Modulation of amyloid-β-induced and age-associated changes in rat hippocampus by eicosapentaenoic acid

Journal of Neurochemistry

Volumn 103, Issue 3, 2007, Pages 914-926

  Minogue, Aedín M ^a   Lynch, Aileen M ^b   Loane, David J ^b   Herron, Caroline E ^a   Lynch, Marina A ^b  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Age; Amyloid ; Eicosapentaenoic acid; Interleukin 1beta; Long term potentiation; Microglia

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; AMYLOID BETA PROTEIN; CD40 ANTIGEN; ICOSAPENTAENOIC ACID; INTERLEUKIN 1BETA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STRESS ACTIVATED PROTEIN KINASE;

AGED; AGING; ANALYTIC METHOD; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AGE FACTORS; AGING; AMYLOID BETA-PROTEIN; ANIMALS; ANIMALS, NEWBORN; ANTI-INFLAMMATORY AGENTS; ANTIGENS, CD40; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EICOSAPENTAENOIC ACID; ENCEPHALITIS; HIPPOCAMPUS; INJECTIONS, INTRAVENTRICULAR; INTERLEUKIN-1BETA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LONG-TERM POTENTIATION; MALE; NEUROPROTECTIVE AGENTS; PHOSPHORYLATION; RATS; RATS, WISTAR; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; UP-REGULATION;

RATTUS;

EID: 35248821724     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04848.x     Document Type: Article

References (77)

1. Abraham J., Jang S., Godbout J. P., Chen J., Kelley K. W., Dantzer R. Johnson R. W. (2006) Aging sensitizes mice to behavioral deficits induced by central HIV-1 gp120. Neurobiol. Aging [Epub ahead of print].
2. Aloisi F., De Simone R., Columba-Cabezas S. Levi G. (1999) Opposite effects of interferon-gamma and prostaglandin E2 on tumor necrosis factor and interleukin-10 production in microglia: a regulatory loop controlling microglia pro- and anti-inflammatory activities. J. Neurosci. Res. 56, 571 580.
3. Avital A., Goshen I., Kamsler A., Segal M., Iverfeldt K., Richter-Levin G. Yirmiya R. (2003) Impaired interleukin-1 signaling is associated with deficits in hippocampal memory processes and neural plasticity. Hippocampus 13, 826 834.
4. Babcock T., Helton W. S. Espat N. J. (2000) Eicosapentaenoic acid (EPA): an antiinflammatory omega-3 fat with potential clinical applications. Nutrition 16, 1116 1118.
5. Balschun D., Wetzel W., Del Rey A., Pitossi F., Schneider H., Zuschratter W. Besedovsky H. O. (2004) Interleukin-6: a cytokine to forget. FASEB J. 18, 1788 1790.
6. 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. (2006) Peripheral infection and aging interact to impair hippocampal memory consolidation. Neurobiol. Aging 27, 723 732.
7. Barry C. E., Nolan Y., Clarke R. M., Lynch A. Lynch M. A. (2005) Activation of c-Jun-N-terminal kinase is critical in mediating lipopolysaccharide-induced changes in the rat hippocampus. J. Neurochem. 93, 221 231.
8. Berger J. Moller D. E. (2002) The mechanisms of action of PPARs. Annu. Rev. Med. 53, 409 435.
9. Bernardo A. Minghetti L. (2006) PPAR-gamma agonists as regulators of microglial activation and brain inflammation. Curr. Pharm. Des. 12, 93 109.
10. Bernardo A., Levi G. Minghetti L. (2000) Role of the peroxisome proliferator-activated receptor-gamma (PPAR-gamma) and its natural ligand 15-deoxy-Delta12, 14- prostaglandin J2 in the regulation of microglial functions. Eur. J. Neurosci. 12, 2215 2223.
11. Block M. L. Hong J.-S. (2005) Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 76, 77 98.
12. Blum-Degen D., Muller T., Kuhn W., Gerlach M., Przuntek H. Riederer P. (1995) Interleukin-1 beta and interleukin-6 are elevated in the cerebrospinal fluid of Alzheimer's and de novo Parkinson's disease patients. Neurosci. Lett. 202, 17 20.
13. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analyt. Biochem. 72, 248 254.
14. Calder P. C. (2001) Polyunsaturated fatty acids, inflammation, and immunity. Lipids 36, 1007 1024.
15. Calon F., Lim G. P., Yang F. et al. (2004) Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 43, 633 645.
16. Chen Q. S., Kagan B. L., Hirakura Y. Xie C. W. (2000) Impairment of hippocampal long-term potentiation by Alzheimer amyloid beta-peptides. J. Neurosci. Res. 60, 65 72.
17. Clarke R. M., O'Connell F., Lyons A. Lynch M. A. (2006) The HMG-CoA reductase inhibitor, atorvastatin, attenuates the effects of acute administration of amyloid-β in rat hippocampus. Neuropharmacology 52, 136 145.
18. Cole G. M., Lim G. P., Yang F., Teter B., Begum A., Ma Q., Harris-White M. E. Frautschy S. A. (2005) Prevention of Alzheimer's disease: omega-3 fatty acid and phenolic anti-oxidant interventions. Neurobiol. Aging 26, 133 136.
19. Craft J. M., Watterson D. M., Hirsch E. Van Eldik L. J. (2005) Interleukin 1 receptor antagonist knockout mice show enhanced microglial activation and neuronal damage induced by intracerebroventricular infusion of human beta-amyloid. J. Neuroinflammation 2, 15.
20. Curran B. O'Connor J. J. (2001) The pro-inflammatory cytokine interleukin-18 impairs long-term potentiation and NMDA receptor-mediated transmission in the rat hippocampus in vitro. Neuroscience 108, 83 90.
21. Curran B. P., Murray H. J. O'Connor J. J. (2003) A role for c-jun n-terminal kinase in the inhibition of long-term potentiation by interleukin-1[beta] and long-term depression in the rat dentate gyrus in vitro. Neuroscience 118, 347 357.
22. Curtis C. L., Hughes C. E., Flannery C. R., Little C. B., Harwood J. L. Caterson B. (2000) n-3 fatty acids specifically modulate catabolic factors involved in articular cartilage degradation. J. Biol. Chem. 275, 721 724.
23. D'Arcangelo G., Grassi F., Ragozzino D., Santoni A., Tancredi V. Eusebi F. (1991) Interferon inhibits synaptic potentiation in rat hippocampus. Brain Res. 564, 245 248.
24. Davies C. A., Loddick S. A., Toulmond S., Stroemer R. P., Hunt J. Rothwell N. J. (1999) The progression and topographic distribution of interleukin-1beta expression after permanent middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 19, 87 98.
25. Fantuzzi G., Puren A. J., Harding M. W., Livingston D. J. Dinarello C. A. (1998) Interleukin-18 regulation of interferon gamma production and cell proliferation as shown in interleukin-1beta-converting enzyme (caspase-1)-deficient mice. Blood 91, 2118 2125.
26. Fantuzzi G., Reed D. A. Dinarello C. A. (1999) IL-12-induced IFN-gamma is dependent on caspase-1 processing of the IL-18 precursor. J. Clin. Invest. 104, 761 767.
27. Freir D. B., Holscher C. Herron C. E. (2001) Blockade of long-term potentiation by beta-amyloid peptides in the CA1 region of the rat hippocampus in vivo. J. Neurophysiol. 85, 708 713.
28. Godbout J. P. Johnson R. W. (2004) Interleukin-6 in the aging brain. Journal of Neuroimmunology: Neuroimmune Circuits and Infectious Disease: Proceedings of the 9th Conference of the Society for NeuroImmune Pharmacology 147, 141 144.
29. Godbout J. P., Chen J., Abraham J., Richwine A. F., Berg B. M., Kelley K. W. Johnson R. W. (2005) Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 19, 1329 1331.
30. Griffin W. S., Stanley L. C., Ling C., White L., MacLeod V., Perrot L. J., White III. C. L. Araoz C. (1989) Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc. Natl Acad. Sci. USA 86, 7611 7615.
31. Griffin R., Nally R., Nolan Y., McCartney Y., Linden J. Lynch M. A. (2006) The age-related attenuation in LTP is associated with microglial activation. J. Neurochem. 99, 1263 1272.
32. Hauss-Wegrzyniak B., Vraniak P. Wenk G. L. (1999) The effects of a novel NSAID on chronic neuroinflammation are age dependent. Neurobiol. Aging 20, 305 313.
33. Hayashi N., Tashiro T., Yamamori H. et al. (1999) Effect of intravenous omega-6 and omega-3 fat emulsions on nitrogen retention and protein kinetics in burned rats. Nutrition 15, 135 139.
34. Kavanagh T., Lonergan P. E. Lynch M. A. (2004) Eicosapentaenoic acid and gamma-linolenic acid increase hippocampal concentrations of IL-4 and IL-10 and abrogate lipopolysaccharide-induced inhibition of long-term potentiation. Prostaglandins Leukot. Essent. Fatty Acids 70, 391 397.
35. Kelly A., Lynch A., Vereker E., Nolan Y., Queenan P., Whittaker E., O'Neill L. A. Lynch M. A. (2001) 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, 45564 45572.
36. Kim K.-Y., Ju W.-K. Neufeld A. H. (2004) Neuronal susceptibility to damage: comparison of the retinas of young, old and old/caloric restricted rats before and after transient ischemia. Neurobiol. Aging 25, 491 500.
37. Kullberg S., Aldskogius H. Ulfhake B. (2001) Microglial activation, emergence of ED1-expressing cells and clusterin upregulation in the aging rat CNS, with special reference to the spinal cord. Brain Res. 899, 169 186.
38. Li A.-J., Katafuchi T., Oda S., Hori T. Oomura Y. (1997) Interleukin-6 inhibits long-term potentiation in rat hippocampal slices. Brain Res. 748, 30 38.
39. Li Y., Liu L., Barger S. W. Griffin W. S. (2003) Interleukin-1 mediates pathological effects of microglia on tau phosphorylation and on synaptophysin synthesis in cortical neurons through a p38-MAPK pathway. J. Neurosci. 23, 1605 1611.
40. Lonergan P. E., Martin D. S. D., Horrobin D. F. Lynch M. A. (2002) Neuroprotective effect of eicosapentaenoic acid in hippocampus of rats exposed to gamma-irradiation. J. Biol. Chem. 277, 20804 20811.
41. Lonergan P. E., Martin D. S. D., Horrobin D. F. Lynch M. A. (2004) Neuroprotective actions of eicosapentaenoic acid on lipopolysaccharide-induced dysfunction in rat hippocampus. J. Neurochem. 91, 20 29.
42. Lue L. F., Walker D. G., Brachova L., Beach T. G., Rogers J., Schmidt A. M., Stern D. M. Yan S. D. (2001) Involvement of microglial receptor for advanced glycation endproducts (RAGE) in Alzheimer's disease: identification of a cellular activation mechanism. Exp. Neurol. 171, 29 45.
43. Lynch M. A. (2004) Long-term potentiation and memory. Physiol. Rev. 84, 87 136.
44. Lynch A. M. Lynch M. A. (2002) The age-related increase in IL-1 type I receptor in rat hippocampus is coupled with an increase in caspase-3 activation. Eur. J. Neurosci. 15, 1779 1788.
45. Lynch M. A., Errington M. L. Bliss T. V. (1985) Long-term potentiation of synaptic transmission in the dentate gyrus: increased release of [14C]glutamate without increase in receptor binding. Neurosci. Lett. 62, 123 129.
46. Lynch A. M., Moore M., Craig S., Lonergan P. E., Martin D. S. Lynch M. A. (2003) Analysis of interleukin-1 beta-induced cell signaling activation in rat hippocampus following exposure to gamma irradiation. Protective effect of eicosapentaenoic acid. J. Biol. Chem. 278, 51075 51084.
47. Lynch A. M., Loane D. J., Minogue A. M., Clarke R. M., Kilroy D. M., Nally R. E., Roche O. J., O'Connell F. Lynch M. A. (2007) Eicosapentaenoic acid confers neuroprotection in the amyloid-beta challenged aged hippocampus. Neurobiol. Aging 28, 845 855.
48. Maher F. O., Nolan Y. Lynch M. A. (2005) Downregulation of IL-4-induced signalling in hippocampus contributes to deficits in LTP in the aged rat. Neurobiol. Aging 26, 717 728.
49. Maher F. O., Clarke R. M., Kelly A., Nally R. E. Lynch M. A. (2006) 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, 1560 1571.
50. Martin D. S., Lonergan P. E., Boland B., Fogarty M. P., Brady M., Horrobin D. F., Campbell V. A. Lynch M. A. (2002) Apoptotic changes in the aged brain are triggered by interleukin-1beta-induced activation of p38 and reversed by treatment with eicosapentaenoic acid. J. Biol. Chem. 277, 34239 34246.
51. McCarty M. F. (1999) Vascular nitric oxide, sex hormone replacement, and fish oil may help to prevent Alzheimer's disease by suppressing synthesis of acute-phase cytokines. Med. Hypotheses 53, 369 374.
52. McGahon B. M., Martin D. S., Horrobin D. F. Lynch M. A. (1999) Age-related changes in synaptic function: analysis of the effect of dietary supplementation with omega-3 fatty acids. Neuroscience 94, 305 314.
53. Mehlhorn G., Hollborn M. Schliebs R. (2000) Induction of cytokines in glial cells surrounding cortical beta-amyloid plaques in transgenic Tg2576 mice with Alzheimer pathology. Int. J. Dev. Neurosci. 18, 423 431.
54. Miller A.-M., Piazza A., Walsh M., Martin D. S. D., Mandel A., Bolton A. Lynch M. A. (2007) A novel phospholipid based drug formulation inhibits amyloid-β induced granzyme B, caspase 3 and sphingomyelinase activation in the rat cortex. British Neurosci. Assoc. Abstr. 43, 12.
55. Minogue A. M., Schmid A. W., Fogarty M. P., Moore A. C., Campbell V. A., Herron C. E. Lynch M. A. (2003) 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, 27971 27980.
56. Moore M. E., Piazza A., McCartney Y. Lynch M. A. (2005) Evidence that vitamin D3 reverses age-related inflammatory changes in the rat hippocampus. Biochem. Soc. Trans. 33, 573 577.
57. Mrak R. E. Griffin W. S. (2000) Interleukin-1 and the immunogenetics of Alzheimer disease. J. Neuropathol. Exp. Neurol. 59, 471 476.
58. Murasko D. M. Jiang J. (2005) Response of aged mice to primary virus infections. Immunol. Rev. 205, 285 296.
59. Murray C. A. Lynch M. A. (1998) 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, 2974 2981.
60. Nolan Y., Maher F. O., Martin D. S., Clarke R. M., Brady M. T., Bolton A. E., Mills K. H. Lynch M. A. (2005) Role of interleukin-4 in regulation of age-related inflammatory changes in the hippocampus. J. Biol. Chem. 280, 9354 9362.
61. O'Donnell E., Vereker E. Lynch M. A. (2000) Age-related impairment in LTP is accompanied by enhanced activity of stress-activated protein kinases: analysis of underlying mechanisms. Eur. J. Neurosci. 12, 345 352.
62. Petrova T. V., Akama K. T. Van Eldik L. J. (1999) Cyclopentenone prostaglandins suppress activation of microglia: down-regulation of inducible nitric-oxide synthase by 15-deoxy-Delta12,14-prostaglandin J2. Proc. Natl Acad. Sci. USA 96, 4668 4673.
63. Sadeghi S., Wallace F. A. Calder P. C. (1999) Dietary lipids modify the cytokine response to bacterial lipopolysaccharide in mice. Immunology 96, 404 410.
64. Saleshando G. O'Connor J. J. (2000) SB203580, the p38 mitogen-activated protein kinase inhibitor blocks the inhibitory effect of beta-amyloid on long-term potentiation in the rat hippocampus. Neurosci. Lett. 288, 119 122.
65. Schneider H., Pitossi F., Balschun D., Wagner A., del Rey A. Besedovsky H. O. (1998) A neuromodulatory role of interleukin-1beta in the hippocampus. Proc. Natl Acad. Sci. USA 95, 7778 7783.
66. Sheng J. G., Mrak R. E., Bales K. R., Cordell B., Paul S. M., Jones R. A., Woodward S., Zhou X. Q., McGinness J. M. Griffin W. S. (2000) Overexpression of the neuritotrophic cytokine S100beta precedes the appearance of neuritic beta-amyloid plaques in APPV717 F mice. J. Neurochem. 74, 295 301.
67. Simm A., Casselmann C., Schubert A., Hofmann S., Reimann A. Silber R.-E. (2004) Age associated changes of AGE-receptor expression: RAGE upregulation is associated with human heart dysfunction. Exp. Geron. 39, 407 413.
68. Suo Z., Tan J., Placzek A., Crawford F., Fang C. Mullan M. (1998) Alzheimer's beta-amyloid peptides induce inflammatory cascade in human vascular cells: the roles of cytokines and CD40. Brain Res. 807, 110 117.
69. Suzuki Y., Claflin J., Wang X., Lengi A. Kikuchi T. (2005) Microglia and macrophages as innate producers of interferon-gamma in the brain following infection with Toxoplasma gondii. Int. J. Parasitol. 35, 83 90.
70. Szczepanik A. M., Funes S., Petko W. Ringheim G. E. (2001) IL-4, IL-10 and IL-13 modulate A beta(1-42)-induced cytokine and chemokine production in primary murine microglia and a human monocyte cell line. J. Neuroimmunol. 113, 49 62.
71. Tan J., Town T., Paris D., Mori T., Suo Z., Crawford F., Mattson M. P., Flavell R. A. Mullan M. (1999) Microglial activation resulting from CD40-CD40 L interaction after beta-amyloid stimulation. Science 286, 2352 2355.
72. Tan J., Town T., Crawford F., Mori T., DelleDonne A., Crescentini R., Obregon D., Flavell R. A. Mullan M. J. (2002) Role of CD40 ligand in amyloidosis in transgenic Alzheimer's mice. Nat. Neurosci. 5, 1288 1293.
73. Townsend K. P., Shytle D. R., Bai Y. et al. (2004) Lovastatin modulation of microglial activation via suppression of functional CD40 expression. J. Neurosci. Res. 78, 167 176.
74. Vereker E., Campbell V., Roche E., McEntee E. Lynch M. A. (2000) Lipopolysaccharide inhibits long term potentiation in the rat dentate gyrus by activating caspase-1. J. Biol. Chem. 275, 26252 26258.
75. Wallace F. A., Miles E. A. Calder P. C. (2000) Activation state alters the effect of dietary fatty acids on pro-inflammatory mediator production by murine macrophages. Cytokine 12, 1374 1379.
76. Walsh D. M., Klyubin I., Fadeeva J. V., Cullen W. K., Anwyl R., Wolfe M. S., Rowan M. J. Selkoe D. J. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535 539.
77. Wang H. W., Pasternak J. F., Kuo H. et al. (2002) Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res. 924, 133 140.