Ultrastructural and behavioural changes precede amyloid deposition in a transgenic model of Alzheimer's disease

Neuroscience

Volumn 122, Issue 1, 2003, Pages 213-228

  Richardson, J C ^a   Kendal, C E ^b   Anderson, R ^a   Priest, F ^a   Gower, E ^a   Soden, P ^a   Gray, R ^a   Topps, S ^a   Howlett, D R ^a   Lavender, D ^a   Clarke, N J ^a   Barnes, J C ^a,c   Haworth, R ^a   Stewart, M G ^b   Rupniak, H T R ^a  

^a GLAXOSMITHKLINE   (United Kingdom)

^b OPEN UNIVERSITY   (United Kingdom)

^c BioWisdom Ltd   (United Kingdom)

Author keywords

Cognition; Dementia; Dystrophic neurites; Electron microscopy

Indexed keywords

AMYLOID PRECURSOR PROTEIN;

AGE DISTRIBUTION; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL ULTRASTRUCTURE; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE MODEL; ELECTRON MICROSCOPY; GENETIC ANALYSIS; HIPPOCAMPUS; HISTOPATHOLOGY; LEARNING DISORDER; LONGITUDINAL STUDY; MAZE TEST; MORPHOMETRICS; MOUSE; NEURITE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; SYNAPSE; TRANSGENIC ANIMAL; WORKING MEMORY;

EID: 10744230072     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00389-0     Document Type: Article

References (61)

1. Adams I. Plasticity of the synaptic contact zone following loss of synapses in the cerebral cortex of ageing humans. Brain Res. 424:1987;343-351.
2. Bach M.E., Hawkins R.D., Osman M., Kandel E.R., Mayford M. Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell. 81:1995;905-915.
3. Benzing W.C., Wujek J.R., Ward E.K., Shaffer D., Ashe K.H., Younkin S., Brunden K.R. Evidence for glial-mediated inflammation in aged APPsw transgenic mice. Neurobiol Aging. 20:1999;581-589.
4. Bertoni-Freddari C., Fattoretti P., Paoloni R., Caselli U., Galeazzi L., Meier-Ruge W. Synaptic structural dynamics and aging. Gerontology. 42:1996;170-180.
5. Bjugn R. The use of the optical disector to estimate the number of neurons, glial and endothelial cells in the spinal cord of the mouse with a comparative note on the rat spinal cord. Brain Res. 627:1993;25-33.
6. Bohbot V.D., Allen J.J., Nadel L. Memory deficits characterized by patterns of lesions to the hippocampus and parahippocampal cortex. Ann NY Acad Sci. 911:2000;355-368.
7. Braak H., Braak E. Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol Aging. 16:1995;271-278.
8. Calhoun M., Wiederhold K., Abramowski D., Phinney A., Probst A., Struchler-Pierrat C., Staufenbiel M., Sommer B., Juker M. Neuron loss in APP transgenic mice. Nature. 395:1998;755-756.
9. Cataldo A.M., Hamilton D.J., Barnett J.L., Paskevich P.A., Nixon R.A. Properties of the endosomal-lysosomal system in the human central nervous system disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease . J Neurosci. 16:1996;186-199.
10. Chapman P.F., White G.L., Jones M.W., Cooper-Blacketer D., Marshall V.J., Irizarry M., Younkin L., Good M.A., Bliss T.V.P., Hyman B.T., Younkin S.G., Hsiao K.K. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci. 2:1999;271-276.
11. Chen G., Chen K.S., Knox J., Inglis J., Bernard A., Martim S.J., Justice A., McConlogue L., Games D., Freedman S.B., Morris R.G.M. A learning deficit related to age and β-amyloid plaques in a mouse model of Alzheimer's disease. Nature. 408:2000;975-979.
12. Cordero M.I., Sandi C. A role for brain glucocorticoid receptors in contextual fear conditioning dependence upon training intensity . Brain Res. 786:1998;11-17.
13. Cummings B.J., Pike C.J., Shankle R., Cotman C.W. Beta-amyloid deposition and other measures of neuropathology predict cognitive status in Alzheimer's disease. Neurobiol Aging. 17:1996;921-933.
14. DeGroot D. A comparison of methods for the estimation of the thickness of ultrathin tissue sections. J Microsc. 151:1988;23-42.
15. Dewachter I., Reverse D., Caluwaerts N., Ris L., Kuiperi C., Van den Haute C., Spittaels K., Umans L., Serneels L., Thiry E., Moechars D., Mercken M., Godaux E., Van Leuven F. Neuronal deficiency of presenilin 1 inhibits amyloid plaque formation and corrects hippocampal long-term potentiation but not a cognitive defect of amyloid precursor protein [V717I] transgenic mice. J Neurosci. 22:2002;3445-3453.
16. Dickson D. The pathogenesis of senile plaques. J Neuropathol Exp Neurol. 56:1997;321-339.
17. Flood D., Buell S., Horwitz G., Coleman P. Dendritic extent in human dentate gyrus granule cells in normal aging and senile dementia. Brain Res. 402:1987;205-216.
18. Frackowiak J., Wisniewski H., Wegiel J., Merz G., Iqbal K., Wang K. Ultrastructure of the microglia that phagocytose amyloid and the microglia that produce β-amyloid fibrils. Acta Neuropathol. 84:1992;225-233.
19. Games D., Adams D., Alessandrini R., Barbour R., Berthelette P., Blackwell C., Carr T., Clements J., Donaldson T., Gillespie F., Guido T., Hagopian S., Johnson-Wood K., Khan K., Lee M., Leibowitz P., Lieberburg I., Little S., Masliah E., McConlogue L., Monotya-Zavala M., Mucke L., Paganini L., Penniman E., Power M., Schenk D., Seubert P., Snyder B., Soriano F., Tan H., Vitale J., Wadsworth S., Wolozin B., Zhao J. Alzheimer's type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature. 373:1995;523-527.
20. Geula C., Wu C.K., Saroff D., Lorenzo A., Yuan M., Yankner B.A. Aging renders the brain vulnerable to amyloid beta-protein neurotoxicity. Nat Med. 4:1998;827-831.
21. Gower A.J., Lamberty Y. The aged mouse as a model of cognitive decline with special emphasis on studies in NMRI mice. Behav Brain Res. 57:1993;163-173.
22. Hardman R., Evans D.J., Fellows L., Hayes B., Rupniak H.T., Barnes J.C., Higgins G.A. Evidence for recovery of spatial learning following entorhinal cortex lesions in mice. Brain Res. 758:1997;187-200.
23. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Aβ elevation and amyloid plaques in transgenic mice. Science. 274:1996;99-102.
24. Hussain I., Powell D., Howlett D., Tew D., Meek T., Chapman C., Gloger I., Murphy K., Southan C., Ryan D., Smith T., Simmons D., Walsh F., Dingwall C., Christie G. Identification of a novel aspartic protease (Asp 2) as β-secretase. Mol Cell Neurosci. 14:1999;419-427.
25. Janus C., Pearson J., LcLaurin J., Matthews P., Jiang Y., Schmidt S.D., Chishti M.A., Horne P., Heslin D., French J., Mount H.T.J., Nixon R.A., Mercken M., Bergeron C., Fraser P.E., St George-Hyslop P., Westaway D. Aβ peptide immunisation reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature. 48:2000;979-982.
26. Irizarry M., McNamara M., Fedorchak K., Hsiao K., Hyman B. APPsw transgenic mice develop age-related Aβ deposits and neuropil abnormalities, but no neuronal loss in CA1. J Neuropathol Exp Neurol. 56:1997;965-973.
27. Kim K.S., Wen G.Y., Bancher C., Chen C.M.J., Sapienza V.J., Hong H., Wisniewski H.M. Detection and quantitation of amyloid beta peptide with two monoclonal antibodies. Neurosci Res Comm. 7:1990;113-122.
28. MacKenzie I., Hao C., Muoz D. Role of microglia in senile plaque formation. Neurobiol Aging. 16:1995;797-804.
29. Maren S., Fanselow M.S. The amygdala and fear conditioning has the nut been cracked? Neuron. 16:1996;16240.
30. Masliah E., Ellisman M., Carragher B., Mallory M., Young S., Hansen L., DeTeresa R., Terry R. Three-dimensional analysis of the relationship between synaptic pathology and neuropil threads in Alzheimer's disease. J Neuropathol Exp Neurol. 51:1992;404-414.
31. Masliah E., Abraham C., Johnson W., Forss-Petter S., Mallory M., Terry R., Mucke L. Synaptic alterations in the cortex of APP transgenic mice. J Neuropathol Exp Neurol. 52:1993;307.
32. Masliah E., Sisk A., Mallory M., Mucke L., Schenk D., Games D. Comparison of neurodegenerative pathology in transgenic mice overexpressing V717F beta-amyloid precursor protein and Alzheimer's disease. J Neurosci. 16:1996;5795-5811.
33. Masliah E., Sisk A., Mallory M., Games D. Neurofibrillary pahtology in transgenic mice overexpressing V717F beta-amyloid precursor protein. J Neuropathol Exp Neurol. 60:2001;357-368.
34. Mayhew T.M. A review of recent advances in stereology for quantifying neural structure. J Neurocytol. 21:1992;313-328.
35. McFarland D.J. Effects of scopolamine, d-amphetamine, and apomorphine on alternation and position biases. Pharmacol Biochem Behav. 32:1989;723-726.
36. Moechars D., Lorent K., DeStrooper B., Dewachter I., Van Leuven F. Expression in brain of amyloid precursor protein mutated in the alpha-secretase site causes disturbed behavior, neuronal degeneration and premature death in transgenic mice. EMBO J. 15:1996;1265-1274.
37. Moechars D., Dewachter I., Lorent K., Reverse D., Baekelandt V., Naidu A., Tesseur I., Spittaels K., Van Den Haute C., Checler F., Godaux E., Cordell B., Van Leuven F. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J Biol Chem. 274:1999;6483-6492.
38. Morgan D., Diamond D.M., Gottschall P.E., Ugens K.E., Dickey C., Hardy J., Duff K., Jantzen P., DiCarlo G., Wilcock D., Connor K., Hatcher J., Hope C., Gordon M., Arendash G.W. Aβ peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature. 408:2000;982-985.
39. Mucke L., Masliah E., Johnson W., Ruppe M., Alford M., Rockenstein E., Forss-Petter S., Pietropaolo M., Mallory M., Abraham C. Synaptotrophic effects of human amyloid β protein precursors in the cortex of transgenic mice. Brain Res. 666:1994;151-167.
40. Mufson E.J., Chen E.Y., Cochran E.J., Beckett L.A., Bennett D.A., Kordower E. Entorhinal cortex and beta-amyloid load in individuals with mild cognitive impairment. Exp Neurol. 158:1999;469-490.
41. Myers C.E., Gluck M.A. Context, conditioning, and hippocampal representation in animal learning. Behav Neurosci. 108:1994;835-847.
42. Naslund J., Haroutunian V., Mohs R., Davis K.L., Greengard P., Buxbaum J.D. Correlation between elevated levels of amyloid β-peptide in the brain and cognitive decline. JAMA. 283:2000;1571-1577.
43. Owen E.H., Logue S.F., Rasmussen D.L., Wehner J.M. Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F-1 hybrids implications of genetic background for single gene mutations and quantitative trait loci analyses . Neuroscience. 80:1997;1087-1099.
44. Pakkenberg B., Gundersen H.J. Neocortical neuron number in humans effect of sex and age . J Comp Neurol. 384:1997;312-320.
45. Phinney A.L., Deller T., Stalder M., Calhoun M.E., Frotscher M., Sommer B., Staufenbiel Jucker M. Cerebral amyloid induces sprouting and ectopic terminal formation in amyloid precursor protein transgenic mice. J Neurosci. 19:1999;8552-8559.
46. Rusakov D.A., Harrison E., Stewart M.G. Synapses in hippocampus occupy only 1-2% of cell membranes and are spaced less than half-micron apart a quantitative ultrastructural analysis with discussion of physiological implications . Neuropharmacology. 37:1998;513-521.
47. Scheff S., DeKosky S., Price D. Quantitative assessment of cortical synaptic density in Alzheimer's disease. Neurobiol Aging. 11:1990;29-37.
48. Scheff S., Price D. Synaptic density in the inner molecular layer of the hippocampal dentate gyrus in Alzheimer's disease. J Neuropathol Exp Neurology. 57:1998;1146-1153.
49. Schenk D., Barbour R., Dunn W., Gordon G., Grajeda H., Guido T., Hu J., Johnson-Wood K., Khan K., Kholodenko D., Lee M., Liao Z., Lieberburg I., Motter R., Mutter L., Soriano F., Shopp G., Vasquez N., Vandevert C., Walker S., Wogulis M., Yednock T., Games D., Seubert P. Immunisation with amyloid-β attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature. 400:1999;173-177.
50. Stein T., Johnson J.A. Lack of neurodegeneration in transgenic mice overexpressing mutant amyloid precursor protein is associated with increased levels of transthyretin and the activation of cell survival pathways. J Neuroscience. 22:2002;7380-7388.
51. Sterio D.C. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc. 34:1984;127-136.
52. Stuart D.A., Oorschot D.E. Embedding, sectioning, immunocytochemical and stereological methods that optimise research on the lesioned adult rat spinal cord. J Neurosci Methods. 61:1995;5-14.
53. Sturchler-Pierrat C., Abramowski D., Duke M., Wiederhold K., Mistl C., Rothacher S., Ledermann B., Burki K., Frey P., Paganetti P., Waridel C., Calhoun M., 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. 94:1997;13287-13292.
54. Su J., Cummings B., Cotman C. Plaque biogenesis in brain aging and Alzheimer's disease II. Progressive transformation and developmental sequence of dystrophic neurites . Acta Neuropathol. 96:1998;463-471.
55. Underwood (1970) Quantiative stereology. Reading, MA: Addison Wesley.
56. Van Dam D., D'Hooge R., Staufenbiel M., Van Ginneken C.V., Van Meir F., De Deyn P.P. Age-dependent cognitive decline in the APP23 model precedes amyloid deposition. Eur J Neurosci. 17:2003;388-396.
57. Vassar R., Bennett B.D., Babu-Khan S., Khan S., Mendiaz E.A., Denis P., Teplow D.B., Ross S., Amarante P., Loeloff R., Luo Y., Fisher S., Fuller J., Edenson S., Lile J., Jarosinski M.A., Biere A.L., Curran E., Burgess T., Louis J., Collins F., Treanor J., Rogers G., Citron M. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science. 286:1999;735-741.
58. Vidal M., Morris R., Grosveld F., Spanopoulou E. Tissue-specific control elements of the Thy-1 gene. EMBO J. 9:1990;833-840.
59. Warburton E.C., Baird A.L., Morgan A., Muir J.L., Aggleton J.P. Disconnecting hippocampal projections to the anterior thalamus produces deficits on tests of spatial memory in rats. Eur J Neurosci. 12:2000;1714-1726.
60. Westerman M.A., Cooper-Blacketer D., Mariash A., Kotilinek L., Kawarabayashi T., Younkin L., Carlsson G., Younkin S.G., Ashe K.H. The relationship between Aβ and memory in the Tg2576 mouse model of Alzheimer's disease. J Neurosci. 22:2002;1858-1867.
61. Winocur G., Rawlins J.N.P., Gray J.A. The hippocampus and conditioning to contextual cues. Behav Neurosci. 5:1987;617-625.