.V. Traumatic brain injury precipitates cognitive impairment and extracellular Abeta aggregation in Alzheimer's disease transgenic mice. PLoS One 2013, 8:e78851.
199. Takahashi J.L., Giuliani F., Power C., Imai Y., Yong V.W. Interleukin-1beta promotes oligodendrocyte death through glutamate excitotoxicity. Ann Neurol 2003, 53:588-595.
200. Takao T., Tracey D.E., Mitchell W.M., De Souza E.B. Interleukin-1 receptors in mouse brain: characterization and neuronal localization. Endocrinology 1990, 127:3070-3078.
201. Tan H., Cao J., Zhang J., Zuo Z. Critical role of inflammatory cytokines in impairing biochemical processes for learning and memory after surgery in rats. J Neuroinflammation 2014, 11:93.
202. Terrando N., Gomez-Galan M., Yang T., Carlstrom M., Gustavsson D., Harding R.E., Lindskog M., Eriksson L.I. Aspirin-triggered resolvin D1 prevents surgery-induced cognitive decline. FASEB J 2013, 27:3564-3571.
203. Tilleux S., Hermans E. Neuroinflammation and regulation of glial glutamate uptake in neurological disorders. J Neurosci Res 2007, 85:2059-2070.
204. Tokutomi T., Miyagi T., Ogawa T., Ono J., Kawamata T., Sakamoto T., Shigemori M., Nakamura N. Age-associated increases in poor outcomes after traumatic brain injury: a report from the Japan Neurotrauma Data Bank. J Neurotrauma 2008, 25:1407-1414.
205. Tomura S., de Rivero Vaccari J.P., Keane R.W., Bramlett H.M., Dietrich W.D. Effects of therapeutic hypothermia on inflammasome signaling after traumatic brain injury. J Cereb Blood Flow Metab 2012, 32:1939-1947.
206. Turrin N.P., Gayle D., Ilyin S.E., Flynn M.C., Langhans W., Schwartz G.J., Plata-Salaman C.R. Pro-inflammatory and anti-inflammatory cytokine mRNA induction in the periphery and brain following intraperitoneal administration of bacterial lipopolysaccharide. Brain Res Bull 2001, 54:443-453.
207. Tzingounis A.V., Wadiche J.I. Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 2007, 8:935-947.
208. Van Dam A.M., Bauer J., Tilders F.J., Berkenbosch F. Endotoxin-induced appearance of immunoreactive interleukin-1 beta in ramified microglia in rat brain: a light and electron microscopic study. Neuroscience 1995, 65:815-826.
209. Varma V.R., Chuang Y., Harris G.C., Tan E.J., Carlson M.C. Low-intensity daily walking activity is associated with hippocampal volume in older adults. Hippocampus 2014.
210. Vereker E., Campbell V., Roche E., McEntee E., Lynch M.A. Lipopolysaccharide inhibits long term potentiation in the rat dentate gyrus by activating caspase-1. J Biol Chem 2000, 275:26252-26258.
211. Vereker E., O'Donnell E., Lynch M.A. The inhibitory effect of interleukin-1beta on long-term potentiation is coupled with increased activity of stress-activated protein kinases. J Neurosci 2000, 20:6811-6819.
212. Vukovic J., Colditz M.J., Blackmore D.G., Ruitenberg M.J., Bartlett P.F. Microglia modulate hippocampal neural precursor activity in response to exercise and aging. J Neurosci 2012, 32:6435-6443.
213. Webb M., Barclay A.N. Localisation of the MRC OX-2 glycoprotein on the surfaces of neurones. J Neurochem 1984, 43:1061-1067.
214. Wenk G.L., McGann-Gramling K., Hauss-Wegrzyniak B., Ronchetti D., Maucci R., Rosi S., Gasparini L., Ongini E. Attenuation of chronic neuroinflammation by a nitric oxide-releasing derivative of the antioxidant ferulic acid. J Neurochem 2004, 89:484-493.
215. Wimo A., Jonsson L., Bond J., Prince M., Winblad B. The worldwide economic impact of dementia 2010. Alzheimers Dement 2013, 9(1-11):e13.
216. Wine R.N., McPherson C.A., Harry G.J. IGF-1 and pAKT signaling promote hippocampal CA1 neuronal survival following injury to dentate granule cells. Neurotox Res 2009, 16:280-292.
217. Wynne A.M., Henry C.J., Huang Y., Cleland A., Godbout J.P. Protracted downregulation of CX3CR1 on microglia of aged mice after lipopolysaccharide challenge. Brain Behav Immun 2010, 24:1190-1201.
218. Wyrwoll C.S., Holmes M.C., Seckl J.R. 11beta-Hydroxysteroid dehydrogenases and the brain: from zero to hero, a decade of progress. Front Neuroendocrinol 2011, 32:265-286.
219. Yang J., Li M.X., Luo Y., Chen T., Liu J., Fang P., Jiang B., Hu Z.L., Jin Y., Chen J.G., Wang F. Chronic ceftriaxone treatment rescues hippocampal memory deficit in AQP4 knockout mice via activation of GLT-1. Neuropharmacology 2013, 75:213-222.
220. Yang T.T., Lin C., Hsu C.T., Wang T.F., Ke F.Y., Kuo Y.M. Differential distribution and activation of microglia in the brain of male C57BL/6J mice. Brain Struct Funct 2013, 218:1051-1060.
221. Yau J.L., Noble J., Seckl J.R. 11beta-Hydroxysteroid dehydrogenase type 1 deficiency prevents memory deficits with aging by switching from glucocorticoid receptor to mineralocorticoid receptor-mediated cognitive control. J Neurosci 2011, 31:4188-4193.
222. Yau J.L., Wheelen N., Noble J., Walker B.R., Webster S.P., Kenyon C.J., Ludwig M., Seckl J.R. Intrahippocampal glucocorticoids generated by 11beta-HSD1 affect memory in aged mice. Neurobiol Aging 2015, 36:334-343.
223. Ye S.M., Johnson R.W. Increased interleukin-6 expression by microglia from brain of aged mice. J Neuroimmunol 1999, 93:139-148.
224. Yu L., Sun L., Chen S. Protective effect of senegenin on splenectomy-induced postoperative cognitive dysfunction in elderly rats. Exp Ther Med 2014, 7:821-826.
225. Zhang J., Jiang W., Zuo Z. Pyrrolidine dithiocarbamate attenuates surgery-induced neuroinflammation and cognitive dysfunction possibly via inhibition of nuclear factor kappaB. Neuroscience 2014, 261:1-10.
226. Zou J.Y., Crews F.T. TNF alpha potentiates glutamate neurotoxicity by inhibiting glutamate uptake in organotypic brain slice cultures: neuroprotection by NF kappa B inhibition. Brain Res 2005, 1034:11-24.