Independent effects of intra- and extracellular Aβ on learning-related gene expression

American Journal of Pathology

Volumn 175, Issue 1, 2009, Pages 271-282

  Wegenast Braun, Bettina M ^a,b   Maisch, Ana Fulgencio ^a   Eicke, Daniel ^a   Radde, Rebecca ^a   Herzig, Martin C ^a   Staufenbiel, Matthias ^c   Jucker, Mathias ^a   Calhoun, Michael E ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; MESSENGER RNA; SYNAPTOPHYSIN;

AGED; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARC GENE; ARTICLE; BRAIN BLOOD VESSEL; CELL VIABILITY; COGNITION; CONTROLLED STUDY; DENTATE GYRUS; EXPLORATORY BEHAVIOR; GENE; GENE EXPRESSION; LEARNING; MOUSE; NEOCORTEX; NERVE CELL NETWORK; NONHUMAN; PARENCHYMA; PATHOGENESIS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; STAINING; TRANSGENIC MOUSE;

EID: 67650000210     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.090044     Document Type: Article

References (64)

1. Arriagada PV, Growdon JH, Hedley-Whyte ET, Hyman BT: Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 1992, 42:631-639
2. Ingelsson M, Fukumoto H, Newell KL, Growdon JH, Hedley-Whyte ET, Frosch MP, Albert MS, Hyman BT, Irizarry MC: Early Abeta accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology 2004, 62:925-931
3. Tsai J, Grutzendler J, Duff K, Gan WB: Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches. Nat Neurosci 2004, 7:1181-1183
4. Brendza RP, Bacskai BJ, Cirrito JR, Simmons KA, Skoch JM, Klunk WE, Mathis CA, Bales KR, Paul SM, Hyman BT, Holtzman DM: Anti-Abeta antibody treatment promotes the rapid recovery of amyloidassociated neuritic dystrophy in PDAPP transgenic mice. J Clin Invest 2005, 115:428-433
5. Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, Nguyen PT, Bacskai BJ, Hyman BT: Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 2005,25:7278-7287
6. Stern EA, Bacskai BJ, Hickey GA, Attenello FJ, Lombardo JA, Hyman BT: Cortical synaptic integration in vivo is disrupted by amyloid-beta plaques. J Neurosci 2004, 24:4535-4540
7. Humpel C, Marksteiner J: Cerebrovascular damage as a cause for Alzheimer's disease. Curr Neurovasc Res 2005, 2:341-347
8. Jellinger KA: Alzheimer disease and cerebrovascular pathology: an update. J Neural Transm 2002, 109:813-836
9. Attems J, Quass M, Jellinger KA, Lintner F: Topographical distribution of cerebral amyloid angiopathy and its effect on cognitive decline are influenced by Alzheimer disease pathology. J Neurol Sci 2007,257:49-55
10. Vinters HV: Cerebral amyloid angiopathy. A critical review. Stroke 1987, 18:311-324
11. Itoh Y, Yamada M, Hayakawa M, Otomo E, Miyatake T: Cerebral amyloid angiopathy: a significant cause of cerebellar as well as lobar cerebral hemorrhage in the elderly. J Neurol Sci 1993, 116:135-141
12. Winkler DT, Bondolfi L, Herzig MC, Jann L, Calhoun ME, Wiederhold KH, Tolnay M, Staufenbiel M, Jucker M: Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J Neurosci 2001, 21:1619-1627
13. Natte R, Maat-Schieman ML, Haan J, Bornebroek M, Roos RA, van Duinen SG: Dementia in hereditary cerebral hemorrhage with amyloidosis-Dutch type is associated with cerebral amyloid angiopathy but is independent of plaques and neurofibrillary tangles. Ann Neurol 2001, 50:765-772
14. Greenberg SM, Gurol ME, Rosand J, Smith EE: Amyloid angiopathyrelated vascular cognitive impairment. Stroke 2004, 35:2616-2619
15. Thal DR, Ghebremedhin E, Orantes M, Wiestler OD: Vascular pathology in Alzheimer disease: correlation of cerebral amyloid angiopathy and arteriosclerosis/lipohyalinosis with cognitive decline. J Neuropathol Exp Neurol 2003, 62:1287-1301
16. LaFerla FM, Green KN, Oddo S: Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci 2007, 8:499-509
17. Tseng BP, Kitazawa M, LaFerla FM: Amyloid beta-peptide: the inside story. Curr Alzheimer Res 2004, 1:231-239
18. Gouras GK, Tsai J, Naslund J, Vincent B, Edgar M, Checler F, Greenfield JP, Haroutunian V, Buxbaum JD, Xu H, Greengard P, Relkin NR: Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 2000, 156:15-20
19. Mochizuki A, Tamaoka A, Shimohata A, Komatsuzaki Y, Shoji S: Abeta42-positive non-pyramidal neurons around amyloid plaques in Alzheimer's disease. Lancet 2000, 355:42-43
20. Gyure KA, Durham R, Stewart WF, Smialek JE, Troncoso JC: Intraneuronal abeta-amyloid precedes development of amyloid plaques in Down syndrome. Arch Pathol Lab Med 2001, 125:489-492
21. Mori C, Spooner ET, Wisniewsk KE, Wisniewski TM, Yamaguch H, Saido TC, Tolan DR, Selkoe DJ, Lemere CA: Intraneuronal Abeta42 accumulation in Down syndrome brain. Amyloid 2002, 9:88-102
22. Knobloch M, Konietzko U, Krebs DC, Nitsch RM: Intracellular Abeta and cognitive deficits precede beta-amyloid deposition in transgenic arcAbeta mice. Neurobiol Aging 2007, 28:1297-1306
23. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R: 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 2006, 26:10129-10140
24. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM: Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003, 39:409-421
25. Wirths O, Multhaup G, Czech C, Blanchard V, Moussaoui S, Tremp G, Pradier L, Beyreuther K, Bayer TA: Intraneuronal Abeta accumulation precedes plaque formation in beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 2001, 306:116-120
26. Magrane J, Smith RC, Walsh K, Querfurth HW: Heat shock protein 70 participates in the neuroprotective response to intracellularly expressed beta-amyloid in neurons. J Neurosci 2004, 24:1700-1706
27. Zhang Y, McLaughlin R, Goodyer C, LeBlanc A: Selective cytotoxicity of intracellular amyloid beta peptide1-42 through p53 and Bax in cultured primary human neurons. J Cell Biol 2002, 156:519-529
28. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM: Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 2005, 45:675-688
29. Radde R, Bolmont T, Kaeser SA, Coomaraswamy J, Lindau D, Stoltze L, Calhoun ME, Jaggi F, Wolburg H, Gengler S, Haass C, Ghetti B, Czech C, Holscher C, Mathews PM, Jucker M: Abeta42-driven cerebral amyloidosis in transgenic mice reveals early and robust pathology. EMBO Rep 2006, 7:940-946
30. Levy E, Carman MD, Fernandez-Madrid IJ, Power MD, Lieberburg I, van Duinen SG, Bots GT, Luyendijk W, Frangione B: Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage. Dutch type, Science 1990, 248:1124-1126
31. Herzig MC, Winkler DT, Burgermeister P, Pfeifer M, Kohler E, Schmidt SD, Danner S, Abramowski D, Sturchler-Pierrat C, Burki K, van Duinen SG, Maat-Schieman ML, Staufenbiel M, Mathews PM, Jucker M: Abeta is targeted to the vasculature in a mouse model of hereditary cerebral hemorrhage with amyloidosis. Nat Neurosci 2004, 7: 954-960
32. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, Rothacher S, Ledermann B, Burki K, Frey P, Paganetti PA, Waridel C, Calhoun ME, Jucker M, Probst A, Staufenbiel M, Sommer B: Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci USA 1997, 94:13287-13292
33. Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF: Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 1995, 14:433-445
34. Link W, Konietzko U, Kauselmann G, Krug M, Schwanke B, Frey U, Kuhl D: Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci USA 1995, 92:5734-5738
35. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA: Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of longterm potentiation and the consolidation of long-term memory. J Neurosci 2000, 20:3993-4001
36. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A, Mahlke C, Welzl H, Kobalz U, Stawrakakis A, Fernandez E, Waltereit R, Bick-Sander A, Therstappen E, Cooke SF, Blanquet V, Wurst W, Salmen B, Bosl MR, Lipp HP, Grant SG, Bliss TV, Wolfer DP, Kuhl D: Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 2006, 52:437-444
37. Guzowski JF, McNaughton BL, Barnes CA, Worley PF: Environmentspecific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 1999, 2:1120-1124
38. Burke SN, Chawla MK, Penner MR, Crowell BE, Worley PF, Barnes CA, McNaughton BL: Differential encoding of behavior and spatial context in deep and superficial layers of the neocortex. Neuron 2005, 45:667-674
39. Tagawa Y, Kanold PO, Majdan M, Shatz CJ: Multiple periods of functional ocular dominance plasticity in mouse visual cortex. Nat Neurosci 2005, 8:380-388
40. Wang KH, Majewska A, Schummers J, Farley B, Hu C, Sur M, Tonegawa S: In vivo two-photon imaging reveals a role of arc in enhancing orientation specificity in visual cortex. Cell 2006, 126: 389-402
41. Zou Z, Buck LB: Combinatorial effects of odorant mixes in olfactory cortex. Science 2006, 311:1477-1481
42. Shepherd JD, Rumbaugh G, Wu J, Chowdhury S, Plath N, Kuhl D, Huganir RL, Worley PF: Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 2006, 52:475-484
43. Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, Kuhl D, Huganir RL, Worley PF: Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 2006,52:445-459
44. Rial Verde EM, Lee-Osbourne J, Worley PF, Malinow R, Cline HT: Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 2006,52:461-474
45. Blalock EM, Chen KC, Sharrow K, Herman JP, Porter NM, Foster TC, Landfield PW: Gene microarrays in hippocampal aging: statistical profiling identifies novel processes correlated with cognitive impairment. J Neurosci 2003, 23:3807-3819
46. Small SA, Chawla MK, Buonocore M, Rapp PR, Barnes CA: Imaging correlates of brain function in monkeys and rats isolates a hippocampal subregion differentially vulnerable to aging. Proc Natl Acad Sci USA 2004, 101:7181-7186
47. Dickey CA, Loring JF, Montgomery J, Gordon MN, Eastman PS, Morgan D: Selectively reduced expression of synaptic plasticityrelated genes in amyloid precursor protein + presenilin-1 transgenic mice. J Neurosci 2003, 23:5219-5226
48. Dickey CA, Gordon MN, Mason JE, Wilson NJ, Diamond DM, Guzowski JF, Morgan D: Amyloid suppresses induction of genes critical for memory consolidation in APP + PS1 transgenic mice. J Neurochem 2004, 88:434-442
49. Palop JJ, Chin J, Bien-Ly N, Massaro C, Yeung BZ, Yu GQ, Mucke L: Vulnerability of dentate granule cells to disruption of arc expression in human amyloid precursor protein transgenic mice. J Neurosci 2005, 25:9686-9693
50. Andra K, Abramowski D, Duke M, Probst A, Wiederhold KH, Burki K, Goedert M, Sommer B, Staufenbiel M: Expression of APP in transgenic mice: a comparison of neuron-specific promoters. Neurobiol Aging 1996, 17:183-190
51. Gomori G: Microtechnical demonstration of iron. Am J Pathol 1936, 12:655-663
52. Bondolfi L, Calhoun M, Ermini F, Kuhn HG, Wiederhold KH, Walker L, Staufenbiel M, Jucker M: Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice. J Neurosci 2002, 22:515-522
53. Calhoun ME, Wiederhold KH, Abramowski D, Phinney AL, Probst A, Sturchler-Pierrat C, Staufenbiel M, Sommer B, Jucker M: Neuron loss in APP transgenic mice. Nature 1998, 395:755-756
54. West MJ, Slomianka L, Gundersen HJ: Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991, 231: 482-497
55. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ: Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis 1988,96:379-394
56. Calhoun ME, Burgermeister P, Phinney AL, Stalder M, Tolnay M, Wiederhold KH, Abramowski D, Sturchler-Pierrat C, Sommer B, Staufenbiel M, Jucker M: Neuronal overexpression of mutant amyloid precursor protein results in prominent deposition of cerebrovascular amyloid. Proc Natl Acad Sci USA 1999, 96:14088-14093
57. Oddo S, Caccamo A, Tran L, Lambert MP, Glabe CG, Klein WL, LaFerla FM: Temporal profile of amyloid-beta (Abeta) oligomerization in an in vivo model of Alzheimer disease. A link between Abeta and tau pathology. J Biol Chem 2006, 281:1599-1604
58. Chawla MK, Guzowski JF, Ramirez-Amaya V, Lipa P, Hoffman KL, Marriott LK, Worley PF, McNaughton BL, Barnes CA: Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 2005, 15:579-586
59. Wolfer DP, Stagljar-Bozicevic M, Errington ML, Lipp HP: Spatial memory and learning in transgenic mice: fact or artifact? News Physiol Sci 1998, 13:118-123
60. Wahlsten D, Rustay NR, Metten P, Crabbe JC: In search of a better mouse test. Trends Neurosci 2003, 26:132-136
61. Ingram DK, Jucker M: Developing mouse models of aging: a consideration of strain differences in age-related behavioral and neural parameters. Neurobiol Aging 1999, 20:137-145
62. Radde R, Duma C, Goedert M, Jucker M: The value of incomplete mouse models of Alzheimer's disease. Eur J Nucl Med Mol Imaging 2008, 35 Suppl 1:S70-S74
63. Stalder M, Phinney A, Probst A, Sommer B, Staufenbiel M, Jucker M: Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am J Pathol 1999, 154:1673-1684
64. Rolls ET, Kesner RP: A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 2006, 79:1-48