Cognitive deficits in interleukin-10-deficient mice after peripheral injection of lipopolysaccharide

Brain, Behavior, and Immunity

Volumn 23, Issue 6, 2009, Pages 794-802

  Richwine, Amy F ^a   Sparkman, Nathan L ^a   Dilger, Ryan N ^a   Buchanan, Jessica B ^a   Johnson, Rodney W ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Behavior; Cytokines; Hippocampus; Interleukin 10; Mice; Working memory

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROTROPHIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CELL STRUCTURE; COGNITIVE DEFECT; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITE; GENOTYPE; HIPPOCAMPUS; IMMUNE RESPONSE; INFECTION; LEARNING; MALE; MAZE TEST; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PYRAMIDAL NERVE CELL; TASK PERFORMANCE; WILD TYPE; WORKING MEMORY;

ANIMALS; BEHAVIOR; COGNITION DISORDERS; CORTICOSTERONE; CYTOKINES; DENDRITES; INJECTIONS, INTRAPERITONEAL; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NERVE GROWTH FACTORS; PSYCHOMOTOR PERFORMANCE; PYRAMIDAL CELLS; RNA, MESSENGER;

EID: 67649846244     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.02.020     Document Type: Article

References (50)

1. Agnello D., Villa P., and Ghezzi P. Increased tumor necrosis factor and interleukin-6 production in the central nervous system of interleukin-10-deficient mice. Brain Res. 869 (2000) 241-243
2. Aubert A., Vega C., Dantzer R., and Goodall G. Pyrogens specifically disrupt the acquisition of a task involving cognitive processing in the rat. Brain Behav. Immun. 9 (1995) 129-148
3. 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
4. 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
5. Ben Menachem-Zidon O., Goshen I., Kreisel T., Ben Menahem Y., Reinhartz E., Ben Hur T., and Yirmiya R. Intrahippocampal transplantation of transgenic neural precursor cells overexpressing interleukin-1 receptor antagonist blocks chronic isolation-induced impairment in memory and neurogenesis. Neuropsychopharmacology 33 (2008) 2251-2262
6. Bluthe R.M., Castanon N., Pousset F., Bristow A., Ball C., Lestage J., Michaud B., Kelley K.W., and Dantzer R. Central injection of IL-10 antagonizes the behavioural effects of lipopolysaccharide in rats. Psychoneuroendocrinology 24 (1999) 301-311
7. Bonow, R.H., Aid, S., Zhang, Y., Becker, K.G., Bosetti, F., 2008. The brain expression of genes involved in inflammatory response, the ribosome, and learning and memory is altered by centrally injected lipopolysaccharide in mice. Pharmacogenomics J., doi:10.1038/tpj.2008.15.
8. 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
9. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., and Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9 (2008) 46-56
10. de Jong B.A., Schrijver H.M., Huizinga T.W., Bollen E.L., Polman C.H., Uitdehaag B.M., Kersbergen M.C., Sturk A., and Westendorp R.G. Innate production of interleukin-10 and tumor necrosis factor affects the risk of multiple sclerosis. Ann. Neurol. 48 (2000) 641-646
11. Gibertini M. IL1 beta impairs relational but not procedural rodent learning in a water maze task. Adv. Exp. Med. Biol. 402 (1996) 207-217
12. Glaser E.M., and Van der Loos H. Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J. Neurosci. Methods 4 (1981) 117-125
13. 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
14. Godbout J.P., Moreau M., Lestage J., Chen J., Sparkman N.L., O'Connor J., Castanon N., Kelley K.W., Dantzer R., and Johnson R.W. Aging exacerbates depressive-like behavior in mice in response to activation of the peripheral innate immune system. Neuropsychopharmacology 33 (2008) 2341-2351
15. Gould E., Woolley C.S., Frankfurt M., and McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10 (1990) 1286-1291
16. Greenough W.T., Volkmar F.R., and Juraska J.M. Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Exp. Neurol. 41 (1973) 371-378
17. Grilli M., Barbieri I., Basudev H., Brusa R., Casati C., Lozza G., and Ongini E. Interleukin-10 modulates neuronal threshold of vulnerability to ischaemic damage. Eur. J. Neurosci. 12 (2000) 2265-2272
18. 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
19. Howard M., O'Garra A., Ishida H., l Malefyt R., and de Vries J. Biological properties of interleukin 10. J. Clin. Immunol. 12 (1992) 239-247
20. Knoblach S.M., and Faden A.I. Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental traumatic brain injury. Exp. Neurol. 153 (1998) 143-151
21. Krzyszton C.P., Sparkman N.L., Grant R.W., Buchanan J.B., Broussard S.R., Woods J., and Johnson R.W. Exacerbated fatigue and motor deficits in interleukin-10-deficient mice after peripheral immune stimulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295 (2008) R1109-1114
22. Leon L.R., Kozak W., Rudolph K., and Kluger M.J. An antipyretic role for interleukin-10 in LPS fever in mice. Am. J. Physiol. 276 (1999) R81-89
23. Markham J.A., McKian K.P., Stroup T.S., and Juraska J.M. Sexually dimorphic aging of dendritic morphology in CA1 of hippocampus. Hippocampus 15 (2005) 97-103
24. McAllister A.K., Katz L.C., and Lo D.C. Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17 (1996) 1057-1064
25. McAllister A.K., Lo D.C., and Katz L.C. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15 (1995) 791-803
26. McGeer P.L., and McGeer E.G. Anti-inflammatory drugs in the fight against Alzheimer's disease. Ann. NY Acad. Sci. 777 (1996) 213-220
27. Milatovic D., Zaja-Milatovic S., Montine K.S., Horner P.J., and Montine T.J. Pharmacologic suppression of neuronal oxidative damage and dendritic degeneration following direct activation of glial innate immunity in mouse cerebrum. J. Neurochem. 87 (2003) 1518-1526
28. Moore K.W., l Malefyt R., Coffman R.L., and O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19 (2001) 683-765
29. Moore M.E., Piazza A., McCartney Y., and Lynch M.A. Evidence that vitamin D3 reverses age-related inflammatory changes in the rat hippocampus. Biochem. Soc. Trans. 33 (2005) 573-577
30. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11 (1984) 47-60
31. Moser M.B., Trommald M., and Andersen P. An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc. Natl. Acad. Sci. USA 91 (1994) 12673-12675
32. O'Connor, J.C., Lawson, M.A., Andre, C., Moreau, M., Lestage, J., Castanon, N., Kelley, K.W., Dantzer, R., 2008. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol. Psychiatry., doi:10.1038/sj.mp.4002148.
33. 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
34. Pugh R.C., Fleshner M., Watkins L.R., Maier S.F., and Rudy J.W. The immune system and memory consolidation: a role for the cytokine IL-1beta. Neurosci. Biobehav. Rev. 25 (2001) 29-41
35. Richwine A.F., Godbout J.P., Berg B.M., Chen J., Escobar J., Millard D.K., and Johnson R.W. Improved psychomotor performance in aged mice fed diet high in antioxidants is associated with reduced ex vivo brain interleukin-6 production. Brain Behav. Immun. 19 (2005) 512-520
36. Richwine A.F., Parkin A.O., Buchanan J.B., Chen J., Markham J.A., Juraska J.M., and Johnson R.W. Architectural changes to CA1 pyramidal neurons in adult and aged mice after peripheral immune stimulation. Psychoneuroendocrinology 33 (2008) 1369-1377
37. Rosi S., Ramirez-Amaya V., Vazdarjanova A., Worley P.F., Barnes C.A., and Wenk G.L. Neuroinflammation alters the hippocampal pattern of behaviorally induced Arc expression. J. Neurosci. 25 (2005) 723-731
38. Schippers E.F., van 't Veer C., van Voorden S., Martina C.A., Huizinga T.W., le Cessie S., and van Dissel J.T. IL-10 and toll-like receptor-4 polymorphisms and the in vivo and ex vivo response to endotoxin. Cytokine 29 (2005) 215-228
39. Sibley W.A., Bamford C.R., and Clark K. Clinical viral infections and multiple sclerosis. Lancet 1 (1985) 1313-1315
40. Silva-Gomez A.B., Rojas D., Juarez I., and Flores G. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res. 983 (2003) 128-136
41. Sparkman N.L., Buchanan J.B., Heyen J.R., Chen J., Beverly J.L., and Johnson R.W. Interleukin-6 facilitates lipopolysaccharide-induced disruption in working memory and expression of other proinflammatory cytokines in hippocampal neuronal cell layers. J. Neurosci. 26 (2006) 10709-10716
42. Sparkman N.L., and Johnson R.W. Neuroinflammation associated with aging sensitizes the brain to the effects of infection or stress. Neuroimmunomodulation 15 (2008) 323-330
43. Sparkman N.L., Kohman R.A., Garcia A.K., and Boehm G.W. Peripheral lipopolysaccharide administration impairs two-way active avoidance conditioning in C57BL/6J mice. Physiol. Behav. 85 (2005) 278-288
44. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99 (1992) 195-231
45. Strle K., Zhou J.H., Shen W.H., Broussard S.R., Johnson R.W., Freund G.G., Dantzer R., and Kelley K.W. Interleukin-10 in the brain. Crit. Rev. Immunol. 21 (2001) 427-449
46. Tapia-Arancibia L., Aliaga E., Silhol M., and Arancibia S. New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Res. Rev. 59 (2008) 201-220
47. Thackray A.M., McKenzie A.N., Klein M.A., Lauder A., and Bujdoso R. Accelerated prion disease in the absence of interleukin-10. J. Virol. 78 (2004) 13697-13707
48. Whishaw I.Q., and Tomie J.A. Perseveration on place reversals in spatial swimming pool tasks: further evidence for place learning in hippocampal rats. Hippocampus 7 (1997) 361-370
49. Woolley C.S., Gould E., and McEwen B.S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531 (1990) 225-231
50. Ye S.M., and Johnson R.W. An age-related decline in interleukin-10 may contribute to the increased expression of interleukin-6 in brain of aged mice. Neuroimmunomodulation 9 (2001) 183-192