Evidence of a protective effect of phosphatidylserine-containing liposomes on lipopolysaccharide-induced impairment of long-term potentiation in the rat hippocampus

Journal of Neuroimmunology

Volumn 151, Issue 1-2, 2004, Pages 12-23

  Nolan, Yvonne ^a   Martin, Darren ^b   Campbell, Veronica A ^b   Lynch, M A ^b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Hippocampus; IL 1 ; IL 10; Lipopolysaccharide; Long term potentiation; Phosphatidylserine

Indexed keywords

INTERLEUKIN 10; LIPOPOLYSACCHARIDE; LIPOSOME; PHOSPHATIDYLSERINE; SYNAPTOPHYSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; COGNITIVE DEFECT; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; ENZYME ACTIVATION; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; ENZYME ACTIVATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1; INTERLEUKIN-10; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOPOLYSACCHARIDES; LIPOSOMES; LONG-TERM POTENTIATION; MALE; MAP KINASE KINASE 4; MICROGLIA; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLSERINES; RATS; RATS, WISTAR;

EID: 2442581292     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2004.02.001     Document Type: Article

References (67)

1. Ajmone-Cat M.A., De Simone R., Nicolini A., Minghetti L. Effects of phosphatidylserine on p38 mitogen activated protein kinase, cyclic AMP responding element binding protein and nuclear factor-kappaB activation in resting and activated microglial cells. J. Neurochem. 84:2003;413-416
2. Allan S.M. The role of pro- and antiinflammatory cytokines in neurodegeneration. Ann. N.Y. Acad. Sci. 917:2000;84-93
3. Aramaki Y., Matsuno R., Tsuchiya S. Involvement of p38 MAP Kinase in the inhibitory effects of phosphatidylserine liposomes on nitric oxide production from macrophages stimulated with LPS. Biochem. Biophys. Res. Commun. 280:2001;982-987
4. Bach M.E., Barad M., Son H., Zhuo M., Lu Y.F., Shih R., Mansuy I., Hawkins R.D., Kandel E.R. Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 96:1999;5280-5285
5. Bachis A., Colangelo A.M., Vicini S., Doe P.P., De Bernardi M.A., Brooker G., Mocchetti I. Interleukin-10 prevents glutamate-mediated cerebellar granule cell death by blocking caspase-3-like activity. J. Neurosci. 21:2001;3104-3112
6. Bluthe R.M., Castanon N., Pousset F., Bristow A., Ball C., Lestage J., Michaud B., Kelley K.W., Dantzer R. Central injection of IL-10 antagonizes the behavioural effects of lipopolysaccharide in rats. Psychoneuroendocrinology. 24:1999;301-311
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254
8. Chauvet N., Palin K., Verrier D., Poole S., Dantzer R., Lestage J. Rat microglial cells secrete predominantly the precursor of interleukin-1beta in response to lipopolysaccharide. Eur. J. Neurosci. 14:2001;609-617
9. De S.R., Ajmone-Cat M.A., Nicolini A., Minghetti L. Expression of phosphatidylserine receptor and down-regulation of pro-inflammatory molecule production by its natural ligand in rat microglial cultures. J. Neuropathol. Exp. Neurol. 61:2002;237-244
10. De Freitas Balanco J.M., Moreira M.E., Bonomo A., Bozza P.T., Amarante-Mendes G., Pirmez C., Barcinski M.A. Apoptotic mimicry by an obligate intracellular parasite downregulates macrophage microbicidal activity. Curr. Biol. 11:2001;1870-1873
11. Diana G., Domenici M.R., Scotti de Carolis A., Loizzo A., Sagratella S. Reduced hippocampal CA1 Ca(2+)-induced long-term potentiation is associated with age-dependent impairment of spatial learning. Brain Res. 686:1995;107-110
12. Di Santo E., Sironi M., Pozzi P., Gnocchi P., Isetta A.M., Delvaux A., Goldman M., Marchant A., Ghezzi P. Interleukin-10 inhibits lipopolysaccharide- induced tumor necrosis factor and interleukin-1β production in the brain without affecting the activation of the hypothalamus-pituitary-adrenal axis. Neuroimmunomodulation. 2:1995;149-154
13. 2, and PAF. J. Clin. Invest. 101:1998;890-898
14. Fadok V.A., Bratton D.L., Rose D.M., Pearson A., Ezekewitz R.A., Henson P.M. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature. 405:2000;85-90
15. Fadok V.A., de Cathelineau A., Daleke D.L., Henson P.M., Bratton D.L. Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. J. Biol. Chem. 276:2001;1071-1077
16. Fadok V.A., Bratton D.L., Guthrie L.A., Henson P.M. Differential effects of apoptotic versus lysed cells on macrophage production of cytokines: role of proteases. J. Immunol. 166:2001;6847-6854
17. Fogarty M.P., Downer E.J., Campbell V. A role for c-Jun N-terminal kinase 1 (JNK1), but not JNK2, in the beta-amyloid-mediated stabilization of protein p53 and induction of the apoptotic cascade in cultured cortical neurons. Biochem. J. 371:2003;789-798
18. Friedman W.J. Cytokines regulate expression of the type 1 interleukin-1 receptor in rat hippocampal neurons and glia. Exp. Neurol. 168:2001;23-31
19. Gallucci S., Matzinger P. Danger signals: SOS to the immune system. Curr. Opin. Immunol. 13:2001;114-119
20. Goldman M., Marchant A., Schandene L. Endogenous interleukin-10 in inflammatory disorders: regulatory roles and pharmacological modulation. Ann. N.Y. Acad. Sci. 796:1996;282-293
21. Haan E.A., Bowen D.M. Protection of neocortical tissue prisms from freeze-thaw injury by dimethyl sulphoxide. J. Neurochem. 37:1981;243-246
22. Hambleton J., Weinstein S.L., Lem L., DeFranco A.L. Activation of c-Jun N-terminal kinase in bacterial lipopolysaccharide-stimulated macrophages. Proc. Natl. Acad. Sci. U. S. A. 93:1996;2774-2778
23. Hartlage-Rubsamen M., Lemke R., Schliebs R. Interleukin-1β, inducible nitric oxide synthase, and nuclear factor-kappaB are induced in morphologically distinct microglia after rat hippocampal lipopolysaccharide/ interferon-γ injection. J. Neurosci. Res. 57:1999;388-398
24. Hauss-Wegrzyniak B., Lukovic L., Bigaud M., Stoeckel M.E. Brain inflammatory response induced by intracerebroventricular infusion of lipopolysaccharide: an immunohistochemical study. Brain Res. 794:1998;211-224
25. Hetier E., Ayala J., Denefle P., Bousseau A., Rouget P., Mallat M., Prochiantz A. Brain macrophages synthesize interleukin-1 and interleukin-1 mRNAs in vitro. J. Neurosci. Res. 21:1988;391-397
26. Hirsch E.C., Breidert T., Rousselet E., Hunot S., Hartmann A., Michel P.P. The role of glial reaction and inflammation in Parkinson's disease. Ann. N.Y. Acad. Sci. 991:2003;214-228
27. Huynh M.L., Fadok V.A., Henson P.M. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-β1 secretion and the resolution of inflammation. J. Clin. Invest. 109:2002;41-50
28. Ilyin S.E., Gayle D., Flynn M.C., Plata-Salaman C.R. Interleukin-1β system (ligand, receptor type I, receptor accessory protein and receptor antagonist), TNF-α, TGF-β1 and neuropeptide Y mRNAs in specific brain regions during bacterial LPS-induced anorexia. Brain Res. Bull. 45:1998;507-515
29. Kelly A., Lynch A., Vereker E., Nolan Y., Queenan P., Whittaker E., O'Neill L.A., Lynch M.A. 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. 276:2001;45564-45572
30. Kelly A., Vereker E., Nolan Y., Brady M., Barry C., Loscher C.E., Mills K.H., Lynch M.A. 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. 278:2003;19453-19462
31. Lechan R.M., Toni R., Clark B.D., Cannon J.G., Shaw A.R., Dinarello C.A., Reichlin S. Immunoreactive interleukin-1β localization in the rat forebrain. Brain Res. 514:1990;135-140
32. Ledeboer A., Breve J.J., Poole S., Tilders F.J., Van Dam A.M. Interleukin-10, interleukin-4, and transforming growth factor-beta differentially regulate lipopolysaccharide-induced production of pro-inflammatory cytokines and nitric oxide in co-cultures of rat astroglial and microglial cells. Glia. 30:2000;134-142
33. Ledeboer A., Binnekade R., Brevé J.J., Bol J.G., Tilders F.J., Van Dam A.M. Site-specific modulation of LPS-induced fever and interleukin-1β expression in rats by interleukin-10. Am. J. Physiol., Regul. Integr. Comp. Physiol. 282:2002;R1762-R1772
34. Ledeboer A., Breve J.J., Wierinckx A., van der Jagt S., Bristow A.F., Leysen J.E., Tilders F.J., Van Dam A.M. Expression and regulation of interleukin-10 and interleukin-10 receptor in rat astroglial and microglial cells. Eur. J. Neurosci. 16:2002;1175-1185
35. Liu B., Hong J.S. Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J. Pharmacol. Exp. Ther. 304:2003;1-7
36. Lynch A.M., Lynch M.A. 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. 15:2002;1779-1788
37. Lynch A.M., Moore M., Craig S., Lonergan P.E., Lynch M.A. Irradiation upregulates IL-1β-induced cell signalling in hippocampus: protective effect of eicosapentaneoic acid. J. Physiol. 551P:2003;C36
38. Martin D.S., Lonergan P.E., Boland B., Fogarty M.P., Brady M., Horrobin D.F., Campbell V.A., Lynch M.A. 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. 277:2002;34239-34246
39. Meda L., Cassatella M.A., Szendrei G.I., Otvos L. Jr., Baron P., Villalba M., Ferrari D., Rossi F. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature. 374:1995;647-650
40. Minogue A.M., Schmid A.W., Fogarty M.P., Moore A.C., Campbell V.A., Herron C.E., Lynch M.A. 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. 278:2003;27971-27980
41. Molina-Holgado F., Grencis R., Rothwell N.J. Actions of exogenous and endogenous IL-10 on glial responses to bacterial LPS/cytokines. Glia. 33:2001;97-106
42. Molina-Holgado E., Vela J.M., Arevalo-Martin A., Guaza C. LPS/IFNγ cytotoxicity in oligodendroglial cells: role of nitric oxide and protection by the anti-inflammatory cytokine IL-10. Eur. J. Neurosci. 13:2001;493-502
43. Monastra G., Bruni A. Decreased serum level of tumor necrosis factor in animals treated with lipopolysaccharide and liposomes containing phosphatidylserine. Lymphokine Cytokine Res. 11:1992;39-43
44. Murray C.A., Lynch M.A. Evidence that increased hippocampal expression of the cytokine interleukin-1β is a common trigger for age- and stress-induced impairments in long-term potentiation. J. Neurosci. 18:1998;2974-2981
45. Nick J.A., Avdi N.J., Gerwins P., Jognson G.L., Worthen G.S. Activation of a p38 mitogen-activated protein kinase in human neutrophils by lipopolysaccharide. J. Immunol. 156:1996;4867-4875
46. Nolan Y., Minogue A., Vereker E., Bolton A.E., Campbell V.A., Lynch M.A. Attenuation of LPS-induced changes in synaptic activity in rat hippocampus by Vasogen's Immune Modulation Therapy. Neuroimmunomodulation. 10:2002;40-46
47. Nolan Y., Vereker E., Lynch A.M., Lynch M.A. Evidence that lipopolysaccharide-induced cell death is mediated by accumulation of reactive oxygen species and activation of p38 in rat cortex and hippocampus. Exp. Neurol. 184:2003;794-804
48. O'Donnell E., Vereker E., Lynch M.A. Age-related impairment in LTP is accompanied by enhanced activity of stress-activated protein kinases: analysis of underlying mechanisms. Eur. J. Neurosci. 12:2000;345-352
49. O'Neill L.A. Signal transduction pathways activated by the IL-1 receptor/toll-like receptor superfamily. Curr. Top. Microbiol. Immunol. 270:2002;47-61
50. Orr C.F., Rowe D.B., Halliday G.M. An inflammatory review of Parkinson's disease. Prog. Neurobiol. 68:2002;325-340
51. Parker L.C., Luheshi G.N., Rothwell N.J., Pinteaux E. IL-1β signalling in glial cells in wildtype and IL-1RI deficient mice. Br. J. Pharmacol. 136:2002;312-320
52. Pyo H., Jou I., Jung S., Hong S., Joe E.-H. Mitogen-activated protein kinases activated by lipopolysaccharide and β-amyloid in cultured rat microglia. NeuroReport. 9:1998;871-874
53. Quan N., Sundar S.K., Weiss J.M. Induction of interleukin-1 in various brain regions after peripheral and central injections of lipopolysaccharide. J. Neuroimmunol. 49:1994;125-134
54. Schumann R.R., Pfeil D., Freyer D., Buerger W., Lamping N., Kirschning C.J., Goebel U.B., Weber J.R. Lipopolysaccharide and pneumococcal cell wall components activate the mitogen activated protein kinases (MAPK) erk-1, erk-2, and p38 in astrocytes. Glia. 22:1998;295-305
55. Sherry B., Espinoza M., Manogue K.R., Cerami A. Induction of the chemokine β peptides, MIP-1α and MIP-1β, by lipopolysaccharide is differentially regulated by immunomodulatory cytokines γ-IFN, IL-10, IL-4, and TGF-β Mol. Med. 4:1998;648-657
56. Suzuki S., Yamatoya H., Sakai M., Kataoka A., Furushiro M., Kudo S. Oral administration of soybean lecithin transphosphatidylated phosphatidylserine improves memory impairment in aged rats. J. Nutr. 131:2001;2951-2956
57. Suzuki K., Hino M., Kutsuna H., Hato F., Sakamoto C., Takahashi T., Tatsumi N., Kitagawa S. Selective activation of p38 mitogen-activated protein kinase cascade in human neutrophils stimulated by IL-1β J. Immunol. 167:2001;5940-5947
58. Szczepanik A.M., Funes S., Petko W., Ringheim G.E. IL-4, IL-10 and IL-13 modulate Aβ(1-42)-induced cytokine and chemokine production in primary murine microglia and a human monocyte cell line. J. Neuroimmunol. 113:2001;49-62
59. Van Dam A.M., Poole S., Schultzberg M., Zavala F., Tilders F.J. Effects of peripheral administration of LPS on the expression of immunoreactive interleukin-1 alpha, beta, and receptor antagonist in rat brain. Ann. N.Y. Acad. Sci. 840:1998;128-138
60. Van der Poll T., Jansen P.M., Montegut W.J., Braxton C.C., Calvano S.E., Stackpole S.A., Smith S.R., Swanson S.W., Hack C.E., Lowry S.F., Moldawer L.L. Effects of IL-10 on systemic inflammatory responses during sublethal primate endotoxemia. J. Immunol. 158:1997;1971-1975
61. Vereker E., Campbell V., Roche E., McEntee E., Lynch M.A. Lipopolysaccharide inhibits long term potentiation in the rat dentate gyrus by activating caspase-1. J. Biol. Chem. 275:2000;26252-26258
62. Vereker E., O'Donnell E., Lynch M.A. The inhibitory effect of interleukin-1β on long-term potentiation is coupled with increased activity of stress-activated protein kinases. J. Neurosci. 20:2000;6811-6819
63. Vereker E., O'Donnell E., Lynch A., Kelly A., Nolan Y., Lynch M.A. Evidence that interleukin-1β and reactive oxygen species production play a pivotal role in stress-induced impairment of LTP in the rat dentate gyrus. Eur. J. Neurosci. 14:2001;1809-1819
64. Watt J.A., Hobbs N.K. Interleukin-1β immunoreactivity in identified neurons of the rat magnocellular neurosecretory system: evidence for activity-dependent release. J. Neurosci. Res. 60:2000;478-489
65. Yao J., Keri J.E., Taffs R.E., Colton C.A. Characterization of interleukin-1 production by microglia in culture. Brain Res. 591:1992;88-93
66. Zanotti A., Valzelli L., Toffano G. Chronic phosphatidylserine treatment improves spatial memory and passive avoidance in aged rats. Psychopharmacology (Berl.). 99:1989;316-321
67. Zhang P., Miller B.S., Rosenzweig S.A., Bhat N.R. Activation of C-jun N-terminal kinase/stress-activated protein kinase in primary glial cultures. J. Neurosci. Res. 46:1996;114-121