The anti-amnesic effects of luteolin against amyloid β25-35 peptide-induced toxicity in mice involve the protection of neurovascular unit

Neuroscience

Volumn 162, Issue 4, 2009, Pages 1232-1243

  Liu, R ^a,b   Gao, M ^a,b   Qiang, G F ^a,b   Zhang, T T ^a,b   Lan, X ^a,b   Ying, J ^a,b   Du, G H ^a,b  

^a INSTITUTE OF MATERIA MEDICA   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

Author keywords

amyloid peptide; blood brain barrier; luteolin; neurovascular unit

Indexed keywords

ACETYLCHOLINE; ACETYLCHOLINESTERASE; AMYLOID BETA PROTEIN[25-35]; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CLAUDIN 5; LUTEOLIN; OCCLUDIN; PROTEIN ZO1; REACTIVE OXYGEN METABOLITE;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN CORTEX; CEREBROVASCULAR DISEASE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG STRUCTURE; HISTOPATHOLOGY; LEARNING DISORDER; MALE; MAZE TEST; MEMORY DISORDER; MICROVASCULATURE; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPATIAL DISCRIMINATION; TREATMENT DURATION;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CAPILLARIES; CAPILLARY PERMEABILITY; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; LUTEOLIN; MALE; MAZE LEARNING; MEMBRANE PROTEINS; MEMORY; MICE; NOOTROPIC AGENTS; PEPTIDE FRAGMENTS; PHOSPHOPROTEINS; REACTIVE OXYGEN SPECIES; RECEPTOR, TRKB; SPATIAL BEHAVIOR;

EID: 68049102040     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.05.009     Document Type: Article

References (100)

1. Abbott N.J., Ronnback L., and Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7 (2006) 41-53
2. Alderson R.F., Alterman A.L., Barde Y.A., and Lindsay R.M. Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron 5 (1990) 297-306
3. Arancibia S., Lecomte A., Rage F., Silhol M., Aliaga E., and Tapia Arancibia L. In vivo BDNF release and TrkB receptors expression in the supraoptic nucleus after osmotic stress stimulus in rats. Neuroscience 146 (2007) 864-873
4. Arvanitis D.N., Ducatenzeiler A., Ou J.N., Grodstein E., Andrews S.D., Tendulkar S.R., Ribeiro-da-Silva A., Szyf M., and Cuello A.C. High intracellular concentrations of amyloid-beta block nuclear translocation of phosphorylated CREB. J Neurochem 103 (2007) 216-228
5. Auld D.S., Mennicken F., and Quirion R. Nerve growth factor rapidly induces prolonged acetylcholine release from cultured basal forebrain neurons: differentiation between neuromodulatory and neurotrophic influences. J Neurosci 21 (2001) 3375-3382
6. Auld D.S., Kornecook T.J., Bastianetto S., and Quirion R. Alzheimer's disease and the basal forebrain cholinergic system: relations to beta amyloid peptides, cognition, and treatment strategies. Prog Neurobiol 68 (2002) 209-245
7. Beal M.F. Oxidatively modified proteins in aging and disease. Free Radic Biol Med 32 (2002) 797-803
8. Behl C., Davis J., Cole G.M., and Schubert D. Vitamin E protects nerve cells from amyloid b protein toxicity. Biochem Biophys Res Commun 186 (1992) 944-950
9. Bekinschtein P., Cammarota M., Igaz L.M., Bevilaqua L.R., Izquierdo I., and Medina J.H. Persistence of long-term memory storage requires a late protein synthesis- and BDNF-dependent phase in the hippocampus. Neuron 53 (2007) 261-277
10. Berse B., Szczecinska W., Lopez-Coviella I., Madziar B., Zemelko V., Kaminski R., Kozar K., Lips K.S., Pfeil U., and Blusztajn J.K. Expression of high affinity choline transporter during mouse development in vivo and its upregulation by NGF and BMP-4 in vitro. Brain Res Dev Brain Res 157 (2005) 132-140
11. Bibel M., and Barde Y.A. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 14 (2000) 2919-2937
12. Burke S.N., and Barnes C.A. Neural plasticity in the ageing brain. Nat Rev Neurosci 7 (2006) 30-40
13. Cafe C., Torri C., Bertorelli L., Angeretti N., Lucca E., Forloni G., et al. Oxidative stress after acute and chronic application of b-amyloid fragment 25-35 in cortical cultures. Neurosci Lett 203 (1996) 61-65
14. Chao M.V. Neurotrophins and their receptors: a convergence point for many signaling pathways. Nat Rev Neurosci 4 (2003) 299-309
15. Cotman C.W., and Anderson A.J. A potential role for apoptosis in neurodegeneration and Alzheimer's disease. Mol Neurobiol 10 (1995) 19-45
16. Dall'Acqua S., and Innocenti G. Antioxidant compounds from Chaerophyllum hirsutum extracts. Fitoterapia 75 (2004) 592-595
17. De la Torre J.C. Is Alzheimer's disease a neurodegenerative or a vascular disorder?. Data, dogma, and dialectics. Lancet Neurol 3 (2004) 184-190
18. De la Torre J., and Mussivand T. Can disturbed brain microcirculation cause Alzheimer's disease?. Neurol Res 15 (1993) 146-153
19. Dye J.F., Leach L., Clark P., and Firth A. Cyclic AMP and acidic fibroblast growth factor have opposing effects on tight and adherens junctions in microvascular endothelial cells in vitro. Microvasc Res 62 (2001) 94-113
20. Echeverria V., Berman D.E., and Arancio O. Oligomers of beta-amyloid peptide inhibit BDNF-induced arc expression in cultured cortical neurons. Curr Alzheimer Res 4 (2007) 518-521
21. Edvinsson L., MacKenzie E.T., McCulloch J., and Uddman R. Perivascular innervation and receptor mechanisms in cerebrovascular bed. In: Wood J.H. (Ed). Cerebral blood flow. Physiologic and clinical aspects (1987), McGraw-Hill, New York 145-172
22. Eiden L.E. The cholinergic gene locus. J Neurochem 70 (1998) 2227-2240
23. Ellman G.L., Courtney K.D., Andres Jr. V., and Feather-stone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7 (1961) 88-95
24. El-Sherbiny D.A., Khalifa A.E., Attia A.S., and Eldenshary E.-D. Hypericum perforatum extract demonstrates antioxidant properties against elevated rat brain oxidative status induced by amnestic dose of scopolamine. Pharmacol Biochem Behav 76 (2003) 525-533
25. Erme M., Geula C., Ransil B.J., and Mesulam M.M. The acute neurotoxicity and effects upon cholinergic axons or intracerebrally injected b-amyloid in the rat brain. Neurobiol Aging 13 (1992) 553-559
26. Fahnestock M., Garzon D., Holsinger R.M., and Michalski B. Neurotrophic factors and Alzheimer's disease: are we focusing on the wrong molecule?. J Neural Transm Suppl Suppl (2002) 241-252
27. Farkas E., and Luiten P.G. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog Neurobiol 64 (2001) 575-611
28. Finkel T., and Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 408 (2000) 239-247
29. Forloni G., Chiesa R., Smiroldo S., Verga L., Salmona M., Tagliavini F., and Angeretti N. Apoptosis mediated neurotoxicity induced by chronic application of b amyloid fragment 25-35. Neuroreport 4 (1993) 523-526
30. Fox M.A., and Umemori H. Seeking long-term relationship: axon and target communicate to organize synaptic differentiation. J Neurochem 97 (2006) 1215-1231
31. Gloor S.M., Wachtel M., Bolliger M.F., Ishihara H., Landmann R., and Frei K. Molecular and cellular control at the blood-brain barrier. Brain Res Rev 36 (2001) 258-264
32. 2 formation in RAW 264.7 cells. J Nutr 136 (2006) 1517-1521
33. Heldt S.A., Stanek L., Chhatwal J.P., and Ressler K.J. Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 12 (2007) 656-670
34. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 5 (2004) 347-360
35. Ishizaki T., Chiba H., Kojima T., Fujibe M., Soma T., Miyajima H., Nagasawa K., Wada I., and Sawada N. Cyclic AMP induces phosphorylation of claudin-5 immunoprecipitates and expression of claudin-5 gene in blood-brain-barrier endothelial cells via protein kinase A-dependent and -independent pathways. Exp Cell Res 290 (2003) 275-288
36. Kim S.H., Shin K.J., Kim D., Kim Y.H., Han M.S., Lee T.G., Kim E., Ryu S.H., and Suh P.G. Luteolin inhibits the nuclear factor-κB transcriptional activity in Rat-1 fibroblasts. Biochem Pharmacol 66 (2003) 955-963
37. Kotanidou A., Xagorari A., Bagli E., Kitsanta P., Fotsis T., Papapetropoulos A., and Roussos C. Luteolin reduces lipopolysaccharide-induced lethal toxicity and expression of proinflammatory molecules in mice. Am J Respir Crit Care Med 165 (2002) 818-823
38. Kowall N.W., Beal M.F., Busciglio J., Duffy L.K., and Yanker B.A. An in vivo model for the neurodegenerative effects of β-amyloid and protection by substance P. Proc Natl Acad Sci U S A 88 (1991) 7247-7251
39. Kowall N.W., McKee A.C., Yankner B.A., and Beal M.F. In vivo neurotoxicity of β-amyloid β1-40 and the β25-35 fragment. Neurobiol Aging 13 (1992) 537-542
40. Kuppusamy U.R., and Das N.P. Effects of flavonoids on cyclic AMP phosphodiesterase and lipid mobilization in rat adipocytes. Biochem Pharmacol 44 (1992) 1307-1315
41. Laursen S.E., and Belknap J.K. Intracerebroventricular injections in mice. Some methodological refinements. J Pharmacol Methods 16 (1986) 355-357
42. Lewin G.R., and Barde Y.A. Physiology of the neurotrophins. Annu Rev Neurosci 19 (1996) 289-317
43. Lovell M.A., and Markesbery W.R. Amyloid beta peptide, 4-hydroxynonenal and apoptosis. Curr Alzheimer Res 3 (2006) 359-364
44. Mark R.J., Geddes J.W., Uchida K., and Mattson M.P. Amyloid β peptide impairs glucose transport in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J Neurosci 17 (1997) 1646-1654
45. Matsuura T., Fujita H., Seki C., Kashikura K., and Kanno I. Evoked CBF change by somatosensory activation measured by laser-Doppler flowmetry: independent evaluation of RBC velocity and RBC concentration. Jpn J Physiol 49 (1999) 289-296
46. 2+ homeostasis in Alzheimer's disease. Trends Neurosci 16 (1993) 409-414
47. Mattson M.P., Cheng B., Davis D., Bryant K., Lieberburg I., and Rydel R.E. Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12 (1992) 376-389
48. Mattson M.P., and Magnus T. Ageing and neuronal vulnerability. Nat Rev Neurosci 7 (2006) 278-294
49. Maurice T., Lockhart B.P., and Privat A. Amnesia induced in mice by centrally administered β-amyloid peptides involves cholinergic dysfunction. Brain Res 706 (1996) 181-193
50. McAllister A.K., Katz L.C., and Lo D.C. Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22 (1999) 295-318
51. Meunier J., Ieni J., and Maurice T. The anti-amnesic and neuroprotective effects of donepezil against amyloid beta25-35 peptide-induced toxicity in mice involve an interaction with the sigma1 receptor. Br J Pharmacol 149 (2006) 998-1012
52. Morris R.G.M. Developments of a water-maze procedure for studying spatial learning in the rats. J Neurosci Methods 11 (1994) 47-60
53. Murakami Y., Zhao Q., Harada K., Tohda M., Watanabe H., and Matsumoto K. Chotosan, a Kampo formula, improves chronic cerebral hypoperfusion-induced spatial learning deficit via stimulation of muscarinic M1 receptor. Pharmacol Biochem Behav 81 (2005) 616-625
54. Murer M.G., Yan Q., and Raisman-Vozari R. Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog Neurobiol 63 (2001) 71-124
55. Nakagawa Y., Fujimoto N., Matsumoto K., and Cervós-Navarro J. Morphological changes in acute cerebral ischemia after occlusion and reperfusion in the rat. Adv Neurol 52 (1990) 21-27
56. Nonner D., Barrett E.F., and Barrett J.N. Brief exposure to neurotrophins produces a calcium-dependent increase in choline acetyltransferase activity in cultured rat septal neurons. J Neurochem 74 (2000) 988-999
57. Ollivier V., Parry G.C., Cobb R.R., de Prost D., and Mackman N. Elevated cyclic AMP inhibits NF-kappaB-mediated transcription in human monocytic cells and endothelial cells. J Biol Chem 271 (1996) 20828-20835
58. Ouyang S., Sun L.S., Guo S.L., Liu X., and Xu J.P. Effects of timosaponins on learning and memory abilities of rats with dementia induced by lateral cerebral ventricular injection of amyloid beta-peptide. Di Yi Junyi Daxue Xue Bao 25 (2005) 121-126
59. Persidsky Y., Ramirez S.H., Haorah J., and Kanmogne G.D. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 1 (2006) 223-236
60. Pike C.J., Ramezan-Arab N., and Cotman C.W. b-Amyloid neurotoxicity in vitro: evidence of oxidative stress but not protection by antioxidants. J Neurochem 69 (1997) 1601-1611
61. Pike C.J., Walencewicz-Wasserman A.J., Kosmoski J., Cribbs D.H., Glabe C.G., and Cotman C.W. Structure-activity analyses of β-amyloid peptides: contributions of the b25-35 region to aggregation and neurotoxicity. J Neurochem 64 (1995) 253-265
62. Rapôso C., Zago G.M., da Silva G.H., and da Cruz Höfling M.A. Acute blood-brain barrier permeabilization in rats after systemic Phoneutria nigriventer venom. Brain Res 1149 (2007) 18-29
63. Rapp P.R., and Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc Natl Acad Sci U S A 93 (1996) 9926-9930
64. Rasmussen T., Schliemann T., Sorensen J.C., Zimmer J., and West M.J. Memory impaired aged rats: no loss of principal hippocampal and subicular neurons. Neurobiol Aging 17 (1996) 143-147
65. Rastogi L., Godbole M.M., Ray M., Rathore P., Rathore P., Pradhan S., Gupta S.K., and Pandey C.M. Reduction in oxidative stress and cell death explains hypothyroidism induced neuroprotection subsequent to ischemia/reperfusion insult. Exp Neurol 200 (2006) 290-300
66. Rezai-Zadeh K., Shytle R.D., Bai Y., Tian J., Hou H., Mori T., Zeng J., Obregon D., Town T., and Tan J. Flavonoid-mediated presenilin-1 phosphorylation reduces Alzheimer's disease beta-amyloid production. J Cell Mol Med 13 (2009) 574-588
67. Roman G.C., and Kalaria R.N. Vascular determinants of cholinergic deficits in Alzheimer disease and vascular dementia. Neurobiol Aging 27 (2006) 1769-1785
68. Salehi A., Delcroix J.D., and Mobley W.C. Traffic at the intersection of neurotrophic factor signaling and neurodegeneration. Trends Neurosci 26 (2003) 73-80
69. Saragovi H.U. Progression of age-associated cognitive impairment correlates with quantitative and qualitative loss of TrkA receptor protein in nucleus basalis and cortex. J Neurochem 95 (2005) 1472-1480
70. Sato A., Sato Y., and Uchida S. Regulation of cerebral cortical blood flow by the basal forebrain cholinergic fibers and aging. Auton Neurosci 96 (2002) 13-19
71. Scheibel A.B., Duong T.H., and Jacobs R. Alzheimer's disease as a capillary dementia. Ann Med 21 (1989) 103-107
72. Selkoe D.J. The molecular pathology of Alzheimer's disease. Neuron 6 (1991) 487-498
73. Selkoe D.J. Alzheimer's disease: a central role for amyloid. J Neuropathol Exp Neurol 53 (1994) 438-447
74. Selkoe D.J. Aging, amyloid, and Alzheimer's disease: a perspective in honor of Carl Cotman. Neurochem Res 28 (2003) 1705-1713
75. Sheikov N., McDannold N., Sharma S., and Hynynen K. Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium. Ultrasound Med Biol 34 (2008) 1093-1104
76. Simard M., and Nedergaard M. The neurobiology of glia in the context of water and ion homeostasis. Neuroscience 129 (2004) 877-896
77. Smith D.E., Rapp P.R., McKay H.M., Roberts J.A., and Tuszynski M.H. Memory impairment in aged primates is associated with focal death of cortical neurons and atrophy of subcortical neurons. J Neurosci 24 (2004) 4373-4381
78. Snyder E.M., Nong Y., Almeida C.G., Paul S., Moran T., Choi E.Y., Nairn A.C., Salter M.W., Lombroso P.J., Gouras G.K., and Greengard P. Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci 8 (2005) 1051-1058
79. Song L., Che W., Min-Wei W., Murakami Y., and Matsumoto K. Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacol Biochem Behav 83 (2006) 186-193
80. Stein-Behrens B., Adams K., Yeh M., and Sapolsky R. Failure of beta-amyloid protein fragment 25-35 to cause hippocampal damage in the rat. Neurobiol Aging 13 (1992) 577-579
81. Steinmeier R., Bondar I., Bauhuf C., and Fahlbusch R. Laser Doppler flowmetry mapping of cerebrocortical microflow: characteristics and limitations. Neuroimage 15 (2002) 107-119
82. Stepanichev M.Y., Lazareva N.A., Onufriev M.V., Mitrokhina O.S., Moiseeva Y.V., and Gulyaeva N.V. Effects of doses of fragment (25-35) of β-amyloid peptide on behavior in rats. Neurosci Behav Physiol 28 (1998) 564-566
83. Stepanichev M.Y., Zdobnova I.M., Zarubenko I.I., Moiseeva Y.V., Lazareva N.A., Onufriev M.V., and Gulyaeva N.V. Amyloid-beta (25-35)-induced memory impairments correlate with cell loss in rat hippocampus. Physiol Behav 80 (2004) 647-655
84. Tanaka J., Horiike Y., Matsuzaki M., Miyazaki T., Ellis-Davies G.C., and Kasai H. Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319 (2008) 1683-1687
85. Tannenbaum B.M., Tannenbaum G.S., and Anisman H. Impact of life-long macronutrient choice on neuroendocrine and cognitive functioning in aged mice: differential effects in stressor-reactive and stressor-resilient mouse strains. Brain Res 985 (2003) 187-197
86. Teng F.Y., and Tang B.L. Axonal regeneration in adult CNS neurons-signaling molecules and pathways. J Neurochem 96 (2006) 1501-1508
87. Thoenen H. Neurotrophins and neuronal plasticity. Science 270 (1995) 593-598
88. Tong L., Balazs R., Thornton P.L., and Cotman C.W. Beta-amyloid peptide at sublethal concentrations downregulates brain-derived neurotrophic factor functions in cultured cortical neurons. J Neurosci 24 (2004) 6799-6809
89. Tsai F.S., Peng W.H., Wang W.H., Wu C.R., Hsieh C.C., Lin Y.T., Feng I.C., and Hsieh M.T. Effects of luteolin on learning acquisition in rats: involvement of the central cholinergic system. Life Sci 80 (2007) 1692-1698
90. Tuszynski M.H., Thal L., Pay M., Salmon D.P., U H.S., Bakay R., Patel P., Blesch A., Vahlsing H.L., Ho G., Tong G., Potkin S.G., Fallon J., Hansen L., Mufson E.J., Kordower J.H., Gall C., and Conner J. A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat Med 11 (2005) 551-555
91. Tyler W.J., Alonso M., Bramham C.R., and Pozzo-Miller L.D. From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn Mem 9 (2002) 224-237
92. Wang D.C., Chen S.S., Lee Y.C., and Chen T.J. Amyloid-[beta] at sublethal level impairs BDNF-induced arc expression in cortical neurons. Neurosci Lett 398 (2006) 78-82
93. West M.J., Kawas C.H., Stewart W.F., Rudow G.L., and Troncoso J.C. Hippocampal neurons in pre-clinical Alzheimer's disease. Neurobiol Aging 25 (2004) 1205-1212
94. Whitehouse P.J. Paying attention to acetylcholine: the key to wisdom and quality of life?. Prog Brain Res 145 (2004) 311-317
95. Wilcock D.M., Vitek M.P., and Colton C.A. Vascular amyloid alters astrocytic water and potassium channels in mouse models and humans with Alzheimer's disease. Neuroscience 159 (2009) 1055-1069
96. Wolburg H., and Lippoldt A. Tight junctions of the blood-brain barrier: development, composition and regulation. Vasc Pharmacol 38 (2002) 323-337
97. Xagorari A., Papapetropoulos A., Mauromatis A., Economou M., Fotsis T., and Roussos C. Luteolin inhibits an endotoxin-stimulated phosphorylation cascade and proinflammatory cytokine production in macrophages. J Pharmacol Exp Ther 296 (2001) 181-187
98. Yatin S.M., Varadarajan S., Link C.D., and Butterfield D.A. In vitro and in vivo oxidative stress associated with Alzheimer's amyloid β peptide (1-42). Neurobiol Aging 20 (1999) 325-330
99. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57 (2008) 178-201
100. Zonta M., Angulo M.C., Gobbo S., Rosengarten B., Hossmann K.A., Pozzan T., and Carmignoto G. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6 (2003) 43-50