Accumulation of beta-amyloid in the brain microvessels accompanies increased hyperphosphorylated tau proteins following microsphere embolism in aged rats

Neuroscience

Volumn 153, Issue 2, 2008, Pages 414-427

  Han, F ^a   Ali Raie, A ^a   Shioda, N ^a   Qin, Z H ^b   Fukunaga, K ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

Author keywords

Alzheimer's disease; beta amyloid; eNOS; microvascular; peroxynitrite; tau

Indexed keywords

AMYLOID BETA PROTEIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MICROSPHERE; PEROXYNITRITE; TAU PROTEIN;

AGED; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL INJURY; BRAIN ISCHEMIA; CONTROLLED STUDY; ELECTROPHORESIS; EMBOLISM; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MICROVASCULATURE; NERVE DEGENERATION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RAT; WESTERN BLOTTING;

EID: 42749083998     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.02.044     Document Type: Article

References (58)

1. S.A. Bennett Cleavage of amyloid precursor protein elicited by chronic cerebral hypoperfusion Neurobiol Aging 21 2000 207 214
2. M.M. Breteler Vascular risk factors for Alzheimer's disease: an epidemiologic perspective Neurobiol Aging 21 2000 153 160
3. J. Brownlees N.G. Irving J.P. Brion B.J. Gibb U. Wagner C.C. Woodgett J Miller Tau phosphorylation in transgenic mice expressing glycogen synthase kinase-3beta transgenes Neuroreport 8 1997 3251 3255
4. L. Coeroli S. Renolleau S. Arnaud D. Plotkine N. Cachin M. Plotkine Y. Ben-Ari C. Charriaut-Marlangue Nitric oxide production and perivascular tyrosine nitration following focal ischemia in neonatal rat J Neurochem 70 1998 2516 2525
5. L. Dallaire L. Tremblay R. Béliveau Purification and characterization of metabolically active capillaries of the blood-brain barrier Biochem J 276 1991 745 752
6. G.I. De Jong E. Farkas C.M. Stienstra J.R. Plass J.N. Keijser J.C. de la Torre P.G. Luiten Cerebral hypoperfusion yields capillary damage in the hippocampal CA1 area that correlates with spatial memory impairment Neuroscience 91 1999 203 210
7. J.C. de la Torre Alzheimer disease as a vascular disorder: nosological evidence Stroke 33 2002 1152 1162
8. J.C. de la Torre B.A. Pappas V. Prevot M.R. Emmerling K. Mantione T. Fortin M.D. Watson G.B. Stefano Hippocampal nitric oxide upregulation precedes memory loss and A beta 1-40 accumulation after chronic brain hypoperfusion in rats Neurol Res 25 2003 635 641
9. J.C. de la Torre How do heart disease and stroke become risk factors for Alzheimer's disease? Neurol Res 28 2006 637 644
10. N. Demura K. Mizukawa N. Ogawa K. Yamashita I. Kanazawa A cerebral ischemia model produced by injection of microspheres via the external carotid artery in freely moving rats Neurosci Res 17 1993 23 30
11. J. Drake C.D. Link D.A. Butterfield Oxidative stress precedes fibrillar deposition of Alzheimer's disease amyloid beta-peptide (1-42) in a transgenic Caenorhabditis elegans model Neurobiol Aging 24 2003 415 420
12. P.B. Eisenhauer R.J. Johnson J.M. Wells T.A. Davies R.E. Fine Toxicity of various amyloid beta peptide species in cultured human blood-brain barrier endothelial cells: increased toxicity of dutch-type mutant J Neurosci Res 6 2000 804 810
13. T. Engel F. Hernandez J. Avila J.J. Lucas Full reversal of Alzheimer's disease-like phenotype in a mouse model with conditional overexpression of glycogen synthase kinase-3 J Neurosci 26 2006 5083 5090
14. E. Farkas P.G. Luiten Cerebral microvascular pathology in aging and Alzheimer's disease Prog Neurobiol 64 2001 575 611
15. 2+ and calmodulin-dependent protein kinase from rat brain J Neurochem 391 1982 1607 1617
16. K. Fukunaga H. Sato K. Takatsu A. Tominaga E. Miyamoto Monoclonal antibody against a multifunctional calmodulin-dependent protein kinase from rat brain and the tissue distribution of the enzyme Biomed Res 7 1986 405 413
17. K. Fukunaga E. Miyamoto A working model of CaM kinase II activity in hippocampal long-term potentiation and memory Neurosci Res 38 2000 3 17
18. V. Galvan S. Chen D. Lu A. Logvinova P. Goldsmith E.H. Koo D.E. Bredesen Caspase cleavage of members of the amyloid precursor family of proteins J Neurochem 82 2002 283 294
19. F.G. Gervais D. Xu G.S. Robertson J.P. Vaillancourt Y. Zhu J. Huang A. LeBlanc D. Smith M. Rigby M.S. Shearman E.E. Clarke H. Zheng L.H. Van Der Ploeg S.C. Ruffolo N.A. Thornberry S. Xanthoudakis R.J. Zamboni S. Roy D.W. Nicholson Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation Cell 97 1999 395 406
20. G.G. Glenner C.W. Wong Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein Biochem Biophys Res Commun 16 1984 885 890
21. M. Goedert R. Jakes R.A. Crowther J. Six U. Lubke M. Vandermeeren P. Cras J.Q. Trojanowski V.M. Lee The abnormal phosphorylation of tau protein at Ser-202 in Alzheimer disease recapitulates phosphorylation during development Proc Natl Acad Sci U S A 90 1993 5066 5070
22. J. Götz F. Chen J. van Dorpe R.M. Nitsch Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils Science 293 2001 1491 1495
23. F. Han Y. Shirasaki K. Fukunaga 3-[2-[4-(3-Chloro-2-methylphenylmethyl)-1-piperazinyl]ethyl]-5,6-dimethoxy-1-(4-imidazolylmethyl)-1H-indazole dihydro-chloride 3.5 hydrate (DY-9760e) is neuroprotective in rat microsphere embolism: role of the cross-talk between calpain and caspase-3 through calpastatin J Pharmacol Exp Ther 317 2006 529 536
24. F. Han Y. Shirasaki K. Fukunaga Microsphere embolism-induced endothelial nitric oxide synthase expression mediates disruption of the blood-brain barrier in rat brain J Neurochem 99 2006 97 106
25. A. Hashiguchi T. Kawano S. Yano M. Morioka J. Hamada T. Sato Y. Shirasaki Y. Ushio K. Fukunaga The neuroprotective effect of a novel calmodulin antagonist, 3-[2-[4-(3-chloro-2-methylphenyl)-1-piperazinyl]ethyl]-5,6-dimethoxy-1-(4-imidazolylmethyl)-1H-indazole dihydrochloride 3.5 hydrate, in transient forebrain ischemia Neuroscience 121 2003 379 386
26. H. Hayashi K. Sato Y. Kuruhara S. Takeo Microsphere embolism-induced changes in noradrenaline release in the cerebral cortex in rats Brain Res 783 1998 241 248
27. K. Ishiguro K. Sato M. Takamatsu J. Park T. Uchida K. Imahori Analysis of phosphorylation of tau with antibodies specific for phosphorylation sites Neurosci Lett 202 1995 81 84
28. D. Janigro G.A. West T.S. Nguyen H.R. Winn Regulation of blood-brain barrier endothelial cells by nitric oxide Circ Res 75 1994 528 538
29. K.A. Jellinger J. Attems Prevalence and pathogenic role of cerebrovascular lesions in Alzheimer disease J Neurol Sci 229–230 2005 37 41
30. R.N. Kalaria The role of cerebral ischemia in Alzheimer's disease Neurobiol Aging 21 2000 21 30
31. S. Kumar-Singh D. Pirici E. McGowan S. Serneels C. Ceuterick J. Hardy K. Duff D. Dickson C. Van Broeckhoven Dense-core plaques in Tg2576 and PSAPP mouse models of Alzheimer's disease are centered on vessel walls Am J Pathol 167 2005 527 543
32. U.K. Laemmli Cleavage of structure proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
33. J.M. Litersky G.V. Johnson R. Jakes M. Goedert M. Lee P. Seubert Tau protein is phosphorylated by cyclic AMP-dependent protein kinase and calcium/calmodulin-dependent protein kinase II within its microtubule-binding domains at Ser-262 and Ser-356 Biochem J 316 1996 655 660
34. S. Lovestone C.H. Reynolds D. Latimer Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells Curr Biol 4 1994 1077 1086
35. J.J. Lucas F. Hernández P. Gómez-Ramos M.A. Morán R. Hen J. Avila Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice EMBO J 20 2001 27 39
36. H.J. Luth G. Munch T. Arendt Aberrant expression of NOS isoforms in Alzheimer's disease is structurally related to nitrotyrosine formation Brain Res 953 2002 135 143
37. R.J. Mark E.M. Blanc M.P. Mattson Amyloid beta-peptide and oxidative cellular injury in Alzheimer's disease Mol Neurobiol 12 1996 211 224
38. H. Masaoka I. Klatzo S. Tomida K. Vass H.G. Wagner T.S. Nowak Jr Role of circulatory disturbances in the development of post-ischemic brain edema Neurochem Pathol 9 1988 21 29
39. W.G. Mayhan S.P. Didion Glutamate-induced disruption of the blood-brain barrier in rats Role of nitric oxide Stroke 27 1996 965 970
40. J. Miklossy Cerebral hypoperfusion induces cortical watershed microinfarcts which may further aggravate cognitive decline in Alzheimer's disease Neurol Res 25 2003 605 610
41. S. Nagahiro M. Uno K. Sato S. Goto M. Morioka Y. Ushio Pathophysiology and treatment of cerebral ischemia J Med Invest 45 1998 57 70
42. A. Nunomura G. Perry G. Aliev Oxidative damage is the earliest event in Alzheimer disease J Neuropathol Exp Neurol 60 2001 759 767
43. A. Nunomura G. Perry M.A. Pappolla R.P. Friedland K. Hirai S. Chiba M.A. Smith Neuronal oxidative stress precedes amyloid-beta deposition in Down syndrome J Neuropathol Exp Neurol 59 2000 1011 1017
44. R. Pluta A.S. Lossinsky H.M. Wiśniewski M.J. Mossakowski Early blood-brain barrier changes in the rat following transient complete cerebral ischemia induced by cardiac arrest Brain Res 633 1994 41 52
45. A. Popa-Wagner E. Schröder L.C. Walker C. Kessler beta-Amyloid precursor protein and ss-amyloid peptide immunoreactivity in the rat brain after middle cerebral artery occlusion: effect of age Stroke 29 1998 2196 2202
46. D. Praticò K. Uryu S. Leight J.Q. Trojanoswki V.M. Lee Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis J Neurosci 21 2001 4183 4187
47. J. Rodrigo P. Fernandez-Vizarra S. Castro-Blanco M.L. Bentura M. Nieto T. Gomez-Isla R. Martinez-Murillo A. MartInez J. Serrano A.P. Fernandez Nitric oxide in the cerebral cortex of amyloid-precursor protein (SW) Tg2576 transgenic mice Neuroscience 128 2004 73 89
48. P.S. Russell C.M. Chase R.B. Colvin Accelerated atheromatous lesions in mouse hearts transplanted to apolipoprotein-E-deficient recipients Am J Pathol 49 1996 91 99
49. T. Sasaki F. Han N. Shioda S. Moriguchi J. Kasahara K. Ishiguro K. Fukunaga Lithium-induced activation of Akt and CaM kinase II contributes to its neuroprotective action in a rat microsphere embolism model Brain Res 1108 2006 98 106
50. T. Shirakura F. Han N. Shiota S. Moriguchi J. Kasahara T. Sato Y. Shirasaki K. Fukunaga Inhibition of nitric oxide production and protein tyrosine nitration contribute to neuroprotection by a novel calmodulin antagonist, DY-9760e, in the rat microsphere embolism Biol Pharm Bull 28 2005 1658 1661
51. N.A. Simonian T. Elvhage A.J. Czernik P. Greengard B.T. Hyman Calcium/calmodulin-dependent protein kinase II immunostaining is preserved in Alzheimer's disease hippocampal neurons Brain Res 657 1994 294 299
52. J.H. Su G. Deng C.W. Cotman Neuronal DNA damage precedes tangle formation and is associated with up-regulation of nitrotyrosine in Alzheimer's disease brain Brain Res 774 1997 193 199
53. X. Sun G. He H. Qing W. Zhou F. Dobie F. Cai M. Staufenbiel L.E. Huang W. Song Hypoxia facilitates Alzheimer's disease pathogenesis by up-regulating BACE1 gene expression Proc Natl Acad Sci U S A 103 2006 18727 18732
54. S. Takeo T. Taguchi K. Tanonaka K. Miyake T. Horiguchi N. Takagi K. Fujimori Sustained damage to energy metabolism of brain regions after microsphere embolism in rats Stroke 23 1992 62 68
55. K.H. Tan S. Harrington W.M. Purcell R.D. Hurst Peroxynitrite mediates nitric oxide-induced blood-brain barrier damage Neurochem Res 29 2004 579 587
56. D. Zekry C. Duyckaerts J. Belmin C. Geoffre R. Moulias J.J. Hauw Alzheimer's disease and brain infarcts in the elderly Agreement with neuropathology J Neurol 249 2002 1529 1534
57. M. Zhao J. Su E. Head C.W. Cotman Accumulation of caspase cleaved amyloid precursor protein represents an early neurodegenerative event in aging and in Alzheimer's disease Neurobiol Dis 14 2003 391 403
58. C. Zhu X. Wang L. Qiu C. Peeters-Scholte H. Hagberg K. Blomgren Nitrosylation precedes caspase-3 activation and translocation of apoptosis-inducing factor in neonatal rat cerebral hypoxia-ischaemia J Neurochem 90 2004 462 471