Neuroprotective actions of eicosapentaenoic acid on lipopolysaccharide- induced dysfunction in rat hippocampus

Journal of Neurochemistry

Volumn 91, Issue 1, 2004, Pages 20-29

  Lonergan, Peter E ^a   Martin, Darren S D ^a   Horrobin, David F ^b   Lynch, Marina A ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b Laxdale Ltd   (United Kingdom)

Author keywords

c Jun N terminal kinase; Eicosapentaenoic acid; Hippocampus; Interleukin 1 ; Lipopolysaccharide; Long term potentiation

Indexed keywords

CYTOCHROME C; ICOSAPENTAENOIC ACID; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MITOCHONDRIAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEIN BAX; PROTEIN BCL 2; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DYSFUNCTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPTIC POTENTIAL;

ANIMALS; ANIMALS, NEWBORN; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; BRAIN DISEASES; CELLS, CULTURED; CYTOCHROMES C; CYTOSOL; DRUG INTERACTIONS; EICOSAPENTAENOIC ACID; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; INTERLEUKIN-1; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOPOLYSACCHARIDES; LONG-TERM POTENTIATION; MITOCHONDRIA; NEURAL INHIBITION; NEUROPROTECTIVE AGENTS; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-JUN; RATS; RATS, WISTAR; TIME FACTORS;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 4744369972     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02689.x     Document Type: Article

References (59)

1. Alikhani M., Alikhani Z., He H., Liu R., Popek B. I. and Graves D. T. (2003) Lipopolysaccharides indirectly stimulate apoptosis and global induction of apoptotic genes in fibroblasts. J. Biol. Chem. 278, 52901-52908.
2. Babcock T., Helton W. S. and Espat N. J. (2000) Eicosapentaenoic acid (EPA): an antiinflammatory omega-3 fat with potential clinical applications. Nutrition 16, 1116-1118.
3. Babcock T. A., Novak T., Ong E., Jho D. H., Helton W. S. and Espat N. J. (2002) Modulation of lipopolysaccharide-stimulated macrophage tumor necrosis factor-α production by omega-3 fatty acid is associated with differential cyclooxygenase-2 protein expression and is independent of interleukin-10. J. Surg. Res. 107, 135-139.
4. Barry C. E. and Lynch M. A. (2003) The role of c-Jun N-terminal kinase in lipopolysaccharide-induced cell deterioration in rat hippocampus. J. Physiol. (Lond.) 551, 23P.
5. Bellinger F. P., Madamba S. and Siggins G. R. (1993) Interleukin-1β inhibits synaptic strength and long-term potentiation in the rat CA1 hippocampus. Brain Res. 628, 227-234.
6. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
7. Calder P. C. (2001) Polyunsaturated fatty acids, inflammation, and immunity. Lipids 36, 1007-1024.
8. Calder P. C. and Zurier R. B. (2001) Polyunsaturated fatty acids and rheumatoid arthritis. Curr. Opin. Clin. Nutr. Metab. Care 4, 115-121.
9. Choi W. S., Yoon S. Y., Oh T. H., Choi E. J., O'Malley K. L. and Oh Y. J. (1999) Two distinct mechanisms are involved in 6-hydroxydopamine- and MPP+-induced dopaminergic neuronal cell death: role of caspases, ROS, and JNK. J. Neurosci. Res. 57, 86-94.
10. Comalada M., Xaus J., Valledor A. F., Lopez-Lopez C., Pennington D. J. and Celada A. (2003) PKCε is involved in JNK activation that mediates LPS-induced TNF-α, which induces apoptosis in macrophages. Am. J. Physiol. Cell Physiol. 285, C1235-C1245.
11. Cortopassi G. A. and Wong A. (1999) Mitochondria in organismal aging and degeneration. Biochim. Biophys. Acta 1410, 183-193.
12. Cunningham A. J., Murray C. A., O'Neill L. A. J., Lynch M. A. and O'Connor J. J. (1996) Interleukin-1β (IL-1β) and tumour necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro. Neurosci. Lett. 203, 17-20.
13. Curran B. P., Murray H. J. and O'Connor J. J. (2003) A role for c-Jun N-terminal kinase in the inhibition of long-term potentiation by interleukin-1β and long-term depression in the rat dentate gyrus in vitro. Neuroscience 118, 347-357.
14. Curtis C. L., Hughes C. E., Flannery C. R., Little C. B., Harwood J. L. and Caterson B. (2000) n-3 fatty acids specifically modulate catabolic factors involved in articular cartilage degradation. J. Biol. Chem. 275, 721-724.
15. Fuchs S. Y., Adler V., Pincus M. R. and Ronai Z. (1998) MEKK1/JNK signaling stabilizes and activates p53. Proc. Natl Acad. Sci. USA 95, 10541-10546.
16. Haldar S., Jena N. and Croce C. M. (1995) Inactivation of Bcl-2 by phosphorylation. Proc. Natl Acad. Sci. USA 92, 4507-4511.
17. Harper S. J. and LoGrasso P. (2001) Signalling for survival and death in neurones: the role of stress-activated kinases, JNK and p38. Cell. Signal. 13, 299-310.
18. Hauss-Wegrzyniak B., Vraniak P. and Wenk G. L. (1999) The effects of a novel NSAID on chronic neuroinflammation are age dependent. Neurobiol. Aging 20, 305-313.
19. Hayashi H., Tanaka Y., Hibino H., Umeda Y., Kawamitsu H., Fujimoto H. and Amakawa T. (1999) Beneficial effect of salmon roe phosphatidylcholine in chronic liver disease. Curr. Med. Res. Opin. 15, 177-184.
20. Ip Y. T. and Davis R. J. (1998) Signal transduction by the c-Jun N-terminal kinase (JNK) - from inflammation to development. Curr. Opin. Cell Biol. 10, 205-219.
21. Kannan K. and Jain S. K. (2000) Oxidative stress and apoptosis. Pathophysiology 7, 153-163.
22. Katsuki H., Nakai S., Hirai Y., Akaji K., Kiso Y. and Satoh M. (1990) Interleukin-1β inhibits long-term potentiation in the CA3 region of mouse hippocampal slices. Eur. J. Pharmacol. 181, 323-326.
23. Kelly A., Lynch A., Vereker E., Nolan Y., Queenan P., Whittaker E., O'Neill L. A. J. and Lynch M. A. (2001) The anti-inflammatory cytokine, interleukin (IL)-10, blocks the inhibitory effect of IL-1β on long term potentiation. A role for JNK. J. Biol. Chem. 276, 45564-45572.
24. Kelly A., Vereker E., Nolan Y., Brady M., Barry C., Loscher C. E., Mills K. H. G. and Lynch M. A. (2003) Activation of p38 plays a pivotal role in the inhibitory effect of lipopolysaccharide and interleukin-1β on long term potentiation in rat dentate gyrus. J. Biol. Chem. 278, 19453-19462.
25. Kim H. Y., Akbar M. and Kim K. Y. (2001) Inhibition of neuronal apoptosis by polyunsaturated fatty acids. J. Mol. Neurosci. 16, 223-227; discussion 279-284.
26. Kim H. Y., Akbar M., Lau A. and Edsall L. (2000) Inhibition of neuronal apoptosis by docosahexaenoic acid (22:6n-3). Role of phosphatidylserine in antiapoptotic effect. J. Biol. Chem. 275, 35215-35223.
27. Kluck R. M., Bossy-Wetzel E., Green D. R. and Newmeyer D. D. (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136.
28. Kumagae Y., Zhang Y., Kim O. J. and Miller C. A. (1999) Human c-Jun N-terminal kinase expression and activation in the nervous system. Brain Res. Mol. Brain Res. 67, 10-17.
29. Liu X., Kim C. N., Yang J., Jemmerson R. and Wang X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86, 147-157.
30. Lonergan P. E., Martin D. S. D., Horrobin D. F. and Lynch M. A. (2002) Neuroprotective effect of eicosapentaenoic acid in hippocampus of rats exposed to gamma-irradiation. J. Biol. Chem. 277, 20804-20811.
31. Loscher C. E., Donnelly S., Mills K. H. and Lynch M. A. (2000) Interleukin-1β-dependent changes in the hippocampus following parenteral immunization with a whole cell pertussis vaccine. J. Neuroimmunol. 111, 68-76.
32. MacKichan M. L. and DeFranco A. L. (1999) Role of ceramide in lipopolysaccharide (LPS)-induced signaling. LPS increases ceramide rather than acting as a structural homolog. J. Biol. Chem. 274, 1767-1775.
33. Martin D. S. D., Lonergan P. E., Boland B., Fogarty M. P., Brady M., Horrobin D. F., Campbell V. A. and Lynch M. A. (2002) Apoptotic changes in the aged brain are triggered by interleukin-1β-induced activation of p38 and reversed by treatment with eicosapentaenoic acid. J. Biol. Chem. 277, 34239-34246.
34. Martinou J. C. and Sadoul R. (1996) ICE-like proteases execute the neuronal death program. Curr. Opin. Neurobiol. 6, 609-614.
35. Maundrell K., Antonsson B., Magnenat E. et al. (1997) Bcl-2 undergoes phosphorylation by c-Jun N-terminal kinase/stress-activated protein kinases in the presence of the constitutively active GTP-binding protein Rac1. J. Biol. Chem. 272, 25238-25242.
36. 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.
37. Mielke K., Damm A., Yang D. D. and Herdegen T. (2000) Selective expression of JNK isoforms and stress-specific JNK activity in different neural cell lines. Brain Res. Mol. Brain Res. 75, 128-137.
38. Minogue A. M., Schmid A. W., Fogarty M. P., Moore A. C., Campbell V. A., Herron C. E. and Lynch M. A. (2003) Activation of the c-Jun N-terminal kinase signaling cascade mediates the effect of amyloid-β on long term potentiation and cell death in hippocampus: a role for interleukin-1β? J. Biol. Chem. 278, 27971-27980.
39. Miyashita T., Krajewski S., Krajewska M., Wang H. G., Lin H. K., Liebermann D. A., Hoffman B. and Reed J. C. (1994) Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9, 1799-1805.
40. Neary J. (1997) MAPK cascades in cell growth and death. News Physiol. Sci. 12, 286-293.
41. Nick J. A., Avdi N. J., Gerwins P., Johnson G. L. and Worthen G. S. (1996) Activation of a p38 mitogen-activated protein kinase in human neutrophils by lipopolysaccharide. J. Immunol. 156, 4867-4875.
42. Nolan Y., Minogue A., Vereker E., Bolton A. E., Campbell V. A. and Lynch M. A. (2002) Attenuation of LPS-induced changes in synaptic activity in rat hippocampus by Vasogen's Immune Modulation Therapy. Neuroimmunomodulation 10, 40-46.
43. Nolan Y., Martin D., Campbell V. A. and Lynch M. A. (2004) Evidence of a protective effect of phosphatidylserine on lipopolysaccharide-induced impairment of long-term potentiation in the rat hippocampus. J. Neuroimmunol. 151, 12-23.
44. O'Brien M. A., Moravec R. A. and Riss T. L. (2001) Poly (ADP-ribose) polymerase cleavage monitored in situ in apoptotic cells. Biotechniques 30, 886-891.
45. O'Donnell E., Vereker E. and 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.
46. Park D. S., Stefanis L., Yan C. Y., Farinelli S. E. and Greene L. A. (1996) Ordering the cell death pathway. Differential effects of BCL2, an interleukin-1-converting enzyme family protease inhibitor, and other survival agents on JNK activation in serum/nerve growth factor-deprived PC12 cells. J. Biol. Chem. 271, 21898-21905.
47. Pastorino J. G., Chen S. T., Tafani M., Snyder J. W. and Farber J. L. (1998) The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition. J. Biol. Chem. 273, 7770-7775.
48. Picot L., Chevalier S., Mezghani-Abdelmoula S., Merieau A., Lesouhaitier O., Leroux P., Cazin L., Orange N. and Feuilloley M. G. J. (2003) Cytotoxic effects of the lipopolysaccharide from Pseudomonas fluorescens on neurons and glial cells. Microb. Pathog. 35, 95-106.
49. Pugh C. R., Kumagawa K., Fleshner M., Watkins L. R., Maier S. F. and Rudy J. W. (1998) Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain Behav. Immun. 12, 212-229.
50. Pyo H., Jou I., Jung S., Hong S. and Joe E. H. (1998) Mitogen-activated protein kinases activated by lipopolysaccharide and β-amyloid in cultured rat microglia. Neuroreport 9, 871-874.
51. Sadeghi S., Wallace F. A. and Calder P. C. (1999) Dietary lipids modify the cytokine response to bacterial lipopolysaccharide in mice. Immunology 96, 404-410.
52. Shaw K. N., Commins S. and O'Mara S. M. (2001) Lipopolysaccharide causes deficits in spatial learning in the watermaze but not in BDNF expression in the rat dentate gyrus. Behav. Brain Res. 124, 47-54.
53. Slee E. A., Harte M. T., Kluck R. M. et al. (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J. Cell Biol. 144, 281-292.
54. Vereker E., Campbell V., Roche E., McEntee E. and Lynch M. A. (2000a) Lipopolysaccharide inhibits long term potentiation in the rat dentate gyrus by activating caspase-1. J. Biol. Chem. 275, 26252-26258.
55. Vereker E., O'Donnell E. and Lynch M. A. (2000b) The inhibitory effect of interleukin-1β on long-term potentiation is coupled with increased activity of stress-activated protein kinases. J. Neurosci. 20, 6811-6819.
56. Wallace F. A., Miles E. A. and 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.
57. Xia Z., Dickens M., Raingeaud J., Davis R. J. and Greenberg M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331.
58. Yamamoto K., Ichijo H. and Korsmeyer S. J. (1999) BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G (2) /M. Mol. Cell. Biol. 19, 8469-8478.
59. Yang J., Liu X., Bhalla K., Kim C. N., Ibrado A. M., Cai J., Peng T. I., Jones D. P. and Wang X. (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132.