IL-1RA blocks E. coli-induced suppression of Arc and long-term memory in aged F344 × BN F1 rats

Brain, Behavior, and Immunity

Volumn 24, Issue 2, 2010, Pages 254-262

  Frank, Matthew G ^a   Barrientos, Ruth M ^a   Hein, Amy M ^b   Biedenkapp, Joseph C ^c   Watkins, Linda R ^a   Maier, Steven F ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Aging; Arc; IL 1RA; Memory; Neuroinflammation; Pro inflammatory cytokines

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; CYTOKINE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 6; PROTEIN C FOS;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN INFECTION; CISTERNA MAGNA; CONTROLLED STUDY; ESCHERICHIA COLI; FEAR; FISCHER 344 RAT; GENE EXPRESSION; HIPPOCAMPUS; LONG TERM MEMORY; MALE; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RAT;

AGING; ANIMALS; CISTERNA MAGNA; CONDITIONING (PSYCHOLOGY); CYTOSKELETAL PROTEINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI INFECTIONS; FEAR; GENES, FOS; HIPPOCAMPUS; INJECTIONS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-6; MALE; MEMORY; MEMORY DISORDERS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; RATS; RATS, INBRED BN; RATS, INBRED F344; RECEPTORS, INTERLEUKIN-1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 72649093535     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.10.005     Document Type: Article

References (54)

1. Abraham J., Jang S., Godbout J.P., Chen J., Kelley K.W., Dantzer R., and Johnson R.W. Aging sensitizes mice to behavioral deficits induced by central HIV-1 gp120. Neurobiol. Aging 29 (2008) 614-621
2. Abraham J., and Johnson R.W. Central inhibition of interleukin-1beta ameliorates sickness behavior in aged mice. Brain Behav. Immun. 23 (2008) 396-401
3. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
4. Barrientos R.M., Frank M.G., Hein A.M., Higgins E.A., Watkins L.R., Rudy J.W., and Maier S.F. Time course of hippocampal IL-1 beta and memory consolidation impairments in aging rats following peripheral infection. Brain Behav. Immun. 23 (2009) 46-54
5. Barrientos R.M., Higgins E.A., Biedenkapp J.C., Sprunger D.B., Wright-Hardesty K.J., Watkins L.R., Rudy J.W., and Maier S.F. Peripheral infection and aging interact to impair hippocampal memory consolidation. Neurobiol. Aging 27 (2006) 723-732
6. Barrientos R.M., Higgins E.A., Sprunger D.B., Watkins L.R., Rudy J.W., and Maier S.F. 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
7. Barrientos R.M., Sprunger D.B., Campeau S., Higgins E.A., Watkins L.R., Rudy J.W., and Maier S.F. Brain-derived neurotrophic factor mRNA downregulation produced by social isolation is blocked by intrahippocampal interleukin-1 receptor antagonist. Neuroscience 121 (2003) 847-853
8. Barrientos R.M., Sprunger D.B., Campeau S., Watkins L.R., Rudy J.W., and Maier S.F. BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1beta administration. J. Neuroimmunol. 155 (2004) 119-126
9. Bekker A.Y., and Weeks E.J. Cognitive function after anaesthesia in the elderly. Best Pract. Res. Clin. Anaesthesiol. 17 (2003) 259-272
10. Bluthe R.M., Dantzer R., and Kelley K.W. Effects of interleukin-1 receptor antagonist on the behavioral effects of lipopolysaccharide in rat. Brain Res. 573 (1992) 318-320
11. Bramham C.R., Worley P.F., Moore M.J., and Guzowski J.F. The immediate early gene arc/arg3.1: regulation, mechanisms, and function. J. Neurosci. 28 (2008) 11760-11767
12. Cartmell T., Luheshi G.N., and Rothwell N.J. Brain sites of action of endogenous interleukin-1 in the febrile response to localized inflammation in the rat. J. Physiol. 518 Pt. 2 (1999) 585-594
13. Chen J., Buchanan J.B., Sparkman N.L., Godbout J.P., Freund G.G., and Johnson R.W. 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
14. Chomczynski P., and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162 (1987) 156-159
15. Cumiskey D., Curran B.P., Herron C.E., and O'Connor J.J. A role for inflammatory mediators in the IL-18 mediated attenuation of LTP in the rat dentate gyrus. Neuropharmacology 52 (2007) 1616-1623
16. Curran B.P., and O'Connor J.J. The inhibition of long-term potentiation in the rat dentate gyrus by pro-inflammatory cytokines is attenuated in the presence of nicotine. Neurosci. Lett. 344 (2003) 103-106
17. Davis S., Bozon B., and Laroche S. How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning?. Behav. Brain Res. 142 (2003) 17-30
18. Dilger R.N., and Johnson R.W. Aging, microglial cell priming, and the discordant central inflammatory response to signals from the peripheral immune system. J. Leukoc. Biol. 84 (2008) 932-939
19. Dinarello C.A. Interleukin-1. Cytokine Growth Factor Rev. 8 (1997) 253-265
20. Frank M.G., Barrientos R.M., Biedenkapp J.C., Rudy J.W., Watkins L.R., and Maier S.F. MRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol. Aging 27 (2006) 717-722
21. Gemma C., Fister M., Hudson C., and Bickford P.C. Improvement of memory for context by inhibition of caspase-1 in aged rats. Eur. J. Neurosci. 22 (2005) 1751-1756
22. Gibertini M., Newton C., Friedman H., and Klein T.W. Spatial learning impairment in mice infected with Legionella pneumophila or administered exogenous interleukin-1-beta. Brain Behav. Immun. 9 (1995) 113-128
23. Godbout J.P., Chen J., Abraham J., Richwine A.F., Berg B.M., Kelley K.W., and Johnson R.W. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 19 (2005) 1329-1331
24. Granowitz E.V., Porat R., Mier J.W., Orencole S.F., Callahan M.V., Cannon J.G., Lynch E.A., Ye K., Poutsiaka D.D., Vannier E., et al. Hematologic and immunomodulatory effects of an interleukin-1 receptor antagonist coinfusion during low-dose endotoxemia in healthy humans. Blood 82 (1993) 2985-2990
25. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., and 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. 20 (2000) 3993-4001
26. Guzowski J.F., Setlow B., Wagner E.K., and McGaugh J.L. Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci. 21 (2001) 5089-5098
27. Hauss-Wegrzyniak B., Dobrzanski P., Stoehr J.D., and Wenk G.L. Chronic neuroinflammation in rats reproduces components of the neurobiology of Alzheimer's disease. Brain Res. 780 (1998) 294-303
28. Hein A.M., Stutzman D.L., Bland S.T., Barrientos R.M., Watkins L.R., Rudy J.W., and Maier S.F. Prostaglandins are necessary and sufficient to induce contextual fear learning impairments after interleukin-1 beta injections into the dorsal hippocampus. Neuroscience 150 (2007) 754-763
29. Holmes C., El-Okl M., Williams A.L., Cunningham C., Wilcockson D., and Perry V.H. Systemic infection, interleukin 1beta, and cognitive decline in Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 74 (2003) 788-789
30. Huang Y., Henry C.J., Dantzer R., Johnson R.W., and Godbout J.P. Exaggerated sickness behavior and brain proinflammatory cytokine expression in aged mice in response to intracerebroventricular lipopolysaccharide. Neurobiol. Aging 29 (2008) 1744-1753
31. Huff N.C., Frank M., Wright-Hardesty K., Sprunger D., Matus-Amat P., Higgins E., and Rudy J.W. Amygdala regulation of immediate-early gene expression in the hippocampus induced by contextual fear conditioning. J. Neurosci. 26 (2006) 1616-1623
32. Johnson J.D., O'Connor K.A., Watkins L.R., and Maier S.F. The role of IL-1beta in stress-induced sensitization of proinflammatory cytokine and corticosterone responses. Neuroscience 127 (2004) 569-577
33. Kim J.J., and Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 256 (1992) 675-677
34. Link W., Konietzko U., Kauselmann G., Krug M., Schwanke B., Frey U., and Kuhl D. Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc. Natl. Acad. Sci. USA 92 (1995) 5734-5738
35. T) method. Methods 25 (2001) 402-408
36. Luheshi G., Miller A.J., Brouwer S., Dascombe M.J., Rothwell N.J., and Hopkins S.J. Interleukin-1 receptor antagonist inhibits endotoxin fever and systemic interleukin-6 induction in the rat. Am. J. Physiol. 270 (1996) E91-E95
37. Lupien S.J., Gaudreau S., Tchiteya B.M., Maheu F., Sharma S., Nair N.P., Hauger R.L., McEwen B.S., and Meaney M.J. Stress-induced declarative memory impairment in healthy elderly subjects: relationship to cortisol reactivity. J. Clin. Endocrinol. Metab. 82 (1997) 2070-2075
38. 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., and Worley P.F. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14 (1995) 433-445
39. Lynch M.A. Age-related impairment in long-term potentiation in hippocampus: a role for the cytokine, interleukin-1 beta?. Prog. Neurobiol. 56 (1998) 571-589
40. Miller A.J., Hopkins S.J., and Luheshi G.N. Sites of action of IL-1 in the development of fever and cytokine responses to tissue inflammation in the rat. Br. J. Pharmacol. 120 (1997) 1274-1279
41. Morrow B.A., Elsworth J.D., Inglis F.M., and Roth R.H. An antisense oligonucleotide reverses the footshock-induced expression of fos in the rat medial prefrontal cortex and the subsequent expression of conditioned fear-induced immobility. J. Neurosci. 19 (1999) 5666-5673
42. Oitzl M.S., van Oers H., Schobitz B., and de Kloet E.R. Interleukin-1 beta, but not interleukin-6, impairs spatial navigation learning. Brain Res. 613 (1993) 160-163
43. Plath N., Ohana O., Dammermann B., Errington M.L., Schmitz D., Gross C., Mao X., Engelsberg A., Mahlke C., Welzl H., Kobalz U., Stawrakakis A., Fernandez E., Waltereit R., Bick-Sander A., Therstappen E., Cooke S.F., Blanquet V., Wurst W., Salmen B., Bosl M.R., Lipp H.P., Grant S.G., Bliss T.V., Wolfer D.P., and Kuhl D. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52 (2006) 437-444
44. Proescholdt M.G., Hutto B., Brady L.S., and Herkenham M. Studies of cerebrospinal fluid flow and penetration into brain following lateral ventricle and cisterna magna injections of the tracer [14C]inulin in rat. Neuroscience 95 (2000) 577-592
45. Pugh C.R., Johnson J.D., Martin D., Rudy J.W., Maier S.F., and Watkins L.R. Human immunodeficiency virus-1 coat protein gp120 impairs contextual fear conditioning: a potential role in AIDS related learning and memory impairments. Brain Res. 861 (2000) 8-15
46. Pugh C.R., Kumagawa K., Fleshner M., Watkins L.R., Maier S.F., and Rudy J.W. Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain Behav. Immun. 12 (1998) 212-229
47. Shaw K.N., Commins S., and O'Mara S.M. Lipopolysaccharide causes deficits in spatial learning in the watermaze but not in BDNF expression in the rat dentate gyrus. Behav. Brain Res. 124 (2001) 47-54
48. Steward O., Wallace C.S., Lyford G.L., and Worley P.F. Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21 (1998) 741-751
49. Tanaka S., Ide M., Shibutani T., Ohtaki H., Numazawa S., Shioda S., and Yoshida T. Lipopolysaccharide-induced microglial activation induces learning and memory deficits without neuronal cell death in rats. J. Neurosci. Res. 83 (2006) 557-566
50. Tancredi V., D'Antuono M., Cafe C., Giovedi S., Bue M.C., D'Arcangelo G., Onofri F., and Benfenati F. The inhibitory effects of interleukin-6 on synaptic plasticity in the rat hippocampus are associated with an inhibition of mitogen-activated protein kinase ERK. J. Neurochem. 75 (2000) 634-643
51. Thomson L.M., and Sutherland R.J. Systemic administration of lipopolysaccharide and interleukin-1beta have different effects on memory consolidation. Brain Res. Bull. 67 (2005) 24-29
52. Tzingounis A.V., and Nicoll R.A. Arc/Arg3.1: linking gene expression to synaptic plasticity and memory. Neuron 52 (2006) 403-407
53. Van Wagoner N.J., and Benveniste E.N. Interleukin-6 expression and regulation in astrocytes. J. Neuroimmunol. 100 (1999) 124-139
54. Vereker E., O'Donnell E., and 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. 20 (2000) 6811-6819