BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1β administration

Journal of Neuroimmunology

Volumn 155, Issue 1-2, 2004, Pages 119-126

  Barrientos, Ruth M ^a   Sprunger, David B ^a   Campeau, Serge ^a   Watkins, Linda R ^a   Rudy, Jerry W ^a   Maier, Steven F ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

BDNF; In situ hybridization; Intrahippocampal; Memory consolidation; Proinflammatory cytokines; Time course

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; INTERLEUKIN 1BETA;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONDITIONING; CONTROLLED STUDY; DENTATE GYRUS; FEAR; HIPPOCAMPUS; LEARNING; MALE; MEMORY CONSOLIDATION; MOLECULAR MECHANICS; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TASK PERFORMANCE;

ANIMALS; AVOIDANCE LEARNING; BRAIN-DERIVED NEUROTROPHIC FACTOR; DENTATE GYRUS; DOWN-REGULATION; DRUG ADMINISTRATION ROUTES; FEAR; HIPPOCAMPUS; INTERLEUKIN-1; LEARNING; MALE; MEMORY DISORDERS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 4444338123     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2004.06.009     Document Type: Article

References (58)

1. M. Alonso, M.R. Vianna, A.M. Depino, T. Mello e Souza, P. Pereira, G. Szapiro, H. Viola, F. Pitossi, I. Izquierdo, and J.H. Medina BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation Hippocampus 12 2002 551 560
2. A. Balkowiec, and D.M. Katz Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons J. Neurosci. 22 2002 10399 10407
3. R.M. Barrientos, E.A. Higgins, D.B. Sprunger, L.R. Watkins, J.W. Rudy, and S.F. Maier Memory for context is impaired by a post context exposure injection of interleukin-1 beta into dorsal hippocampus Behav. Brain Res. 134 2002 291 298
4. R.M. Barrientos, D.B. Sprunger, S. Campeau, E.A. Higgins, L.R. Watkins, J.W. Rudy, and S.F. Maier Brain-derived neurotrophic factor mRNA downregulation produced by social isolation is blocked by intrahippocampal interleukin-1 receptor antagonist Neuroscience 121 2003 847 853
5. 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
6. T.V.P. Bliss, and T. Lomo Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path J. Physiol. (Lond.) 232 1973 331 356
7. L.A. Boven, J. Middel, P. Portegies, J. Verhoef, G.H. Jansen, and H.S. Nottet Overexpression of nerve growth factor and basic fibroblast growth factor in AIDS dementia complex J. Neuroimmunol. 97 1999 154 162
8. L.S. Brady, A.B. Lynn, M. Herkenham, and Z. Gottesfeld Systemic interleukin-1 induces early and late patterns of c-fos mRNA expression in brain J. Neurosci. 14 1994 4951 4964
9. R. Cacabelos, M. Barquero, P. Garcia, X.A. Alvarez, and E. Varela de Seijas Cerebrospinal fluid interleukin-1 beta (IL-1 beta) in Alzheimer's disease and neurological disorders Methods Find. Exp. Clin. Pharmacol. 13 1991 455 458
10. A.J. Cunningham, C.A. Murray, L.A.J. O'Neil, M.A. Lynch, and J.J. O'Connor Interleukin-1 (IL-1) and tumor necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro Neurosci. Lett. 203 1996 17 20
11. A. Ericsson, K.J. Kovacs, and P.E. Sawchenko A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons J. Neurosci. 14 1994 897 913
12. P. Gallo, A.M. Laverda, A. De Rossi, S. Pagni, A. Del Mistro, P. Cogo, M.G. Piccino, A. Plebani, B. Tavolato, and L. Chieco-Bianchi Immunological markers in the cerebrospinal fluid of HIV-1-infected children Acta Paediatr. Scand. 80 1991 659 666
13. A. Gartner, and V. Staiger Neurotrophin secretion from hippocampal neurons evoked by long-term-potentiation-inducing electrical stimulation patterns Proc. Natl. Acad. Sci. U. S. A. 99 2002 6386 6391
14. M. Gibertini, C. Newton, H. Friedman, and T.W. Klein Spatial learning impairment in mice infected with Legionella pneumophila or administered exogenous interleukin-1 beta Brain Behav. Immun. 9 1995 113 128
15. J. Hall, K.L. Thomas, and B.J. Everitt Rapid and selective induction of BDNF expression in the hippocampus during contextual learning Nat. Neurosci. 3 2000 533 535
16. G.E. Hardingham, F.J. Arnold, and H. Bading Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity Nat. Neurosci. 4 2001 261 267
17. C. Hock, K. Heese, C. Hulette, C. Rosenberg, and U. Otten Region-specific neurotrophin imbalances in Alzheimer disease: decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas Arch. Neurol. 57 2000 846 851
18. M. Korte, P. Carroll, E. Wolf, G. Brem, H. Thoenen, and T. Bonhoeffer Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor Proc. Natl. Acad. Sci. U. S. A. 92 1995 8856 8860
19. R.P. Kwok, J.R. Lundblad, J.C. Chrivia, J.P. Richards, H.P. Bachinger, R.G. Brennan, S.G. Roberts, M.R. Green, and R.H. Goodman Nuclear protein CBP is a coactivator for the transcription factor CREB Nature 370 1994 223 226
20. P.A. Lapchak, D.M. Araujo, and F. Hefti Systemic interleukin-1 beta decreases brain-derived neurotrophic factor messenger RNA expression in the rat hippocampal formation Neuroscience 53 1993 297 301
21. S. Laye, P. Parnet, E. Goujon, and R. Dantzer Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice Brain Res. Mol. Brain Res. 27 1994 157 162
22. J. Lee, W. Duan, and M.P. Mattson Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice J. Neurochem. 82 2002 1367 1375
23. E.S. Levine, and J.E. Kolb Brain-derived neurotrophic factor increases activity of NR2B-containing N-methyl-d-aspartate receptors in excised patches from hippocampal neurons J. Neurosci. Res. 62 2000 357 362
24. E.S. Levine, R.A. Crozier, I.B. Black, and M.R. Plummer Brain-derived neurotrophic factor modulates hippocampal synaptic transmission by increasing N-methyl-d-aspartic acid receptor activity Proc. Natl. Acad. Sci. U. S. A. 95 1998 10235 10239
25. A.C. Linthorst, C. Flachskamm, P. Muller-Preuss, F. Holsboer, and J.M. Reul Effect of bacterial endotoxin and interleukin-1 beta on hippocampal serotonergic neurotransmission, behavioral activity, and free corticosterone levels: an in vivo microdialysis study J. Neurosci. 15 1995 2920 2934
26. V.R. Lombardi, M. Garcia, L. Rey, and R. Cacabelos Characterization of cytokine production, screening of lymphocyte subset patterns and in vitro apoptosis in healthy and Alzheimer's Disease (AD) individuals J. Neuroimmunol. 97 1999 163 171
27. W.P. Luk, Y. Zhang, T.D. White, F.A. Lue, C. Wu, C.G. Jiang, L. Zhang, and H. Moldofsky Adenosine: a mediator of interleukin-1beta-induced hippocampal synaptic inhibition J. Neurosci. 19 1999 4238 4244
28. M.A. Lynch Age-related impairment in long-term potentiation in hippocampus: a role for the cytokine, interleukin-1 beta? Prog. Neurobiol. 56 1998 571 589
29. Y.L. Ma, H.L. Wang, H.C. Wu, C.L. Wei, and E.H. Lee Brain-derived neurotrophic factor antisense oligonucleotide impairs memory retention and inhibits long-term potentiation in rats Neuroscience 82 1998 957 967
30. S.F. Maier, L.R. Wakins, and D.M. Nance Multiple routes of action of interleukin-1 on the nervous system R. Ader D.L. Felton N. Cohen Psychoneuroimmunology vol. 1 2001 Academic Press 563 583
31. J.C. McArthur, N. Sacktor, and O. Selnes Human immunodeficiency virus-associated dementia Semin. Neurol. 19 1999 129 150
32. E. Messaoudi, S.W. Ying, T. Kanhema, S.D. Croll, and C.R. Bramham Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo J. Neurosci. 22 2002 7453 7461
33. M. Mizuno, K. Yamada, A. Olariu, H. Nawa, and T. Nabeshima Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats J. Neurosci. 20 2000 7116 7121
34. R.G.M. Morris, E. Anderson, G.S. Lynch, and M. Baudry Selective impairment of learning and blockade of long-term potentiation by an N-methyl-d-aspartate receptor antagonist, AP5 Nature 319 1986 774 776
35. K.D. Murray, C.M. Gall, E.G. Jones, and P.J. Isackson Differential regulation of brain-derived neurotrophic factor and type II calcium/calmodulin- dependent protein kinase messenger RNA expression in Alzheimer's disease Neuroscience 60 1994 37 48
36. K.T. Nguyen, T. Deak, S.M. Owens, T. Kohno, M. Fleshner, L.R. Watkins, and S.F. Maier Exposure to acute stress induces brain interleukin-1beta protein in the rat J. Neurosci. 18 1998 2239 2246
37. M.S. Oitzl, H. van Oers, B. Schobitz, and E.R. de Kloet Interleukin-1 beta, but not Interleukin-6, impairs spatial navigation learning Brain Res. 613 1993 160 163
38. G.C. Parry, and N. Mackman Role of cyclic AMP response element-binding protein in cyclic AMP inhibition of NF-kappaB-mediated transcription J. Immunol. 159 1997 5450 5456
39. V.H. Perry, T.A. Newman, and C. Cunningham The impact of systemic infection on the progression of neurodegenerative disease Nat. Rev. Neurosci. 4 2003 103 112
40. H.S. Phillips, J.M. Hains, M. Armanini, G.R. Laramee, S.A. Johnson, and J.W. Winslow BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease Neuron 7 1991 695 702
41. 2+ channel currents in hippocampal neurons through protein kinase C Eur. J. Pharmacol. 266 1994 1 10
42. 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 1999 109 118
43. C.R. Pugh, M. Fleshner, L.R. Watkins, S.F. Maier, and J.W. Rudy The immune system and memory consolidation: a role for the cytokine IL-1beta Neurosci. Biobehav. Rev. 25 2001 29 41
44. A. Reichenberg, R. Yirmiya, A. Schuld, T. Kraus, M. Haack, A. Morag, and T. Pollmacher Cytokine-associated emotional and cognitive disturbances in humans Arch. Gen. Psychiatry 58 2001 445 452
45. D.P. Salmon, A.P. Shimamura, N. Butters, and S. Smith Lexical and semantic priming deficits in patients with Alzheimer's disease J. Clin. Exp. Neuropsychol. 10 1988 477 494
46. J.G. Sheng, R.E. Mrak, and W.S.T. Griffin Microglial interleukin-1a expression in brain regions in Alzheimer's disease: correlation with neuritic plaque distribution Neuropathol. Appl. Neurobiol. 21 1995 290 301
47. P.B. Shieh, S.C. Hu, K. Bobb, T. Timmusk, and A. Ghosh Identification of a signaling pathway involved in calcium regulation of BDNF expression Neuron 20 1998 727 740
48. E. Shimizu, Y.P. Tang, C. Rampon, and J.Z. Tsien NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation Science 290 2000 1170 1174
49. Y. Stern, M.P. McDermott, S. Albert, D. Palumbo, O.A. Selnes, J. McArthur, N. Sacktor, G. Schifitto, K. Kieburtz, L. Epstein, and K.S. Marder Factors associated with incident human immunodeficiency virus-dementia Arch. Neurol. 58 2001 473 479
50. J.H. Sun, X.Q. Yan, H. Xiao, J.W. Zhou, Y.Z. Chen, and C.A. Wang Restoration of decreased N-methyl-d-aspartate receptor activity by brain-derived neurotrophic factor in the cultured hippocampal neurons: involvement of cAMP Arch. Biochem. Biophys. 394 2001 209 215
51. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism Neuron 20 1998 709 726
52. S. Tross, R.W. Price, B. Navia, H.T. Thaler, J. Gold, D.A. Hirsch, and J.J. Sidtis Neuropsychological characterization of the AIDS dementia complex: a preliminary report Aids 2 1988 81 88
53. W.J. Tyler, M. Alonso, C.R. Bramham, and L.D. Pozzo-Miller From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning Learn. Mem. 9 2002 224 237
54. T. van Groen, and J.M. Wyss Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections J. Comp. Neurol. 302 1990 515 528
55. E. Vereker, V. Campbell, E. Roche, E. McEntee, and M.A. Lynch Lipopolysaccharide inhibits long-term potentiation in the rat dentate gyrus by activating caspase-1 J. Biol. Chem. 275 2000 26252 26258
56. E. Vereker, E. O'Donnell, and M.A. Lynch The inhibitory effect of interleukin-1beta on long-term potentiation is coupled with increased activity of stress-activated protein kinases J. Neurosci. 20 2000 6811 6819
57. R. Yirmiya, G. Winocur, and I. Goshen Brain interleukin-1 is involved in spatial memory and passive avoidance conditioning Neurobiol. Learn. Mem. 78 2002 379 389
58. S.S. Zakharenko, S.L. Patterson, I. Dragatsis, S.O. Zeitlin, S.A. Siegelbaum, E.R. Kandel, and A. Morozov Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses Neuron 39 2003 975 990