Extracellular amyloid-β and cytotoxic glial activation induce significant entorhinal neuron loss in young PS1M146L/APP751SL mice

Journal of Alzheimer's Disease

Volumn 18, Issue 4, 2009, Pages 755-776

  Moreno Gonzalez, Ines ^a,d   Baglietto Vargas, David ^a,d   Sanchez Varo, Raquel ^a,d   Jimenez, Sebastian ^b,d,e   Trujillo Estrada, Laura ^a,d   Sanchez Mejias, Elisabeth ^a,d   Del Rio, Juan Carlos ^b   Torres, Manuel ^b,d,e   Romero Acebal, Manuel ^c,d   Ruano, Diego ^b,d,e   Vizuete, Marisa ^b,d,e   Vitorica, Javier ^b,d,e   Gutierrez, Antonia ^a,d  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c HOSPITAL UNIVERSITARIO VIRGEN DE LA VICTORIA   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^e HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

Author keywords

Alzheimer's disease; Amyloid; Entorhinal cortex; Microglia; Neurodegeneration; Neuroinflammation; Transgenic

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; COMPLEMENTARY DNA; PRESENILIN 1; RNA;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; CYTOTOXICITY; DEGENERATIVE DISEASE; ENTORHINAL CORTEX; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LASER CAPTURE MICRODISSECTION; MICROGLIA; MOUSE; NERVE CELL NECROSIS; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

EID: 74949114810     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2009-1192     Document Type: Article

References (74)

1. Braak H, Braak E (1997) Diagnostic criteria for neuropathologic assessment of Alzheimer's disease. Neurobiol Aging 18, S85-S88.
2. Gomez-Isla T, Price JL, McKeel DW, Jr., Morris JC, Growdon JH, Hyman BT (1996) Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci 16, 4491-4500.
3. Canto CB, Wouterlood FG, Witter MP (2008) What does the anatomical organization of the entorhinal cortex tell us? Neural Plast 2008, 381243.
4. Chrobak JJ, Amaral DG (2007) Entorhinal cortex of the monkey: VII. intrinsic connections. J Comp Neurol 500, 612-633.
5. Insausti R, Amaral DG (2008) Entorhinal cortex of the monkey: IV. Topographical and laminar organization of cortical afferents. J Comp Neurol 509, 608-641.
6. Toledo-Morrell L, Stoub TR, Bulgakova M, Wilson RS, Bennett DA, Leurgans S, Wuu J, Turner DA (2004) MRI-derived entorhinal volume is a good predictor of conversion from MCI to AD. Neurobiol Aging 25, 1197-1203.
7. Stoub TR, Toledo-Morrell L, Stebbins GT, Leurgans S, Bennett DA, Shah RC (2006) Hippocampal disconnection contributes to memory dysfunction in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci U S A 103, 10041-10045.
8. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82, 239-259.
9. Price JL, Ko AI,Wade MJ, Tsou SK, McKeel DW, Morris JC (2001) Neuron number in the entorhinal cortex and CA1 in preclinical Alzheimer disease. Arch Neurol 58, 1395-1402.
10. Ramos B, Baglietto-Vargas D, Del Rio JC, Moreno-Gonzalez I, Santa-Maria C, Jimenez S, Caballero C, Lopez-Tellez JF, Khan ZU, Ruano D, Gutierrez A, Vitorica J (2006) Early neuropathology of somatostatin/NPY GABAergic cells in the hippocampus of a PS1xAPP transgenic model of Alzheimer's disease. Neurobiol Aging 27, 1658-1672.
11. Blanchard V, Moussaoui S, Czech C, Touchet N, Bonici B, Planche M, Canton T, Jedidi I, Gohin M,Wirths O, Bayer TA, Langui D, Duyckaerts C, Tremp G, Pradier L (2003) Time sequence of maturation of dystrophic neurites associated with Abeta deposits in APP/PS1 transgenic mice. Exp Neurol 184, 247-263.
12. Caballero C, Jimenez S, Moreno-Gonzalez I, Baglietto-Vargas D, Sanchez-Varo R, Gavilan MP, Ramos B, Del Rio JC, Vizuete M, Gutierrez A, Ruano D, Vitorica J (2007) Interindividual variability in the expression of the mutated form of hPS1M146L determined the production of Abeta peptides in the PS1xAPP transgenic mice. J Neurosci Res 85, 787-797.
13. Schmitz C, Rutten BP, Pielen A, Schafer S, Wirths O, Tremp G, Czech C, Blanchard V, Multhaup G, Rezaie P, Korr H, Steinbusch HW, Pradier L, Bayer TA (2004) Hippocampal neuron loss exceeds amyloid plaque load in a transgenic mouse model of Alzheimer's disease. Am J Pathol 164, 1495-1502.
14. Jimenez S, Baglietto-Vargas D, Caballero C, Moreno-Gonzalez I, Torres M, Sanchez-Varo R, Ruano D, Vizuete M, Gutierrez A, Vitorica J (2008) Inflammatory response in the hippocampus of PS1M146L/APP751SL mouse model of Alzheimer's disease: age-dependent switch in the microglial phenotype from alternative to classic. J Neurosci 28, 11650-11661.
15. Colton CA, Mott RT, Sharpe H, Xu Q, Van Nostrand WE, Vitek MP (2006) Expression profiles for macrophage alternative activation genes in AD and in mouse models of AD. J Neuroinflammation 3, 27.
16. van GT (2001) Entorhinal cortex of the mouse: cytoarchitectonical organization. Hippocampus 11, 397-407.
17. Insausti R, Herrero MT, Witter MP (1997) Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7, 146-183.
18. Franklin K.B.J:Paxinos G (2008) The mouse brain in stereotaxic coordinates, Academic Press.
19. Ruano D, Lambolez B, Rossier J, PaternainAV, Lerma J (1995) Kainate receptor subunits expressed in single cultured hippocampal neurons: molecular and functional variants by RNA editing. Neuron 14, 1009-1017.
20. Gundersen HJ, Jensen EB, Kieu K, Nielsen J (1999) The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193, 199-211.
21. Vincent SR, Johansson O, Hokfelt T, Meyerson B, Sachs C, Elde RP, Terenius L, Kimmel J (1982) Neuropeptide coexistence in human cortical neurones. Nature 298, 65-67.
22. Hendry SH, Jones EG, Emson PC (1984) Morphology, distribution, and synaptic relations of somatostatin-and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex. J Neurosci 4, 2497-2517.
23. Chronwall BM, Chase TN, O'Donohue TL (1984) Coexistence of neuropeptide Y and somatostatin in rat and human cortical and rat hypothalamic neurons. Neurosci Lett 52, 213-217.
24. Chan-Palay V (1987) Somatostatin immunoreactive neurons in the human hippocampus and cortex shown by immunogold/ silver intensification on vibratome sections: coexistence with neuropeptide Y neurons, and effects in Alzheimer-type dementia. J Comp Neurol 260, 201-223.
25. Papadopoulos GC, Parnavelas JG, Cavanagh ME (1987) Extensive co-existence of neuropeptides in the rat visual cortex. Brain Res 420, 95-99.
26. Miyoshi G, Butt SJ, Takebayashi H, Fishell G (2007) Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J Neurosci 27, 7786-7798.
27. Casas C, Sergeant N, Itier JM, Blanchard V, Wirths O, van der KN, Vingtdeux V, van de SE, Ret G, Canton T, Drobecq H, Clark A, Bonici B, Delacourte A, Benavides J, Schmitz C, Tremp G, Bayer TA, Benoit P, Pradier L (2004) Massive CA1/2 neuronal loss with intraneuronal and N-terminal truncated Abeta42 accumulation in a novel Alzheimer transgenic model. Am J Pathol 165, 1289-1300.
28. Christensen DZ, Kraus SL, Flohr A, Cotel MC, Wirths O, Bayer TA (2008) Transient intraneuronal Abeta rather than extracellular plaque pathology correlates with neuron loss in the frontal cortex of APP/PS1KI mice. Acta Neuropathol 116, 647-655.
29. Laferla FM, Green KN, Oddo S (2007) Intracellular amyloidbeta in Alzheimer's disease. Nat Rev Neurosci 8, 499-509.
30. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van EL, Berry R, Vassar R (2006) Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci 26, 10129-10140.
31. Thal DR, Rub U, Schultz C, Sassin I, Ghebremedhin E, Del TK, Braak E, Braak H (2000) Sequence of Abeta-protein deposition in the human medial temporal lobe. J Neuropathol Exp Neurol 59, 733-748.
32. Thal DR, Rub U, Orantes M, Braak H (2002) Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 58, 1791-1800.
33. Bryan KJ, Zhu X, Harris PL, Perry G, Castellani RJ, Smith MA, Casadesus G (2008) Expression of CD74 is increased in neurofibrillary tangles in Alzheimer's disease. Mol Neurodegener 3, 13.
34. Edwards MM, Robinson SR (2006) TNF alpha affects the expression of GFAP and S100B: implications for Alzheimer's disease. J Neural Transm 113, 1709-1715.
35. Davies P, Katzman R, Terry RD (1980) Reduced somatostatinlike immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementa. Nature 288, 279-280.
36. Rossor MN, Emson PC, Mountjoy CQ, Roth M, Iversen LL (1980) Reduced amounts of immunoreactive somatostatin in the temporal cortex in senile dementia of Alzheimer type. Neurosci Lett 20, 373-377.
37. Arai H, Moroji T, Kosaka K (1984) Somatostatin and vasoactive intestinal polypeptide in postmortem brains from patients with Alzheimer-type dementia. Neurosci Lett 52, 73-78. (Pubitemid 15179728)
38. Beal MF, Mazurek MF, Svendsen CN, Bird ED, Martin JB (1986) Widespread reduction of somatostatin-like immunoreactivity in the cerebral cortex in Alzheimer's disease. Ann Neurol 20, 489-495.
39. Beal MF, Mazurek MF, Chattha GK, Svendsen CN, Bird ED, Martin JB (1986) Neuropeptide Y immunoreactivity is reduced in cerebral cortex in Alzheimer's disease. Ann Neurol 20, 282-288.
40. Reinikainen KJ, Riekkinen PJ, Jolkkonen J, Kosma VM, Soininen H (1987) Decreased somatostatin-like immunoreactivity in cerebral cortex and cerebrospinal fluid in Alzheimer's disease. Brain Res 402, 103-108. (Pubitemid 17006934)
41. Grouselle D, Winsky-Sommerer R, David JP, Delacourte A, Dournaud P, Epelbaum J (1998) Loss of somatostatin-like immunoreactivity in the frontal cortex of Alzheimer patients carrying the apolipoprotein epsilon 4 allele. Neurosci Lett 255, 21-24.
42. Davis KL, Mohs RC, Marin DB, Purohit DP, Perl DP, Lantz M, Austin G, Haroutunian V (1999) Neuropeptide abnormalities in patients with early Alzheimer disease. Arch Gen Psychiatry 56, 981-987. (Pubitemid 29526380)
43. Morrison JH, Rogers J, Scherr S, Benoit R, Bloom FE (1985) Somatostatin immunoreactivity in neuritic plaques of Alzheimer's patients. Nature 314, 90-92.
44. Beal MF, Benoit R, Mazurek MF, Bird ED, Martin JB (1986) Somatostatin-28(1-12)-like immunoreactivity is reduced in Alzheimer's disease cerebral cortex. Brain Res 368, 380-383.
45. Nakamura S, Vincent SR (1986) Somatostatin-and neuropeptide Y-immunoreactive neurons in the neocortex in senile dementia of Alzheimer's type. Brain Res 370, 11-20.
46. Gaspar P, Duyckaerts C, Febvret A, Benoit R, Beck B, Berger B (1989) Subpopulations of somatostatin 28-immunoreactive neurons display different vulnerability in senile dementia of the Alzheimer type. Brain Res 490, 1-13.
47. Kumar U (2005) Expression of somatostatin receptor subtypes (SSTR1-5) in Alzheimer's disease brain: an immunohistochemical analysis. Neuroscience 134, 525-538.
48. Kordower JH, Chu Y, Stebbins GT, DeKosky ST, Cochran EJ, Bennett D, Mufson EJ (2001) Loss and atrophy of layer II entorhinal cortex neurons in elderly peoplewith mild cognitive impairment. Ann Neurol 49, 202-213.
49. Li M, Chen L, Lee DH, Yu LC, Zhang Y (2007) The role of intracellular amyloid beta in Alzheimer's disease. Prog Neurobiol 83, 131-139.
50. Castellani RJ, Zhu X, Lee HG, Moreira PI, Perry G, SmithMA (2007) Neuropathology and treatment of Alzheimer disease: did we lose the forest for the trees? Expert Rev Neurother 7, 473-485.
51. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, Laferla FM (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39, 409-421.
52. Billings LM, Oddo S, Green KN, McGaugh JL, Laferla FM (2005) Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45, 675-688.
53. Bayer TA, Wirths O (2008) [Alzheimer's disease: Molecular pathology, animal models, and current treatment.]. Nervenarzt 79 (Suppl 3), 117-125.
54. Masliah E, Sisk A, Mallory M, Mucke L, Schenk D, Games D (1996) Comparison of neurodegenerative pathology in transgenic mice overexpressingV717F beta-amyloid precursor protein and Alzheimer's disease. J Neurosci 16, 5795-5811.
55. Wirths O, Multhaup G, Czech C, Blanchard V, Moussaoui S, Tremp G, Pradier L, Beyreuther K, Bayer TA (2001) Intraneuronal Abeta accumulation precedes plaque formation in betaamyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 306, 116-120.
56. Liu Y, Yoo MJ, Savonenko A, Stirling W, Price DL, Borchelt DR, Mamounas L, Lyons WE, Blue ME, Lee MK (2008) Amyloid pathology is associated with progressive monoaminergic neurodegeneration in a transgenic mouse model of Alzheimer's disease. J Neurosci 28, 13805-13814.
57. El Khoury J, Luster AD (2008) Mechanisms of microglia accumulation in Alzheimer's disease: therapeutic implications. Trends Pharmacol Sci 29, 626-632.
58. F arfara D, Lifshitz V, Frenkel D (2008) Neuroprotective and neurotoxic properties of glial cells in the pathogenesis of Alzheimer's disease. J Cell Mol Med 12, 762-780.
59. Zhu X, Su B, Wang X, Smith MA, Perry G (2007) Causes of oxidative stress in Alzheimer disease. Cell Mol Life Sci 64, 2202-2210. (Pubitemid 47347959)
60. McGeer PL, McGeer EG (2007) NSAIDs and Alzheimer disease: epidemiological, animal model and clinical studies. Neurobiol Aging 28, 639-647.
61. Aisen PS (2008) The inflammatory hypothesis of Alzheimer disease: dead or alive? Alzheimer Dis Assoc Disord 22, 4-5.
62. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95, 6448-6453.
63. De Felice FG, Vieira MN, Saraiva LM, Figueroa-Villar JD, Garcia-Abreu J, Liu R, Chang L, Klein WL, Ferreira ST (2004) Targeting the neurotoxic species in Alzheimer's disease: inhibitors of Abeta oligomerization. FASEB J 18, 1366-1372.
64. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid betapeptide. Nat Rev Mol Cell Biol 8, 101-112.
65. Martins IC, Kuperstein I, Wilkinson H, Maes E, Vanbrabant M, Jonckheere W, Van GP, Hartmann D, D'Hooge R, De SB, Schymkowitz J, Rousseau F (2008) Lipids revert inert Abeta amyloid fibrils to neurotoxic protofibrils that affect learning in mice. EMBO J 27, 224-233.
66. Apelt J, Schliebs R (2001) Beta-amyloid-induced glial expression of both pro-and anti-inflammatory cytokines in cerebral cortex of aged transgenic Tg2576 mice with Alzheimer plaque pathology. Brain Res 894, 21-30.
67. Chao CC, Hu S, Sheng WS, Bu D, Bukrinsky MI, Peterson PK (1996) Cytokine-stimulated astrocytes damage human neurons via a nitric oxide mechanism. Glia 16, 276-284.
68. Craft JM, Watterson DM, Van Eldik LJ (2006) Human amyloid beta-induced neuroinflammation is an early event in neurodegeneration. Glia 53, 484-490.
69. Hu J, Akama KT, Krafft GA, Chromy BA,Van Eldik LJ (1998) Amyloid-beta peptide activates cultured astrocytes: morphological alterations, cytokine induction and nitric oxide release. Brain Res 785, 195-206.
70. Itagaki S, McGeer PL, Akiyama H, Zhu S, Selkoe D (1989) Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J Neuroimmunol 24, 173-182.
71. Johnstone M, Gearing AJ, Miller KM (1999) A central role for astrocytes in the inflammatory response to beta-amyloid; chemokines, cytokines and reactive oxygen species are produced. J Neuroimmunol 93, 182-193.
72. Mrak RE, Griffin WS (2005) Glia and their cytokines in progression of neurodegeneration. Neurobiol Aging 26, 349-354.
73. Ralay RH, Craft JM, Hu W, Guo L, Wing LK, Van Eldik LJ, Watterson DM (2006) Glia as a therapeutic target: selective suppression of human amyloid-beta-induced upregulation of brain proinflammatory cytokine production attenuates neurodegeneration. J Neurosci 26, 662-670.
74. Zipp F, Aktas O (2006) The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases. Trends Neurosci 29, 518-527.