Time-course and regional analyses of the physiopathological changes induced after cerebral injection of an amyloid β fragment in rats

American Journal of Pathology

Volumn 179, Issue 1, 2011, Pages 315-334

  Zussy, Charleine ^a   Brureau, Anthony ^a   Delair, Brice ^a   Marchal, Stephane ^a   Keller, Emeline ^a   Ixart, Guy ^b   Naert, Gaelle ^a   Meunier, Johann ^b   Chevallier, Nathalie ^a   Maurice, Tangui ^a   Givalois, Laurent ^a,c  

^a University of Montpellier   (France)

^b UNIV MONTPELLIER   (France)

^c PSL RESEARCH UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[25-35]; CONGO RED;

ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN CORTEX; CELL STRESS; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENCEPHALITIS; HIPPOCAMPUS; INFRARED SPECTROSCOPY; LONG TERM MEMORY; MEMORY DISORDER; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; SHORT TERM MEMORY; STAINING;

ACETYLCHOLINE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; CEREBRAL CORTEX; HUMANS; INFLAMMATION; MALE; MEMORY, LONG-TERM; NEUROFIBRILLARY TANGLES; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 80052466179     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.03.021     Document Type: Article

References (82)

1. D.J. Selkoe Translating cell biology into therapeutic advances in Alzheimer's disease Nature 399 6738 Suppl 1999 A23 A31
2. B.A. Yankner Mechanisms of neuronal degeneration in Alzheimer's disease Neuron 16 1996 921 932
3. D.J. Selkoe Alzheimer's disease: genes, proteins, and therapy Physiol Rev 81 2001 741 766
4. C.J. Pike, B.J. Cummings, and C.W. Cotman Beta-amyloid induces neuritic dystrophy in vitro: similarities with Alzheimer pathology Neuroreport 3 1992 769 772
5. C.J. Pike, A.J. Walencewicz-Wasserman, J. Kosmoski, D.H. Cribbs, C.G. Glabe, and C.W. Cotman Structure-activity analyses of beta-amyloid peptides: contributions of the beta 2535 region to aggregation and neurotoxicity J Neurochem 64 1995 253 265
6. C. Behl, J.B. Davis, F.G. Klier, and D. Schubert Amyloid beta peptide induces necrosis rather than apoptosis Brain Res 645 1994 253 264
7. K.J. Ivins, P.L. Thornton, T.T. Rohn, and C.W. Cotman Neuronal apoptosis induced by beta-amyloid is mediated by caspase-8 Neurobiol Dis 6 1999 440 449
8. B.A. Yankner, L.K. Duffy, and D.A. Kirschner Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides Science 250 1990 279 282
9. M.Y. Stepanichev, I.M. Zdobnova, A.A. Yakovlev, M.V. Onufriev, N.A. Lazareva, I.I. Zarubenko, and N.V. Gulyaeva Effects of tumor necrosis factor-alpha central administration on hippocampal damage in rat induced by amyloid beta-peptide (2535) J Neurosci Res 71 2003 110 120
10. M.Y. Stepanichev, I.M. Zdobnova, I.I. Zarubenko, N.A. Lazareva, and N.V. Gulyaeva Studies of the effects of central administration of beta-amyloid peptide (2535): pathomorphological changes in the hippocampus and impairment of spatial memory Neurosci Behav Physiol 36 2006 101 106
11. V. Villard, J. Espallergues, E. Keller, T. Alkam, A. Nitta, K. Yamada, T. Nabeshima, A. Vamvakides, and T. Maurice Antiamnesic and neuroprotective effects of the aminotetrahydrofuran derivative ANAVEX1-41 against amyloid beta(2535)-induced toxicity in mice Neuropsychopharmacology 34 2009 1552 1566
12. J. Meunier, J. Ieni, and T. Maurice 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
13. M.Y. Stepanichev, I.M. Zdobnova, I.I. Zarubenko, Y.V. Moiseeva, N.A. Lazareva, M.V. Onufriev, and N.V. Gulyaeva Amyloid-beta(2535)-induced memory impairments correlate with cell loss in rat hippocampus Physiol Behav 80 2004 647 655
14. M.A. Gruden, T.B. Davidova, M. Malisauskas, R.D.E. Sewell, N.I. Voskresenskaya, K. Wilhelm, E.I. Elistratova, V.V. Sherstnev, and L.A. Morozova-Roche Differential neuroimmune markers to the onset of Alzheimer's disease neurodegeneration and dementia: autoantibodies to Abeta((2535)) oligomers, S100b and neurotransmitters J Neuroimmunol 186 2007 181 192
15. T. Kubo, S. Nishimura, Y. Kumagae, and I. Kaneko In vivo conversion of racemized beta-amyloid ([D-Ser 26]A beta 140) to truncated and toxic fragments ([D-Ser 26]A beta 2535/40) and fragment presence in the brains of Alzheimer's patients J Neurosci Res 70 2002 474 483
16. B. Klementiev, T. Novikova, V. Novitskaya, P.S. Walmod, O. Dmytriyeva, B. Pakkenberg, V. Berezin, and E. Bock A neural cell adhesion molecule-derived peptide reduces neuropathological signs and cognitive impairment induced by Abeta25-35 Neuroscience 145 2007 209 224
17. F. Chavant, J. Deguil, S. Pain, I. Ingrand, S. Milin, B. Fauconneau, M.C. Perault-Pochat, and C. Lafay-Chebassier Imipramine, in part through tumor necrosis factor inhibition, prevents cognitive decline and -amyloid accumulation in a mouse model of Alzheimer's Disease J Pharmacol Exp Ther 332 2010 505 514
18. T. Maurice, B.P. Lockhart, T.P. Su, and A. Privat Amnesia induced in mice by centrally administered beta-amyloid peptides involves cholinergic dysfunction Brain Res 706 1996 181 193
19. E.M. Sigurdsson, H. Scholtzova, P.D. Mehta, B. Frangione, and T. Wisniewski Immunization with a nontoxic/nonfibrillar amyloid-beta homologous peptide reduces Alzheimer's disease-associated pathology in transgenic mice Am J Pathol 159 2001 439 447
20. S. Marchal, E. Shehi, M.C. Harricane, P. Fusi, F. Heitz, P. Tortora, and R. Lange Structural instability and fibrillary aggregation of non-expanded human Ataxin-3 revealed under high pressure and temperature J Biol Chem 278 2003 31554 31563
21. S. Delobette, A. Privat, and T. Maurice In vitro aggregation facilitates beta-amyloid peptide-(2535)-induced amnesia in the rat Eur J Pharmacol 319 1997 1 4
22. G. Paxinos, and C. Watson The rat brain in stereotaxic coordinates The compact 3rd edition 1997 Academic Press San Diego, CA
23. G. Naert, G. Ixart, L. Tapia-Arancibia, and L. Givalois Continuous i.c.v. infusion of brain-derived neurotrophic factor modifies hypothalamic-pituitary- adrenal axis activity, locomotor activity and body temperature rhythms in adult male rats Neuroscience 139 2006 779 789
24. J. Meunier, M. Gue, M. Récasens, and T. Maurice Attenuation by a sigma1 (sigma1) receptor agonist of the learning and memory deficits induced by a prenatal restraint stress in juvenile rats Br J Pharmacol 142 2004 689 700
25. L. Givalois, G. Naert, F. Rage, G. Ixart, S. Arancibia, and L. Tapia-Arancibia A single brain-derived neurotrophic factor injection modifies hypothalamo-pituitary-adrenocortical axis activity in adult male rats Mol Cell Neurosci 27 2004 280 295
26. M. Hermes-Lima, W.G. Willmore, and K.B. Storey Quantification of lipid peroxidation in tissue extracts based on Fe(III)xylenol orange complex formation Free Radic Biol Med 19 1995 271 280
27. T. Cotrufo, A. Viegi, N. Berardi, Y. Bozzi, L. Mascia, and L. Maffei Effects of neurotrophins on synaptic protein expression in the visual cortex of dark-reared rats J Neurosci 23 2003 3566 3571
28. L. Givalois, S. Arancibia, G. Alonso, and L. Tapia-Arancibia Expression of BDNF and its receptors in the median eminence cells with sensitivity to stress Endocrinology 135 2004 4737 4747
29. K.J. Halverson, I. Sucholeiki, T.T. Ashburn, and P.T. Lansbury Location of beta-sheet-forming sequences in amyloid proteins by FTIR J Am Chem Soc 113 1991 6701 6703
30. K. Janek, J. Behlke, J. Zipper, H. Fabian, Y. Georgalis, M. Beyermann, M. Bienert, and E. Krause Water-soluble beta-sheet models which self-assemble into fibrillar structures Biochemistry 38 1999 8246 8252
31. W.K. Surewicz, H.H. Mantsch, and D. Chapman Determination of protein secondary structure by Fourier transform infra-red spectroscopy: a critical assessment Biochemistry 32 1993 389 394
32. I. Kaneko, K. Morimoto, and T. Kubo Drastic neuronal loss in vivo by beta-amyloid racemized at Ser(26) residue: conversion of non-toxic [D-Ser(26)]beta-amyloid 140 to toxic and proteinase-resistant fragments Neuroscience 104 2001 1003 1011
33. W.J. Streit, S.A. Walter, and N.A. Pennel Reactive microgliosis Prog Neurobiol 57 1999 563 581
34. J.J. Hagan, J.H. Jansen, and C.L. Broekkamp Selective behavioural impairment after acute intoxication with trimethyltin (TMT) in rats Neurotoxicology 9 1988 53 74
35. T. Nabeshima, A. Katoh, H. Ishimaru, Y. Yoneda, K. Ogita, K. Murase, H. Ohtsuka, K. Inari, T. Fukuta, and T. Kameyama Carbon monoxide-induced delayed amnesia, delayed neuronal death and change in acetylcholine concentration in mice J Pharmacol Exp Ther 256 1991 378 384
36. J.M. Ordy, G.J. Thomas, B.T. Volpe, W.P. Dunlap, and P.M. Colombo An animal model of human-type memory loss based on aging, lesion, forebrain ischemia, and drug studies with the rat Neurobiol Aging 9 1988 667 683
37. K. Blennow, M.J. de Leon, and H. Zetterberg Alzheimer's disease Lancet 368 2006 387 403
38. R. Jakob-Roetne, and H. Jacobsen Alzheimer's disease: from pathology to therapeutic approaches Angew Chem Int Ed Engl 48 2009 3030 3059
39. Y. Yamaguchi, and S. Kawashima Effects of amyloid-beta-(2535) on passive avoidance, radial-arm maze learning and choline acetyltransferase activity in the rat Eur J Pharmacol 412 2001 265 272
40. T. Alkam, A. Nitta, H. Mizoguchi, A. Itoh, R. Murai, T. Nagai, K. Yamada, and T. Nabeshima The extensive nitration of neurofilament light chain in the hippocampus is associated with the cognitive impairment induced by amyloid beta in mice J Pharmacol Exp Ther 327 2008 137 147
41. J.W. Allen, B.A. Eldadah, and A.I. Faden Beta-amyloid-induced apoptosis of cerebellar granule cells and cortical neurons: exacerbation by selective inhibition of group I metabotropic glutamate receptors Neuropharmacology 38 1999 1243 1252
42. C.S. Casley, J.M. Land, M.A. Sharpe, J.B. Clark, M.R. Duchen, and L. Canevari Beta-amyloid fragment 2535 causes mitochondrial dysfunction in primary cortical neurons Neurobiol Dis 10 2002 258 267
43. D.C. Lu, S. Soriano, D.E. Bredesen, and E.H. Koo Caspase cleavage of the amyloid precursor protein modulates amyloid beta-protein toxicity J Neurochem 87 2003 733 741
44. M.P. Mattson, J. Partin, and J.G. Begley Amyloid beta-peptide induces apoptosis-related events in synapses and dendrites Brain Res 807 1998 167 176
45. V.A. Movsesyan, B.A. Stoica, and A.I. Faden MGLuR5 activation reduces beta-amyloid-induced cell death in primary neuronal cultures and attenuates translocation of cytochrome c and apoptosis-inducing factor J Neurochem 89 2004 1528 1536
46. W. Wei, D.D. Norton, X. Wang, and J.W. Kusiak Abeta17-42 in Alzheimer's disease activates JNK and caspase-8 leading to neuronal apoptosis Brain 125 2002 2036 2043
47. X.Z. Yan, J.T. Qiao, Y. Dou, and Z.D. Qiao Beta-amyloid peptide fragment 3135 induces apoptosis in cultured cortical neurons Neuroscience 92 1999 177 184
48. E.T. Sutton, G.R. Hellermann, and T. Thomas Beta-amyloid-induced endothelial necrosis and inhibition of nitric oxide production Exp Cell Res 230 1997 368 376
49. C. Geci, J. How, H. Alturaihi, and U. Kumar Beta-amyloid increases somatostatin expression in cultured cortical neurons J Neurochem 101 2007 664 673
50. L. Tong, R. Balazs, P.L. Thornton, and C.W. Cotman Beta-amyloid peptide at sublethal concentrations downregulates brain-derived neurotrophic factor functions in cultured cortical neurons J Neurosci 24 2004 6799 6809
51. Y. Tang, K. Yamada, Y. Kanou, T. Miyazaki, X. Xiong, F. Kambe, Y. Murata, H. Seo, and T. Nabeshima Spatiotemporal expression of BDNF in the hippocampus induced by the continuous intracerebroventricular infusion of beta-amyloid in rats Mol Brain Res 80 2000 188 197
52. H.J. Krugers, J.M. Koolhaas, B. Bohus, and J. Korf A single social stress-experience alters glutamate receptor-binding in rat hippocampal CA3 area Neurosci Lett 154 1993 73 77
53. M.T. Lowy, L. Gault, and B.K. Yamamoto Adrenalectomy attenuates stress-induced elevations in extracellular glutamate concentrations in the hippocampus J Neurochem 61 1993 1957 1960
54. B.S. McEwen Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators Eur J Pharmacol 583 2008 174 185
55. C. Catania, I. Sotiropoulos, R. Silva, C. Onofri, K.C. Breen, N. Sousa, and O.F. Almeida The amyloidogenic potential and behavioral correlates of stress Mol Psychiatry 14 2009 95 105
56. I. Abrahám, T. Harkany, K.M. Horvath, A.H. Veenema, B. Penke, C. Nyakas, and P.G. Luiten Chronic corticosterone administration dose-dependently modulates Abeta(142)- and NMDA-induced neurodegeneration in rat magnocellular nucleus basalis J Neuroendocrinol 12 2000 486 494
57. Y. Goodman, A.J. Bruce, B. Cheng, and M.P. Mattson Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons J Neurochem 66 1996 1836 1844
58. G. Naert, G. Ixart, T. Maurice, L. Tapia-Arancibia, and L. Givalois Brain-derived neurotrophic factor and hypothalamic-pituitary-adrenal axis adaptation processes in a depressive-like state induced by chronic restraint stress Mol Cell Neurosci 46 2011 55 66
59. K.L. Davis, B.M. Davis, B.S. Greenwald, R.C. Mohs, A.A. Mathé, C.A. Johns, and T.B. Horvath Cortisol and Alzheimer's disease I: basal studies Am J Psychiatry 143 1986 300 305
60. F. Masugi, T. Ogihara, K. Sakaguchi, A. Otsuka, Y. Tsuchiya, S. Morimoto, Y. Kumahara, S. Saeki, and M. Nishide High plasma levels of cortisol in patients with senile dementia of the Alzheimer's type Methods Find Exp Clin Pharmacol 11 1989 707 710
61. G.L. Ming, and H. Song Adult neurogenesis in the mammalian central nervous system Annu Rev Neurosci 28 2005 223 250
62. P. Taupin Neurogenesis in the adult central nervous system C R Biol 329 2006 465 475
63. Y. Chen, and C. Dong Abeta40 promotes neuronal cell fate in neural progenitor cells Cell Death Differ 16 2009 386 394
64. M.A. López-Toledano, and M.L. Shelanski Neurogenic effect of beta-amyloid peptide in the development of neural stem cells J Neurosci 24 2004 5439 5444
65. B. Mazur-Kolecka, A. Golabek, K. Nowicki, M. Flory, and J. Frackowiak Amyloid-beta impairs development of neuronal progenitor cells by oxidative mechanisms Neurobiol Aging 27 2006 1181 1192
66. O. von Bohlen Und Halbach Immunohistological markers for staging neurogenesis in adult hippocampus Cell Tissue Res 329 2007 409 420
67. L. Tapia-Arancibia, F. Rage, L. Givalois, and S. Arancibia Physiology of BDNF: focus on hypothalamic function Front Neuroendocrinol 25 2004 77 107
68. L. Givalois, F. Marmigre, F. Rage, G. Ixart, S. Arancibia, and L. Tapia-Arancibia Immobilization stress rapidly and differentially modulates BDNF and TrkB mRNA expression in the pituitary gland of adult male rats Neuroendocrinology 74 2001 148 159
69. F. Marmigre, L. Givalois, F. Rage, S. Arancibia, and L. Tapia-Arancibia Rapid induction of BDNF expression in the hippocampus during immobilization stress challenge in adult rats Hippocampus 13 2003 646 655
70. D.R. Thal, U.M. Rb, M.M. Orantes, and H.M. Braak Phases of Abeta-deposition in the human brain and its relevance for the development of Alzheimer's disease Neurology 58 2002 1791 1800
71. J.A. Van de Nes, W. Kamphorst, R. Ravid, and D.F. Swaab Comparison of beta-protein/a4 deposits and Alz-50-stained cytoskeletal changes in the hypothalamus and adjoining areas of Alzheimer's disease patients: amorphic plaques and cytoskeletal changes occur independently Acta Neuropathol 96 1998 129 138
72. J.A. Van de Nes, S. Konermann, R. Nafe, and D. Swaab Beta-protein/a4 deposits are not associated with hyperphosphorylated Tau in somatostatin neurons in the hypothalamus of Alzheimer's disease patients Acta Neuropathol 111 2006 126 138
73. D.G. Standaert, V.M. Lee, B.D. Greenberg, D.E. Lowery, and J.Q. Trojanowski Molecular features of hypothalamic plaques in Alzheimer's disease Am J Pathol 139 1991 681 691
74. S. Arancibia, M. Silhol, F. Moulire, J. Meffre, I. Höllinger, T. Maurice, and L. Tapia-Arancibia Protective effect of BDNF against beta-amyloid induced neurotoxicity in vitro and in vivo in rats Neurobiol Dis 31 2008 316 326
75. F. Duclot, J. Meffre, C. Jacquet, C. Gong ora, and T. Maurice Mice knock out for the histone acetyltransferase p300/CREB binding protein-associated factor develop a resistance to amyloid toxicity Neuroscience 167 2010 850 863
76. E. Kojro, R. Postina, C. Buro, C. Meiringer, K. Gehrig-Burger, and F. Fahrenholz The neuropeptide PACAP promotes the alpha-secretase pathway for processing the Alzheimer amyloid precursor protein FASEB J 20 2006 512 514
77. S. Bourgault, D. Vaudry, A. Dejda, N.D. Doan, H. Vaudry, and A. Fournier Pituitary adenylate cyclase-activating polypeptide: focus on structure-activity relationships of a neuroprotective peptide Curr Med Chem 16 2009 4462 4480
78. S. Weill-Engerer, J.P. David, V. Sazdovitch, P. Liere, B. Eychenne, A. Pianos, M. Schumacher, A. Delacourte, E.E. Baulieu, and Y. Akwa Neurosteroid quantification in human brain regions: comparison between Alzheimer's and nondemented patients J Clin Endocrinol Metab 87 2002 5138 5143
79. D. Watson, E. Castano, T.A. Kokjohn, Y.M. Kuo, Y. Lyubchenko, D. Pinskyz, E.S. Connolly, C. Esh, D.C. Luehrs, W.B. Stine, L.M. Rowse, M.R. Emmerling, and A.E. Roher Physicochemical characteristics of soluble oligomeric Abeta and their pathologic role in Alzheimer's disease Neurol Res 27 2005 869 881
80. S.T. Ferreira, M.N. Vieira, and F.G. De Felice Soluble protein oligomers as emerging toxins in Alzheimer's and other amyloid diseases IUBMB Life 59 2007 332 345
81. D.M. Walsh, and D.J. Selkoe A beta oligomersa decade of discovery J Neurochem 101 2007 1172 1184
82. L. Millucci, L. Ghezzi, G. Bernardini, and A. Santucci Conformations and biological activities of amyloid beta peptide 2535 Curr Protein Pept Sci 11 2010 54 67