Low energy laser light (632.8 nm) suppresses amyloid-β peptide-induced oxidative and inflammatory responses in astrocytes

Neuroscience

Volumn 171, Issue 3, 2010, Pages 859-868

  Yang, X ^a   Askarova, S ^a   Sheng, W ^b   Chen, J K ^c   Sun, A Y ^b   Sun, G Y ^b   Yao, G ^a   Lee, J C M ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c University of Missouri   (United States)

Author keywords

Inflammation; INOS; Interleukin 1 ; NADPH oxidase; Oxidative stress; Phospholipase A2

Indexed keywords

AMYLOID BETA PROTEIN; CYTOSOLIC PHOSPHOLIPASE A2; HYDROETHIDINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; PHOSPHOLIPASE A2; PROTEIN P47 PHOX; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SUPEROXIDE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; ASTROCYTE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; ENZYME PHOSPHORYLATION; FLUORESCENCE MICROSCOPY; HELIUM NEON LASER; INFLAMMATORY CELL; LOW LEVEL LASER THERAPY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, RADIATION; INFLAMMATION MEDIATORS; LASER THERAPY, LOW-LEVEL; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; RATS; SUPEROXIDES;

EID: 78349305935     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.09.025     Document Type: Article

References (88)

1. Abdel S.E., Abdel-Meguid I., Korraa S. Markers of oxidative stress and aging in Duchene muscular dystrophy patients and the possible ameliorating effect of He:Ne laser. Acta Myol 2007, 26:14-21.
2. Abramov A.Y., Canevari L., Duchen M.R. Beta-amyloid peptides induce mitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase. J Neurosci 2004, 24:565-575.
3. Aimbire F., Ligeiro de Oliveira A.P., Albertini R., Correa J.C., Ladeira de Campos C.B., Lyon J.P., Silva J.A., Costa M.S. Low level laser therapy (LLLT) decreases pulmonary microvascular leakage, neutrophil influx and IL-1beta levels in airway and lung from rat subjected to LPS-induced inflammation. Inflammation 2008, 31:189-197.
4. Akama K.T., Albanese C., Pestell R.G., Van Eldik L.J. Amyloid beta-peptide stimulates nitric oxide production in astrocytes through an NFkappaB-dependent mechanism. Proc Natl Acad Sci U S A 1998, 95:5795-5800.
5. Akama K.T., Van Eldik L.J. Beta-amyloid stimulation of inducible nitric-oxide synthase in astrocytes is interleukin-1beta- and tumor necrosis factor-alpha (TNFalpha)-dependent, and involves a TNFalpha receptor-associated factor- and NFkappaB-inducing kinase-dependent signaling mechanism. J Biol Chem 2000, 275:7918-7924.
6. Albertini R., Villaverde A.B., Aimbire F., Salgado M.A., Bjordal J.M., Alves L.P., Munin E., Costa M.S. Anti-inflammatory effects of low-level laser therapy (LLLT) with two different red wavelengths (660 nm and 684 nm) in carrageenan-induced rat paw edema. J Photochem Photobiol B 2007, 89:50-55.
7. Anders J.J., Borke R.C., Woolery S.K., Van de Merwe W.P. Low power laser irradiation alters the rate of regeneration of the rat facial nerve. Lasers Surg Med 1993, 13:72-82.
8. Baeuerle P.A. Pro-inflammatory signaling: last pieces in the NF-kappaB puzzle?. Curr Biol 1998, 8:R19-R22.
9. Behl C., Davis J.B., Lesley R., Schubert D. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 1994, 77:817-827.
10. Behl C., Holsboer F. [Oxidative stress in the pathogenesis of Alzheimer's disease and antioxidant neuroprotection]. Fortschr Neurol Psychiatr 1998, 66:113-121.
11. Blom M.A., van Twillert M.G., de Vries S.C., Engels F., Finch C.E., Veerhuis R., Eikelenboom P. NSAIDS inhibit the IL-1 beta-induced IL-6 release from human post-mortem astrocytes: the involvement of prostaglandin E2. Brain Res 1997, 777:210-218.
12. Bolmont T., Haiss F., Eicke D., Radde R., Mathis C.A., Klunk W.E., Kohsaka S., Jucker M., Calhoun M.E. Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. J Neurosci 2008, 28:4283-4292.
13. Bortoletto R., Silva N.S., Zangaro R.A., Pacheco M.T., Da Matta R.A., Pacheco-Soares C. Mitochondrial membrane potential after low-power laser irradiation. Lasers Med Sci 2004, 18:204-206.
14. Boschi E.S., Leite C.E., Saciura V.C., Caberlon E., Lunardelli A., Bitencourt S., Melo D.A., Oliveira J.R. Anti-inflammatory effects of low-level laser therapy (660 nm) in the early phase in carrageenan-induced pleurisy in rat. Lasers Surg Med 2008, 40:500-508.
15. Byrnes K.R., Waynant R.W., Ilev I.K., Wu X., Barna L., Smith K., Heckert R., Gerst H., Anders J.J. Light promotes regeneration and functional recovery and alters the immune response after spinal cord injury. Lasers Surg Med 2005, 36:171-185.
16. Cameron B., Landreth G.E. Inflammation, microglia, and Alzheimer's disease. Neurobiol Dis 2010, 37:503-509.
17. Cao Z., Xiong J., Takeuchi M., Kurama T., Goeddel D.V. TRAF6 is a signal transducer for interleukin-1. Nature 1996, 383:443-446.
18. Chapman K.E., Sinclair S.E., Zhuang D., Hassid A., Desai L.P., Waters C.M. Cyclic mechanical strain increases reactive oxygen species production in pulmonary epithelial cells. Am J Physiol Lung Cell Mol Physiol 2005, 289:L834-L841.
19. Cini M., Moretti A. Studies on lipid peroxidation and protein oxidation in the aging brain. Neurobiol Aging 1995, 16:53-57.
20. Combs C.K. Inflammation and microglia actions in Alzheimer's disease. J Neuroimmune Pharmacol 2009, 4:380-388.
21. Correa F., Lopes Martins R.A., Correa J.C., Iversen V.V., Joenson J., Bjordal J.M. Low-level laser therapy (GaAs lambda = 904 nm) reduces inflammatory cell migration in mice with lipopolysaccharide-induced peritonitis. Photomed Laser Surg 2007, 25:245-249.
22. Diebold B.A., Bokoch G.M. Molecular basis for Rac2 regulation of phagocyte NADPH oxidase. Nat Immunol 2001, 2:211-215.
23. Duan R., Zhu L., Liu T.C., Li Y., Liu J., Jiao J., Xu X., Yao L., Liu S. Light emitting diode irradiation protect against the amyloid beta 2535 induced apoptosis of PC12 cell in vitro. Lasers Surg Med 2003, 33:199-203.
24. Eells J.T., Wong-Riley M.T., VerHoeve J., Henry M., Buchman E.V., Kane M.P., Gould L.J., Das R., Jett M., Hodgson B.D., Margolis D., Whelan H.T. Mitochondrial signal transduction in accelerated wound and retinal healing by near-infrared light therapy. Mitochondrion 2004, 4:559-567.
25. Fiebich B.L., Hull M., Lieb K., Schumann G., Berger M., Bauer J. Potential link between interleukin-6 and arachidonic acid metabolism in Alzheimer's disease. J Neural Transm Suppl 1998, 54:268-278.
26. Fillipin L.I., Mauriz J.L., Vedovelli K., Moreira A.J., Zettler C.G., Lech O., Marroni N.P., Gonzalez-Gallego J. Low-level laser therapy (LLLT) prevents oxidative stress and reduces fibrosis in rat traumatized Achilles tendon. Lasers Surg Med 2005, 37:293-300.
27. Forster M.J., Dubey A., Dawson K.M., Stutts W.A., Lal H., Sohal R.S. Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc Natl Acad Sci U S A 1996, 93:4765-4769.
28. Freitas A.C., Pinheiro A.L., Miranda P., Thiers F.A., Vieira A.L. Assessment of anti-inflammatory effect of 830nm laser light using C-reactive protein levels. Braz Dent J 2001, 12:187-190.
29. Giuliani A., Lorenzini L., Gallamini M., Massella A., Giardino L., Calza L. Low infra red laser light irradiation on cultured neural cells: effects on mitochondria and cell viability after oxidative stress. BMC Complement Altern Med 2009, 9:8.
30. Griffin W.S., Mrak R.E. Interleukin-1 in the genesis and progression of and risk for development of neuronal degeneration in Alzheimer's disease. J Leukoc Biol 2002, 72:233-238.
31. Griffin W.S., Sheng J.G., Royston M.C., Gentleman S.M., McKenzie J.E., Graham D.I., Roberts G.W., Mrak R.E. Glial-neuronal interactions in Alzheimer's disease: the potential role of a "cytokine cycle" in disease progression. Brain Pathol 1998, 8:65-72.
32. Groemping Y., Rittinger K. Activation and assembly of the NADPH oxidase: a structural perspective. Biochem J 2005, 386:401-416.
33. Gupta A., Hasan M., Chander R., Kapoor N.K. Age-related elevation of lipid peroxidation products: diminution of superoxide dismutase activity in the central nervous system of rats. Gerontology 1991, 37:305-309.
34. Hamilton M.L., Van Remmen H., Drake J.A., Yang H., Guo Z.M., Kewitt K., Walter C.A., Richardson A. Does oxidative damage to DNA increase with age?. Proc Natl Acad Sci U S A 2001, 98:10469-10474.
35. Hammer K.D., Hillwig M.L., Neighbors J.D., Sim Y.J., Kohut M.L., Wiemer D.F., Wurtele E.S., Birt D.F. Pseudohypericin is necessary for the light-activated inhibition of prostaglandin E2 pathways by a 4 component system mimicking an Hypericum perforatum fraction. Phytochemistry 2008, 69:2354-2362.
36. Han C.H., Freeman J.L., Lee T., Motalebi S.A., Lambeth J.D. Regulation of the neutrophil respiratory burst oxidase.. Identification of an activation domain in p67(phox). J Biol Chem 1998, 273:16663-16668.
37. Hebert L.E., Scherr P.A., Bienias J.L., Bennett D.A., Evans D.A. Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch Neurol 2003, 60:1119-1122.
38. Heneka M.T., O'Banion M.K. Inflammatory processes in Alzheimer's disease. J Neuroimmunol 2007, 184:69-91.
39. Hirai K., Aliev G., Nunomura A., Fujioka H., Russell R.L., Atwood C.S., Johnson A.B., Kress Y., Vinters H.V., Tabaton M., Shimohama S., Cash A.D., Siedlak S.L., Harris P.L., Jones P.K., Petersen R.B., Perry G., Smith M.A. Mitochondrial abnormalities in Alzheimer's disease. J Neurosci 2001, 21:3017-3023.
40. Hu J., Ferreira A., Van Eldik L.J. S100beta induces neuronal cell death through nitric oxide release from astrocytes. J Neurochem 1997, 69:2294-2301.
41. Huang Y.Y., Chen A.C., Carroll J.D., Hamblin M.R. Biphasic dose response in low level light therapy. Dose Response 2009, 7:358-383.
42. Huber J., Furnkranz A., Bochkov V.N., Patricia M.K., Lee H., Hedrick C.C., Berliner J.A., Binder B.R., Leitinger N. Specific monocyte adhesion to endothelial cells induced by oxidized phospholipids involves activation of cPLA2 and lipoxygenase. J Lipid Res 2006, 47:1054-1062.
43. Karageuzyan K.G., Sekoyan E.S., Karagyan A.T., Pogosyan N.R., Manucharyan G.G., Sekoyan A.E., Tunyan A.Y., Boyajyan V.G., Karageuzyan M.K. Phospholipid pool, lipid peroxidation, and superoxide dismutase activity under various types of oxidative stress of the brain and the effect of low-energy infrared laser irradiation. Biochemistry (Mosc) 1998, 63:1226-1232.
44. Koenigsknecht-Talboo J., Meyer-Luehmann M., Parsadanian M., Garcia-Alloza M., Finn M.B., Hyman B.T., Bacskai B.J., Holtzman D.M. Rapid microglial response around amyloid pathology after systemic anti-Abeta antibody administration in PDAPP mice. J Neurosci 2008, 28:14156-14164.
45. Lapchak P.A., Wei J., Zivin J.A. Transcranial infrared laser therapy improves clinical rating scores after embolic strokes in rabbits. Stroke 2004, 35:1985-1988.
46. Lee S.C., Dickson D.W., Liu W., Brosnan C.F. Induction of nitric oxide synthase activity in human astrocytes by interleukin-1 beta and interferon-gamma. J Neuroimmunol 1993, 46:19-24.
47. Liang H.L., Whelan H.T., Eells J.T., Meng H., Buchmann E., Lerch-Gaggl A., Wong-Riley M. Photobiomodulation partially rescues visual cortical neurons from cyanide-induced apoptosis. Neuroscience 2006, 139:639-649.
48. Liang H.L., Whelan H.T., Eells J.T., Wong-Riley M.T. Near-infrared light via light-emitting diode treatment is therapeutic against rotenone- and 1-methyl-4-phenylpyridinium ion-induced neurotoxicity. Neuroscience 2008, 153:963-974.
49. Lim W., Lee S., Kim I., Chung M., Kim M., Lim H., Park J., Kim O., Choi H. The anti-inflammatory mechanism of 635 nm light-emitting-diode irradiation compared with existing COX inhibitors. Lasers Surg Med 2007, 39:614-621.
50. Lovell M.A., Markesbery W.R. Oxidative DNA damage in mild cognitive impairment and late-stage Alzheimer's disease. Nucleic Acids Res 2007, 35:7497-7504.
51. McGeer P.L., McGeer E.G. The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res Brain Res Rev 1995, 21:195-218.
52. McGeer P.L., McGeer E.G. Inflammation, autotoxicity and Alzheimer disease. Neurobiol Aging 2001, 22:799-809.
53. McNaull B.B., Todd S., McGuinness B., Passmore A.P. Inflammation and anti-inflammatory strategies for Alzheimer's disease-a mini-review. Gerontology 2010, 56:3-14.
54. Mecocci P., Beal M.F., Cecchetti R., Polidori M.C., Cherubini A., Chionne F., Avellini L., Romano G., Senin U. Mitochondrial membrane fluidity and oxidative damage to mitochondrial DNA in aged and AD human brain. Mol Chem Neuropathol 1997, 31:53-64.
55. Mecocci P., MacGarvey U., Beal M.F. Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann Neurol 1994, 36:747-751.
56. Mizrahi A., Berdichevsky Y., Ugolev Y., Molshanski-Mor S., Nakash Y., Dahan I., Alloul N., Gorzalczany Y., Sarfstein R., Hirshberg M., Pick E. Assembly of the phagocyte NADPH oxidase complex: chimeric constructs derived from the cytosolic components as tools for exploring structure-function relationships. J Leukoc Biol 2006, 79:881-895.
57. Qin L., Liu Y., Cooper C., Liu B., Wilson B., Hong J.S. Microglia enhance beta-amyloid peptide-induced toxicity in cortical and mesencephalic neurons by producing reactive oxygen species. J Neurochem 2002, 83:973-983.
58. Reis S.R., Medrado A.P., Marchionni A.M., Figueira C., Fracassi L.D., Knop L.A. Effect of 670-nm laser therapy and dexamethasone on tissue repair: a histological and ultrastructural study. Photomed Laser Surg 2008, 26:307-313.
59. Rojas J.C., Lee J., John J.M., Gonzalez-Lima F. Neuroprotective effects of near-infrared light in an in vivo model of mitochondrial optic neuropathy. J Neurosci 2008, 28:13511-13521.
60. Sakurai Y., Yamaguchi M., Abiko Y. Inhibitory effect of low-level laser irradiation on LPS-stimulated prostaglandin E2 production and cyclooxygenase-2 in human gingival fibroblasts. Eur J Oral Sci 2000, 108:29-34.
61. Schippling S., Kontush A., Arlt S., Buhmann C., Sturenburg H.J., Mann U., Muller-Thomsen T., Beisiegel U. Increased lipoprotein oxidation in Alzheimer's disease. Free Radic Biol Med 2000, 28:351-360.
62. Shefer G., Partridge T.A., Heslop L., Gross J.G., Oron U., Halevy O. Low-energy laser irradiation promotes the survival and cell cycle entry of skeletal muscle satellite cells. J Cell Sci 2002, 115:1461-1469.
63. Shelat P.B., Chalimoniuk M., Wang J.H., Strosznajder J.B., Lee J.C., Sun A.Y., Simonyi A., Sun G.Y. Amyloid beta peptide and NMDA induce ROS from NADPH oxidase and AA release from cytosolic phospholipase A2 in cortical neurons. J Neurochem 2008, 106:45-55.
64. Shimohama S., Tanino H., Kawakami N., Okamura N., Kodama H., Yamaguchi T., Hayakawa T., Nunomura A., Chiba S., Perry G., Smith M.A., Fujimoto S. Activation of NADPH oxidase in Alzheimer's disease brains. Biochem Biophys Res Commun 2000, 273:5-9.
65. Simonian N.A., Coyle J.T. Oxidative stress in neurodegenerative diseases. Annu Rev Pharmacol Toxicol 1996, 36:83-106.
66. Smith C.D., Carney J.M., Starke-Reed P.E., Oliver C.N., Stadtman E.R., Floyd R.A., Markesbery W.R. Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc Natl Acad Sci U S A 1991, 88:10540-10543.
67. Smith M.A., Perry G., Richey P.L., Sayre L.M., Anderson V.E., Beal M.F., Kowall N. Oxidative damage in Alzheimer's. Nature 1996, 382:120-121.
68. Song H.Y., Regnier C.H., Kirschning C.J., Goeddel D.V., Rothe M. Tumor necrosis factor (TNF)-mediated kinase cascades: bifurcation of nuclear factor-kappaB and c-jun N-terminal kinase (JNK/SAPK) pathways at TNF receptor-associated factor 2. Proc Natl Acad Sci U S A 1997, 94:9792-9796.
69. Sun G.Y., Horrocks L.A., Farooqui A.A. The roles of NADPH oxidase and phospholipases A2 in oxidative and inflammatory responses in neurodegenerative diseases. J Neurochem 2007, 103:1-16.
70. Trimmer P.A., Schwartz K.M., Borland M.K., De Taboada L., Streeter J., Oron U. Reduced axonal transport in Parkinson's disease cybrid neurites is restored by light therapy. Mol Neurodegener 2009, 4:26.
71. Tuppo E.E., Arias H.R. The role of inflammation in Alzheimer's disease. Int J Biochem Cell Biol 2005, 37:289-305.
72. Viegas V.N., Abreu M.E., Viezzer C., Machado D.C., Filho M.S., Silva D.N., Pagnoncelli R.M. Effect of low-level laser therapy on inflammatory reactions during wound healing: comparison with meloxicam. Photomed Laser Surg 2007, 25:467-473.
73. Wallace M.N., Geddes J.G., Farquhar D.A., Masson M.R. Nitric oxide synthase in reactive astrocytes adjacent to beta-amyloid plaques. Exp Neurol 1997, 144:266-272.
74. Weldon D.T., Maggio J.E., Mantyh P.W. New insights into the neuropathology and cell biology of Alzheimer's disease. Geriatrics 1997, 52(Suppl 2):S13-S16.
75. Whelan H.T., Buchmann E.V., Dhokalia A., Kane M.P., Whelan N.T., Wong-Riley M.T., Eells J.T., Gould L.J., Hammamieh R., Das R., Jett M. Effect of NASA light-emitting diode irradiation on molecular changes for wound healing in diabetic mice. J Clin Laser Med Surg 2003, 21:67-74.
76. Whelan H.T., Smits R.L., Buchman E.V., Whelan N.T., Turner S.G., Margolis D.A., Cevenini V., Stinson H., Ignatius R., Martin T., Cwiklinski J., Philippi A.F., Graf W.R., Hodgson B., Gould L., Kane M., Chen G., Caviness J. Effect of NASA light-emitting diode irradiation on wound healing. J Clin Laser Med Surg 2001, 19:305-314.
77. White J.A., Manelli A.M., Holmberg K.H., Van Eldik L.J., Ladu M.J. Differential effects of oligomeric and fibrillar amyloid-beta 142 on astrocyte-mediated inflammation. Neurobiol Dis 2005, 18:459-465.
78. Wollman Y., Rochkind S. In vitro cellular processes sprouting in cortex microexplants of adult rat brains induced by low power laser irradiation. Neurol Res 1998, 20:470-472.
79. Wong-Riley M.T., Liang H.L., Eells J.T., Chance B., Henry M.M., Buchmann E., Kane M., Whelan H.T. Photobiomodulation directly benefits primary neurons functionally inactivated by toxins: role of cytochrome c oxidase. J Biol Chem 2005, 280:4761-4771.
80. Wyss-Coray T. Inflammation in Alzheimer disease: driving force, bystander or beneficial response?. Nat Med 2006, 12:1005-1015.
81. Yan P., Bero A.W., Cirrito J.R., Xiao Q., Hu X., Wang Y., Gonzales E., Holtzman D.M., Lee J.M. Characterizing the appearance and growth of amyloid plaques in APP/PS1 mice. J Neurosci 2009, 29:10706-10714.
82. Yan S.D., Chen X., Schmidt A.M., Brett J., Godman G., Zou Y.S., Scott C.W., Caputo C., Frappier T., Smith M.A., et al. Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress. Proc Natl Acad Sci U S A 1994, 91:7787-7791.
83. Yin K.J., Cirrito J.R., Yan P., Hu X., Xiao Q., Pan X., Bateman R., Song H., Hsu F.F., Turk J., Xu J., Hsu C.Y., Mills J.C., Holtzman D.M., Lee J.M. Matrix metalloproteinases expressed by astrocytes mediate extracellular amyloid-beta peptide catabolism. J Neurosci 2006, 26:10939-10948.
84. You H.J., Woo C.H., Choi E.Y., Cho S.H., Yoo Y.J., Kim J.H. Roles of Rac and p38 kinase in the activation of cytosolic phospholipase A2 in response to PMA. Biochem J 2005, 388:527-535.
85. Zhang D., Hu X., Qian L., Wilson B., Lee C., Flood P., Langenbach R., Hong J.S. Prostaglandin E2 released from activated microglia enhances astrocyte proliferation in vitro. Toxicol Appl Pharmacol 2009, 238:64-70.
86. Zhu D., Lai Y., Shelat P.B., Hu C., Sun G.Y., Lee J.C. Phospholipases A2 mediate amyloid-beta peptide-induced mitochondrial dysfunction. J Neurosci 2006, 26:11111-11119.
87. Zhu D., Tan K.S., Zhang X., Sun A.Y., Sun G.Y., Lee J.C. Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes. J Cell Sci 2005, 118:3695-3703.
88. Zhu F., Qian C. Berberine chloride can ameliorate the spatial memory impairment and increase the expression of interleukin-1beta and inducible nitric oxide synthase in the rat model of Alzheimer's disease. BMC Neurosci 2006, 7:78.