Mechanisms of neuronal degeneration in Alzheimer's disease

Neuron

Volumn 16, Issue 5, 1996, Pages 921-932

  Yankner, Bruce A ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E; CHOLESTEROL; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL MODEL; APOPTOSIS; CHOLESTEROL TRANSPORT; DEMENTIA; GENETIC SUSCEPTIBILITY; HUMAN; NERVE CELL DEGENERATION; NEUROFIBRILLARY TANGLE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SENILE PLAQUE; SYNAPTOGENESIS; TRANSGENIC MOUSE;

EID: 0029896354     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80115-4     Document Type: Review

References (179)

1. Alonso, A. del C., Zaidi, T., Grundke-Iqbal, I., and Iqbal, K. (1994). Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease. Proc. Natl. Acad. Sci. USA 91, 5562-5566.
2. Alzheimer, A. (1907). Uber eine eigenartige Erkrangkung der Hirnrinde. All. Z. Psychiatr. 64, 146-148.
3. Alzheimer's Disease Collaborative Group (1995). The structure of the presenilin 1 (S182) gene and Identification of six novel mutations in early onset AD families. Nature Genet. 11, 219-222.
4. Arai, H., Lee, V.M.-Y., Otvos, L., Jr., Greenberg, B.D., Lowery, D.E., Sharma, S.K., Schmidt, M.L., and Trojanowski, J.Q. (1990). Defined neurofilament, τ, and β-amyloid precursor protein epitopes distinguish Alzheimer from non-Alzheimer senile plaques. Proc. Natl. Acad. Sci. USA 87, 2249-2253.
5. Arispe, N., Pollard, H.B., and Rojas, E. (1993). Giant multilevel cation channels formed by Alzheimer disease amyloid β-protein [AβP-(1-40)] in bilayer membrane. Proc. Natl. Acad. Sci. USA 90, 10573-10577.
6. Barrow, C.J., and Zagorski, M.G. (1991). Solution structures of β peptide and its constituent fragments: relation to amyloid desposition. Science 253, 179-182.
7. Bartus, R.T., Dean, R.L., Beer, B., and Lippa, A.S. (1982). The cholinergic hypothesis of geriatric memory dysfunction. Science 217, 408-414.
8. Behl, C., Davis, J.B., Lesley, R., and Schubert, D. (1994). Hydrogen peroxide mediates amyloid β protein toxicity. Cell 77, 817-827.
9. 262 strongly reduces binding of tau to microtubules: distinction between PHF-like immunoreactivity and microtubule binding. Neuron 11, 153-163.
10. Blass, J.P. (1993). Pathophysiology of the Alzheimer syndrome. Neurology 43, 525-538.
11. 396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10, 1089-1099.
12. Breen, K.C., Bruce, M., and Anderton, B.H. (1991). β-Amyloid precursor protein mediates neuronal cell-cell and cell-surface adhesion. J. Neurosci. Res. 28, 90-100.
13. Breitner, J.C.S., Gau, B.A., Welsh, K.A., Plassman, B.L., McDonald, W.M., Helms, M.J., and Anthony, J.C. (1992). Inverse association of anti-inflammatory treatments and Alzheimer's disease: initial results of a co-twin control study. Neurology 44, 227-232.
14. Brown, R.H. (1995). Amyotrophic lateral sclerosis: recent insights from genetics and transgenic mice. Cell 80, 687-692.
15. Busciglio, J., and Yankner, B.A. (1995). Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro. Nature 378, 776-779.
16. Busciglio, J., Lorenzo, A., and Yankner, B.A. (1992). Methodological variables in the assessment of β amyloid neurotoxicity. Neurobiol. Aging 13, 609-612.
17. Busciglio, J., Gabuzda, D.H., Matsudaira, P., and Yankner, B.A. (1993a). Generation of β-amyloid in the secretory pathway in neuronal and non-neuronal cells. Proc. Natl. Acad. Sci. USA 90, 2092-2096.
18. Busciglio, J., Yeh, J., and Yankner, B.A. (1993b). β-Amyloid neurotoxicity in human cortical culture is not mediated by excitotoxins. J. Neurochem. 61, 1565-1568.
19. Busciglio, J., Lorenzo, A., Yeh, J., and Yankner, B.A. (1995). β-Amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14, 879-888.
20. Bush, A.I., Pettingell, W.H., Multhaup, G., d. Paradis, M., Vonsattel, J.-P., Gusella, J.F., Beyreuther, K., Masters, C.L., and Tanzi, R.E. (1994). Rapid induction of Alzheimer Aβ amyloid formation by zinc. Science 265, 1464-1467.
21. Cai, X.-D., Golde, T.E., and Younkin, G.S. (1993). Release of excess amyloid β protein from a mutant amyloid β protein precursor. Science 259, 514-516.
22. Cataldo, A.M., Barnett, J.L., Berman, S.A., Li, J., Quarless, S., Bursztajn, S., Lippa, C., and Nixon, R.A. (1995). Gene expression and cellular content of cathepsin D in Alzheimer's disease brain: evidence for early up-regulation of the endosomal-lysosomal system. Neuron 14, 671-680.
23. Caughey, B., and Race, R.E. (1992). Potent inhibition of scrapie-associated PrP accumulation by Congo red. J. Neurochem. 59, 768-771.
24. Chen, M., and Yankner, B.A. (1991). An antibody to β-amyloid and the amyloid precursor protein inhibits cell-substratum adhesion in many mammalian cell types. Neurosci. Lett. 125, 223-226.
25. Citron, M., Oltersdorf, T., Haass, C., McConlogue, L., Hung, A.Y., Seubert, P., Vigo-Pelfrey, C., Lieberburg, I., and Selkoe, D.J. (1992). Mutation of the β-amyloid precursor protein in familial Alzheimer's disease increases β-protein production. Nature 360, 672-674.
26. Copani, A., Koh, J.Y., and Cotman, C.W. (1991). β-Amyloid increases neuronal susceptibility to injury by glucose deprivation. Neuroreport 2, 763-765.
27. Corder, E.H., Saunders, A.M., Risch, N.J., Strittmatter, W.J., Schmechel, D.E., Gaskell, P.C., Rimmler, J.B., Locke, P.A., Conneally, K.E., Schmader, K.E., Small, G.W., Roses, A.D., Haines, J.L., and Pericak-Vance, M.A. (1994). Apolipoprotein E type 2 allele decreases the risk of late-onset Alzheimer's disease. Nature Genet. 7, 180-184.
28. Coyle, J.T., and Puttfarcken, P. (1993). Oxidative stress, glutamate, and neurodegenerative disorders. Science 262, 689-695.
29. Daigle, I., and Li, C. (1993). apl-1, a Caenorhabditis elegans gene encoding a protein related to the human β-amyloid protein precursor. Proc. Natl. Acad. Sci. USA 90, 12045-12049.
30. Davies, P., and Maloney, A.J.F. (1976). Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 2, 1403.
31. Dekker, A.J., Winkler, J., Ray, J., Thal, L.J., and Gage, F.H. (1994). Grafting of nerve growth factor-producing fibroblasts reduces behavioral deficits in rats with lesions of the nucleus basalis magnocellularis. Neuroscience 60, 299-309.
32. Dickson, D.W., Crystal, H.A., Mattiace, L.A., Masur, D.M., Blau, A.D., Davies, P., Yen, S.H., and Aronson, M.K. (1991). Identification of normal and pathological aging in prospectively studied nondemented elderly humans. Neurobiol. Aging 13, 179-189.
33. Dyrks, T., Dyrks, E., Hartmann, T., Masters, C., and Beyreuther, K. (1992). Amyloidogenicity of β/A4 and β/A4-bearing amyloid protein precursor fragments by metal-catalyzed oxidation. J. Biol. Chem. 267, 18210-18217.
34. Esch, F.S., Keim, P.S., Beattie, E.C., Blacher, R.W., Culwell, A.R., Oltersdorf, T., McClure, D., and Ward, P.J. (1990). Cleavage of amyloid β peptide during constitutive processing of its precursor. Science 248, 1122-1124.
35. Fasman, G.D., Perczel, A., and Moore, C.D. (1995). Solubilization of β-amyloid-(1-42)-peptide: reversing the β-sheet conformation induced by aluminum with silicates. Proc. Natl. Acad. Sci. USA 92, 369-371.
36. Forloni, G., Angeretti, N., Chiesa, R., Monzani, E., Salmona, M., Bugiani, O., and Tagliavini, F. (1993a). Neurotoxicity of a prion protein fragment. Nature 362, 543-546.
37. Forloni, G., Chiesa, R., Smiroldo, S., Verga, L., Salmona, M., Tagliavini, F., and Angeretti, N. (1993b). Apoptosis mediated neurotoxicity induced by chronic application of β amyloid fragment 25-35. Neuroreport 4, 523-526.
38. Fraser, P.E., Nguyen, J.T., Chin, D.T., and Kirschner, D.A. (1992). Effects of sulfate ions on Alzheimer β/A4 peptide assemblies: implications for amyloid fibril-proteoglycan interactions. J. Neurochem. 59, 1531-1540.
39. Frautschy, S.A., Baird, A., and Cole, G.M. (1991). Effects of injected Alzheimer β-amyloid cores in rat brain. Proc. Natl. Acad. Sci. USA 88, 8362-8366.
40. + channels and suppression of neuronal activity by secreted β-amyloid-precursor protein. Nature 379, 74-78.
41. Gabuzda, D., Busciglio, J., Chen, L.B., Matsudaira, P., and Yankner, B.A. (1994). Inhibition of energy metabolism alters the processing of amyloid precursor protein and induces a potentially amyloidogenic derivative. J. Biol. Chem. 269, 13623-13628.
42. Games, D., Adams, D., Alessandrini, R., Barbour, R., Berthelette, P., Blackwell, C., Carr, T., Clemens, 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., Montoya-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., and Zhao, J. (1995). Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373, 523-527.
43. Giovannelli, L., Casamenti, F., Scali, C., Bartolini, L., and Pepeu, G. (1995). Differential effects of amyloid peptides β-(1-40) and β-(25-35) injections into the rat nucleus basalis. Neuroscience 66, 781-792.
44. Glenner, G.G., and Wong, C.W. (1984). Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120, 885-890.
45. Goate, A., Chartier-Harlin, M.-C., Mullan, M., Brown, J., Crawford, F., Fidani, L., Giuffra, L., Haynes, A., Irving, N., James, L., Mant, R., Newton, P., Rooke, K., Roques, P., Talbot, C., Pericak-Vance, M., Roses, A., Williamson, R., Rossor, M., Owen, M., and Hardy, J. (1991). Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349, 704-706.
46. Goedert, M. (1993). Tau protein and the neurofibrillary pathology of Alzheimer's disease. Trends Neurosci. 16, 460-465.
47. Greenberg, S.M., Koo, E.H., Selkoe, D.J., Qiu, W.Q., and Kosik, K.S. (1994). Secreted β-amyloid precursor protein stimulates mitogen-activated protein kinase and enhances tau phosphorylation. Proc. Natl. Acad. Sci. USA 91, 7104-7108.
48. Greenlund, L.J.S., Deckwerth, T.L., and Johnson, E.M., Jr. (1995). Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron 14, 303-315.
49. Haass, C., Schlossmacher, M.G., Hung, A.Y., Vigo-Pelfrey, C., Mellon, A., Ostaszewski, B.L., Lieberburg, I., Koo, E.H., Schenk, D., Teplow, D.B., and Selkoe, D.J. (1992). Amyloid β-peptide is produced by cultured cells during normal metabolism. Nature 359, 322-325.
50. Han, S.-H., Einstein, G., Weisgraber, K.H., Strittmatter, W.J., Saunders, A.M., Pericak-Vance, M., Roses, A.D., and Schmechel, D.E. (1994). Apolipoprotein E is localized to the cytoplasm of human cortical neurons: a light and electron microscopic study. J. Neuropathol. Exp. Neurol. 53, 535-544.
51. Hensley, K., Carney, J.M., Mattson, M.P., Aksenova, M., Harris, M., Wu, J.F., Floyd, R.A., and Butterfield, D.A. (1994). A model for β-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease. Proc. Natl. Acad. Sci. USA 91, 3270-3274.
52. Higgins, L.S., Holtzman, D.M., Rabin, J., Mobley, W.C., and Cordell, B. (1994). Transgenic mouse brain histopathology resembles early Alzheimer's disease. Ann. Neurol. 35, 598-607.
53. Howlett, D.R., Jennings, K.H., Lee, D.C., Clark, M.S.G., Brown, F., Wetzel, R., Wood, S.J., Camilleri, P., and Roberts, G.W. (1995). Aggregation state and neurotoxic properties of Alzheimer β-amyloid peptide. Neurodegeneration 4, 23-32.
54. Hsiao, K.K., Borchelt, D.R., Olson, K., Johannsdottir, R., Kitt, C., Yunis, W., Xu, S., Eckman, C., Younkin, S., Price, D., Iadecola, C., Clark, H.B., and Carlson, G. (1995). Age-related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins. Neuron 15 1203-1218.
55. Ignatius, M.J., Gebicke-Haerter, P.J., Skene, J.H.P., Schilling, J.W., Weisgraber, K.H., Mahley, R.W., and Shooter, E.M. (1986). Expression of apolipoprotein E during nerve degeneration and regeneration. Proc. Natl. Acad. Sci. USA 83, 1125-1129.
56. Iwatsubo, T., Odaka, A., Suzuki, N., Mizusawa, H., Nukina, N., and Ihara, Y. (1994). Visualization of Aβ42(43) and Aβ40 in senile plaques with end-specific Aβ monoclonals: evidence that an initially deposited species is Aβ42(43). Neuron 13, 45-53.
57. Jarrett, J.T., and Lansbury, P.T., Jr. (1993). Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058.
58. Kane, D.J., Sarafian, T.A., Anton, R., Hahn, H., Gralla, E.B., Valentine, J.S., Örd, T., and Bredesen, D.E. (1993). Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262, 1274-1277.
59. Kang, J., Lemaire, H.-G., Unterbeck, A., Salbaum, J.M., Masters, C.L., Grzeschik, K.H., Multhaup, G., Beyreuther, K., and Muller-Hill, B. (1987). The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325, 733-736.
60. Katzman, R., Terry, R., DeTeresa, R., Brown, T., Davies, P., Fuld, P., Renbing, X., and Peck, A. (1988). Clinical, pathological, and neurochemical changes in dementia: a subgroup with preserved mental status and numerous neocortical plaques. Ann. Neurol. 23, 138-144.
61. Kibbey, M.C., Jucker, M., Weeks, B.S., Neve, R.L., Van Nostrand, W.E., and Kleinman, H.K. (1993). β-Amyloid precursor protein binds to the neurite-promoting IKVAV site of laminin. Proc. Natl. Acad. Sci. USA 90, 10150-10153.
62. Kisilevsky, R., Lemieux, L.J., Fraser, P.E., Kong, X., Hultin, P.G., and Szarek, W.A. (1995). Arresting amyloids in vivo using small-molecule anionic sulphonates or sulphates: implications for Alzheimer's disease. Nature Med. 1, 143-148.
63. Kitaguchi, N., Takahashi, Y., Tokushima, Y., Shiojiri, S., and Ito, H. (1988). Novel precursor of Alzheimer's disease amyloid protein shows protease inhibitory activity. Nature 331, 530-532.
64. Koh, J.Y., Yang, L.L., and Cotman, C.W. (1990). β-Amyloid protein increases the vulnerability of cultured cortical neurons to excitotoxic damage. Brain Res. 533, 315-320.
65. Koliatsos, V.E., Clatterbuck, R.E., Gouras, G.K., and Price, D.L. (1991). Biologic effects of nerve growth factor on lesioned basal forebrain neurons. Ann. NY Acad. Sci. 640, 102-109.
66. Koo, E.H., Sisodia, S.S., Archer, D.A., Martin, L.J., Weidemann, A., Beyreuther, K., Fischer, P., Masters, C.L., and Price, D.L. (1990). Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc. Natl. Acad. Sci. USA 87, 1561-1565.
67. Kovacs, D.M., Fausett, H.J., Page, K.J., Kim, T.-W., Moir, R.D., Merriam, D.E., Hollister, R.D., Hallmark, O.G., Mancini, R., Felsenstein, K.M., Hyman, B.T., Tanzi, R.E., and Wasco, W. (1996). Alzheimer-associated presenilins 1 and 2: neuronal expression in brain and localization to intracellular membranes in mammalian cells. Nature Med. 2, 224-229.
68. Kowall, N.W., Beal, M.F., Busciglio, J., Duffy, L.K., and Yankner, B.A. (1991). An in vivo model for the neurodegenerative effects of β amyloid and protection by substance P. Proc. Natl. Acad. Sci. USA 88, 7247-7251.
69. Lamb, B.T., Sisodia, S.S., Lawler, A.M., Slunt, H.H., Kitt, C.A., Kearns, W.G., Pearson, P.L., Price, D.L., and Gearhart, J.D. (1993). Introduction and expression of the 400 kilobase amyloid precursor protein gene in transgenic mice. Nature Genet. 5, 22-30.
70. Lassmann, H., Bancher, C., Breitschopf, H., Wegiel, J., Bobinski, M., Jellinger, K., and Wisniewski, H.M. (1995). Cell death in Alzheimer's disease evaluated by DNA fragmentation in situ. Acta Neuropathol. 89, 35-41.
71. Levitan, D., and Greenwald, I. (1995). Facilitation of lin-12-mediated signalling by sel-12, a Caenorhabditis elegans S182 Alzheimer's disease gene. Nature 377, 351-354.
72. Levy, E., Carman, M.D., Fernandez-Madrid, I.J., Power, M.D., Lieberburg, I., van Duinen, S.G., Bots, G.T.A.M., Luyendijk, W., and Frangione, B. (1990). Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch-type. Science 248, 1124-1126.
73. Levy-Lahad, E., Wasco, W., Poorkaj, P., Romano, D.M., Oshima, J., Pettingell, W.H., Yu, C.-E., Jondro, P.D., Schmidt, S.D., Wang, K., Crowley, A.C., Fu, Y.-H., Guenette, S.Y., Galas, D., Nemens, E., Wijsman, E.M., Bird, T.D., Schellenberg, G.D., and Tanzi, R.E. (1995). Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science 269, 973-977.
74. L'Hernault, S.W., and Arduengo, P.M. (1992). Mutation of a putative sperm membrane protein in Caenorhabditis elegans prevents sperm differentiation but not its associated meiotic divisions. J. Cell Biol. 119, 55-68.
75. Li, J., Ma, J., and Potter, H. (1995). Identification and expression analysis of a potential familial Alzheimer disease gene on chromosome 1 related to AD3. Proc. Natl. Acad. Sci. USA 92, 12180-12184.
76. 25-35 peptide-mediated neurotoxicity in rat hippocampal cultures. J. Neurosci. Res. 39, 494-505.
77. Loo, D.T., Copani, A., Pike, C.J., Whittemore, E.R., Walencewicz, A., and Cotman, C.W. (1993). Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA 90, 7951-7955.
78. Lorenzo, A., and Yankner, B.A. (1994). β-Amyloid neurotoxicity requires fibril formation and is inhibited by Congo red. Proc. Natl. Acad. Sci. USA 91, 12243-12247.
79. Lorenzo, A., Razzaboni, B., Weir, G.C., and Yankner, B.A. (1994). Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 368, 756-760.
80. Lu, Q., and Wood, J.G. (1993). Functional studies of Alzheimer's disease tau protein. J. Neurosci. 13, 508-515.
81. Luo, L., Tully, T., and White, K. (1992). Human amyloid precursor protein ameliorates behavioral deficit of flies deleted for Appl gene. Neuron 9, 595-605.
82. 1-antichymotrypsin and apolipoprotein E promote assembly of Alzheimer β-protein into filaments. Nature 372, 92-94.
83. Maggio, J.E., Stimson, E.R., Ghilardi, J.R., Allen, C.J., Dahl, C.E., Whitcomb, D.C., Vigna, S.R., Vinters, H.V., Labenski, M.E., and Mantyh, P.W. (1992). Reversible in vitro growth of Alzheimer disease β-amyloid plaques by deposition of labeled amyloid peptide. Proc. Natl. Acad. Sci. USA 89, 5462-5466.
84. Mahley, R.W. (1988). Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240, 622-630.
85. Mann, D.M.A., and Esiri, M.M. (1989). The pattern of acquisition of plaques and tangles in the brains of patients under 50 years of age with Down's syndrome. J. Neurol. Sci. 89, 169-179.
86. Mantyh, P.W., Ghilardi, J.R., Rogers, S., DeMaster, E., Allen, C.J., Stimson, E.R., and Maggio, J.E. (1993). Aluminum, iron, and zinc ions promote aggregation of physiological concentrations of β-amyloid peptide. J. Neurochem. 61, 1171-1174.
87. Markowska, A.L., Koliatsos, V.E., Breckler, S.J., Price, D.L., and Olton, D.S. (1994). Human nerve growth factor improves spatial memory in aged but not in young rats. J. Neurosci. 14, 4815-4824.
88. Martin, L.J., Pardo, C.A., Cork, L.C., and Price, D.L. (1994). Synaptic pathology and glial responses to neuronal injury precede the formation of senile plaques and amyloid deposits in the aging cerebral cortex. Am. J. Pathol. 145, 1358-1381.
89. Masters, C.L., Simms, G., Weinman, N.A., Multhaup, G., McDonald, B.L., and Beyreuther, K. (1985). Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. USA 82, 4245-4249.
90. Mattson, M.P., and Goodman, Y. (1995). Different amyloidogenic peptides share a similar mechanism of neurotoxicity involving reactive oxygen species and calcium. Brain Res. 676, 219-224.
91. Mattson, M.P., Cheng, B., Davis, D., Bryant, K., Lieberburg, I., and Rydel, R.E. (1992). β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neurosci. 12, 376-389.
92. Mattson, M.P., Cheng, B., Culwell, A.R., Esch, F.S., Lieberburg, I., and Rydel, R.E. (1993a). Evidence for excitoprotective and interneuronal calcium-regulating roles for secreted forms of the β-amyloid precursor protein. Neuron 10, 243-254.
93. Mattson, M.P., Tomaselli, K.J., and Rydel, R.E. (1993b). Calcium-destabilizing and neurodegenerative effects of aggregated β-amyloid peptide are attenuated by basic FGF. Brain Res. 621, 35-49.
94. May, P.C., Gitter, B.D., Waters, D.C., Simmons, L.K., Becker, G.W., Small, J.S., and Robison, P.M. (1992). β-Amyloid peptide in vitro toxicity: lot-to-lot variability. Neurobiol. Aging 13, 605-607.
95. May, P.C., Boggs, L.N., and Fuson, K.S. (1993). Neurotoxicity of human amylin in rat primary hippocampal cultures: similarity to Alzheimer's disease amyloid-β neurotoxicity. J. Neurochem. 61, 2330-2333.
96. McGeer, P.L., Rogers, J., and McGeer, E.G. (1994). Neuroimmune mechanisms in Alzheimer disease pathogenesis. Alzheimer Dis. Assoc. Disord. 8, 149-158.
97. Mecocci, P., MacGarvey, U., and Beal, M.F. (1994). Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann. Neurol. 36, 747-750.
98. Meda, L., Cassatella, M.A., Szendrei, G.I., Otvos, L., Jr., Baron, P., Villalba, M., Ferrari, D., and Rossi, F. (1995). Activation of microglial cells by β-amyloid protein and interferon-γ. Nature 374, 647-650.
99. Mesulam, M.-M., and Geula, C. (1994). Butyrylcholinesterase reactivity differentiates the amyloid plaques of aging from those of dementia. Ann. Neurol. 36, 722-724.
100. Milward, E.A., Papadopoulos, R., Fuller, S.J., Moir, R.D., Small, D., Beyreuther, K., and Masters, C.L. (1992). The amyloid protein precursor of Alzheimer's disease is a mediator of the effects of nerve growth factor on neurite outgrowth. Neuron 9, 129-137.
101. Moran, P.M., Higgins, L.S., Cordell, B., and Moser, P.C. (1995). Age-related learning deficits in transgenic mice expressing the 751-amino acid isoform of human β-amyloid precursor protein. Proc. Natl. Acad. Sci. USA 92, 5341-5345.
102. Morris, J.C., McKeel, D.W., Jr., Storandt, M., Rubin, E.H., Price, J.L., Grant, E.A., Ball, M.J., and Berg, L. (1991). Very mild Alzheimer's disease: informant-based clinical, psychometric, and pathologic distinction from normal aging. Neurology 41, 469-478.
103. Mucke, L., Masliah, E., Johnson, W.B., Ruppe, M.D., Alford, M., Rockenstein, E.M., Forss-Petter, S., Pietropaolo, M., Mallory, M., and Abraham, C.R. (1994). Synaptotrophic effects of human amyloid β protein precursors in the cortex of transgenic mice. Brain Res. 666, 151-167.
104. Mucke, L., Abraham, C.R., Ruppe, M.D., Rockenstein, E.M., Toggas, S.M., Mallory, M., Alford, M., and Masliah, E. (1995). Protection against HIV gp120-induced brain damage by neuronal expression of human amyloid precursor protein. J. Exp. Med. 181, 1551-1556.
105. Mullan, M., Crawford, F., Axelman, K., Houlden, H., Lilius, L., Winblad, B., and Lannfelt, L. (1992). A pathogenic mutation for probable Alzheimer's disease in the APP gene at the N-terminus of β-amyloid. Nature Genet. 1, 345-347.
106. Müller, U., Cristina, N., Li, Z.-W., Wolfer, D.P., Lipp, H.-P., Rülicke, T., Brandner, S., Aguzzi, A., and Weissmann, C. (1994). Behavioral and anatomical deficits in mice homozygous for a modified β-amyloid precursor protein gene. Cell 79, 755-765.
107. Namba, Y., Tomonaga, M., Kawasaki, H., Otomo, E., and Ikeda, K. (1991). Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer's disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Res. 541, 163-166.
108. Näslund, J., Thyberg, J., Tjernberg, L.O., Wernstedt, C., Karlström, A. R., Bogdanovic, N., Gandy, S.E., Lannfelt, L., Terenius, L., and Nordstedt, C. (1995). Characterization of stable complexes involving apolipoprotein E and the amyloid β peptide in Alzheimer's disease brain. Neuron 15, 219-228.
109. Nathan, B.P., Bellosta, S., Sanan, D.A., Weisgraber, K.H., Mahley, R.W., and Pitas, R.E. (1994). Differential effects of apolipoproteins E3 and E4 on neuronal growth in vitro. Science 264, 850-852.
110. Nelson, P.T., Greenberg, S.G., and Saper, C.B. (1994). Neurofibrillary tangles in the cerebral cortex of sheep. Neurosci. Lett. 170, 187-190.
111. o. Nature 362, 75-79.
112. Pike, C.J., Walencewicz, A.J., Glabe, C.G., and Cotman, C.W. (1991). In vitro aging of β-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res. 563, 311-314.
113. Pike, C.J., Burdick, D., Walencewicz, A.J., Glabe, C.G., and Cotman, C.W. (1993). Neurodegeneration induced by β-amyloid peptides in vitro: the role of peptide assembly state. J. Neurosci. 13, 1676-1687.
114. Podlisny, M.B., Stephenson, D.T., Frosch, M.P., Tolan, D.R., Lieberburg, I., Clemens, J.A., and Selkoe, D.J. (1993). Microinjection of synthetic amyloid β-protein in monkey cerebral cortex fails to produce acute neurotoxicity. Am. J. Pathol. 142, 17-24.
115. Podlisny, M.B., Ostaszewski, B.L., Squazzo, S.L., Koo, E.H., Rydell, R.E., Teplow, D.B., and Selkoe, D.J. (1995). Aggregation of secreted amyloid β-protein into sodium dodecyl sulfate-stable oligomers in cell culture. J. Biol. Chem. 270, 9564-9570.
116. Poirier, J. (1994). Apolipoprotein E in animal models of CNS injury and in Alzheimer's disease. Trends Neurosci. 17, 525-530.
117. Poirier, J., Hess, M., May, P.C., and Finch, C.E. (1991). Astrocytic apolipoprotein E mRNA and GFAP mRNA in hippocampus after entorhinal cortex lesioning. Mol. Brain Res. 11, 97-106.
118. Pollack, S.J., Sadler, I.I.J., Hawtin, S.R., Tailor, V.J., and Shearman, M.S. (1995). Sulfated glycosaminoglycans and dyes attenuate the neurotoxic effects of β-amyloid in rat PC12 cells. Neurosci. Lett. 184, 113-116.
119. Polvikoski, T., Sulkava, R., Haltia, M., Kainulainen, K., Vuorio, A., Verkkoniemi, A., Niinisto, L., Halonin, P., and Kontula, K. (1995). Apolipoprotein E, dementia, and cortical deposition of β-amyloid protein. N. Engl. J. Med. 333, 1242-1247.
120. Ponte, P., Gonzalez-DeWhitt, P., Schilling, J., Miller, J., Hsu, D., Greenberg, B., Davis, K., Wallace, W., Lieberburg, I., Fuller, F., and Cordell, B. (1988). A new A4 amyloid mRNA contains a domain homologous to serine proteinase inhibitors. Nature 331, 525-527.
121. Quon, D., Wang, Y., Catalano, R., Scardina, J.M., Murakami, K., and Cordell, B. (1991). Formation of β-amyloid protein deposits in brains of transgenic mice. Nature 352, 239-241.
122. Rebeck, G.W., Reiter, J.S., Strickland, D.K., and Hyman, B.T. (1993). Apolipoprotein E in sporadic Alzheimer's disease: allelic variation and receptor interactions. Neuron 11, 575-580.
123. Rogaev, E.I., Sherrington, R., Rogaeva, E.A., Levesque, G., Ikeda, M., Liang, Y., Chi, H., Lin, C., Holman, K., Tsuda, T., Mar, L., Sorbi, S., Nacmias, B., Placentini, S., Amaducci, L., Chumakov, I., Cohen, D., Lannfelt, L., Fraser, P.E., Rommens, J.M., and St George-Hyslop, P.H. (1995). Familial Alzheimer's disease in kindred with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature 376, 775-778.
124. Rogers, J., Cooper, N.R., Webster, S., Schultz, J., McGeer, P.L., Styren, S.D., Civin, W.H., Brachova, L., Bradt, B., Ward, P., and Lieberburg, I. (1992). Complement activation by β-amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. USA 89, 10016-10020.
125. Rogers, J., Kirby, L.C., Hempelman, S.R., Berry, D.L., McGeer, P.L., Kaszniak, A.W., Zalinski, J., Cofield, M., Mansukhani, L., Willson, P., and Kogan, F. (1993). Clinical trial of indomethacin in Alzheimer's disease. Neurology 43, 1609-1611.
126. Roher, A.E., Ball, M.J., Bhave, S.V., and Wakade, A.R. (1991). β-Amyloid from Alzheimer's disease brain inhibits spouting and survival of sympathetic neurons. Biochem. Biophys. Res. Commun. 174, 572-579.
127. Roher, A.E., Lowenson, J.D., Clarke, S., Wolkow, C., Wang, R., Cotter, R.J., Reardon, I.M., Zürcher-Neely, H.A., Heinrikson, R.L., Ball, M.J., and Greenberg, B.D. (1993). Structural alterations in the peptide backbone of β-amyloid core protein may account for its deposition and stability in Alzheimer's disease. J. Biol. Chem. 268, 3072-3083.
128. Royston, M.C., Mann, D., Pickering-Brown, S., Owen, F., Perry, R., Raghavan, R., Khin-Nu, C., Tyrer, S., Day, K., Crook, R., Hardy, J., and Roberts, G.W. (1994). Apolipoprotein E ∈2 allele promotes longevity and protects patients with Down's syndrome from dementia. Neuroreport 5, 2583-2585.
129. Rumble, B., Retallack, R., Hilbich, C., Simms, G., Multhaup, G., Martins, R., Hockey, A., Montgomery, P., Beyreuther, K., and Masters, C. L. (1989). Amyloid A4 protein and its precursor in Down's syndrome and Alzheimer's disease. N. Engl. J. Med. 320, 1446-1452.
130. Saitoh, T., Sundsmo, M., Roch, J.-M., Kimura, N., Cole, G., Schubert, D., Oltersdorf, T., and Schenk, D.B. (1989). Secreted form of amyloid β protein precursor is involved inthe growth regulation of fibroblasts. Cell 58, 615-622.
131. Sanan, D.A., Weisgraber, K., Huang, D.Y., Saunders, A., Schmechel, D., Wisniewski, T., Frangione, B., Roses, A.D., and Strittmatter, W.J. (1994). Apolipoprotein E associates with Aβ amyloid peptide to form novel monofibrils: isoform apoE4 associates more efficiently than apoE3. J. Clin. Invest. 94, 880-889.
132. Schellenberg, G.D., Bird, T.D., Wijsman, E.M., Orr, H.T., Anderson, L., Nemens, E., White, J.A., Bonnycastle, L., Weber, J.L., Alonso, M.E., Potter, H., Heston, L.L., and Martin, G.M. (1992). Genetic linkage evidence for a familial Alzheimer's disease locus on chromosome 14. Science 258, 668-671.
133. Schmechel, D.E., Saunders, A.M., Strittmatter, W.J., Crain, B.J., Hulette, C.M., Joo, S.H., Pericak-Vance, M.A., Goldgaber, D., and Roses, A.D. (1993). Increased amyloid β-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc. Natl. Acad. Sci. USA 90, 9649-9653.
134. Schubert, D., and Behl, C. (1993). The expression of amyloid β protein precursor protects nerve cells from β-amyloid and glutamate toxicity and alters their interaction with the extracellular matrix. Brain Res. 629, 275-282.
135. Schubert, D., Jin, L.-W., Saitoh, T., and Cole, G. (1989). The regulation of amyloid β protein precursor secretion and its modulatory role in cell adhesion. Neuron 3, 689-694.
136. Schweers, O., Mandelkow, E.-M., Biernat, J., and Mandelkow, E. (1995). Oxidation of cysteine-322 in the repeat domain of microtubule-associated protein tau controls the in vitro assembly of paired helical filaments. Proc. Natl. Acad. Sci. USA 92, 8463-8467.
137. Selkoe, D.J. (1994). Cell biology of the amyloid β-protein precursor and the mechanism of Alzheimer's disease. Annu. Rev. Cell. Biol. 10, 373-403.
138. Seubert, P., Vigo-Pelfrey, C., Esch, F., Lee, M., Dovey, H., Davis, D., Sinha, S., Schlossmacher, M., Whaley, J. Swindlehurst, C., McCormack, R., Wolfert, R., Selkoe, D., Lieberburg, I., and Schenk, D. (1992). Isolation and quantitation of soluble Alzheimer's β-peptide from biological fluids. Nature 359, 325-327.
139. Shearman, M.S., Ragan, C.I., and Iversen, L.I. (1994). Inhibition of PC12 cell redox activity is a specific, early indicator of the mechanism of β-amyloid-mediated cell death. Proc. Natl. Acad. Sci. USA 91, 1470-1474.
140. Sherrington, R., Rogaev, E.I., Liang, Y., Rogaeva, E.A., Levesque, G., Ikeda, M., Chi, H., Li, G., Holman, K., Tsuda, T., Mar, L., Foncin, J.-F., Bruni, A.C., Montesi, M.P., Sorbi, S., Rainero, I., Pinessi, L., Nee, L., Chumakov, I., Pollen, D., Brookes, A., Sanseau, P., Polinsky, R.J., Wasco, W., Da Silva, H.A., Haines, J.L., Pericak-Vance, M.A., Tanzi, R.E., Roses, A.D., Fraser, P.E., Rommens, J.M., and St George-Hyslop, P.H. (1995). Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375, 754-760.
141. 1-antichymotrypsin. Proc. Natl. Acad. Sci. USA 90, 6825-6828.
142. Shoji, M., Golde, T.E., Ghiso, J., Cheung, T.T., Estus, S., Shaffer, L.M., Cai, X.-D., McKay, D.M., Tintner, R., Frangione, B., and Younkin, S.G. (1992). Production of the Alzheimer amyloid β protein by normal proteolytic processing. Science 258, 126-129.
143. Sisodia, S.S., Koo, E.H., Beyreuther, K., Unterbeck, A., and Price, D.L. (1990). Evidence that β-amyloid protein in Alzheimer's disease is not derived by normal processing. Science 248, 492-495.
144. Slunt, H.H., Thinakaran, G., Von Koch, C., Lo, A.C.Y., Tanzi, R.E., and Sisodia, S.S. (1994). Expression of a ubiquitous, cross-reactive homologue of the mouse β-amyloid precursor protein (APP). J. Biol. Chem. 269, 2637-2644.
145. Smith, C.D., Carney, J.M., Starke-Reed, P.E., Oliver, C.N., Stadtman, E.R., Floyd, R.A., and Markesbery, W.R. (1991). Excess brain protein oxidation and enzyme dysfunction in normal aging and Alzheimer disease. Proc. Natl. Acad. Sci. USA 88, 10540-10543.
146. Smith, M.A., Taneda, S., Richey, P.L., Miyata, S., Yan, S.-D., Stern, D., Sayre, L.M., Monnier, V.M., and Perry, G. (1994). Advanced Maillard reaction end products are associated with Alzheimer disease pathology. Proc. Natl. Acad. Sci. USA 91, 5710-5714.
147. Smith, M.A., Rudnicka-Nawrot, M., Richey, P.L., Praprotnik, D., Mulvihill, P., Miller, C.A., Sayre, L.M., and Perry, G. (1995). Carbonyl-related posttranslational modification of neurofilament protein in the neurofibrillary pathology of Alzheimer's disease. J. Neurochem. 64, 2660-2666.
148. Snow, A.D., Sekiguchi, R., Nochlin, D., Fraser, P., Kimata, K., Mizutani, A., Arai, M., Schreier, W.A., and Morgan, D.G. (1994). An important role of heparan sulfate proteoglycan (Perlecan) in a model system for the deposition and
149. St George-Hyslop, P.H., Haines, J., Rogaev, E., Mortilla, M., Vaula, G., Pericak-Vance, M., Foncin, J.-F., Montesi, M., Bruni, A., Sorbi, S., Rainero, I., Pinessi, L., Pollen, D., Polinsky, R., Nee, L., Kennedy, J., Macciardi, F., Rogaeva, E., Liang, Y., Alexandrova, N., Lukiw, W., Schlumpf, K., Tanzi, R., Tsuda, T., Farrer, L., Cantu, J.-M., Duara, L., Amaducci, L., Bergamini, L., Gusella, J., Roses, A., and Crapper McLachlan, D. (1992). Genetic evidence for a novel familial Alzheimer's disease locus on chromosome 14. Nature Genet. 2, 330-334.
150. Strittmatter, W.J., Saunders, A.M., Schmechel, D., Pericak-Vance, M., Enghild, J., Salvesen, G.S., and Roses, A.D. (1993a). Apolipoprotein E: high avidity binding to β-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. USA 90, 1977-1981.
151. Strittmatter, W.J., Weisgraber, K.H., Huang, D.Y., Dong, L.-M., Salvesen, G.S., Pericak-Vance, M., Schmechel, D., Saunders, A.M., Goldgaber, D., and Roses, A.D. (1993b). Binding of human apolipoprotein E to synthetic amyloid β peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc. Natl. Acad. Sci. USA 90, 8098-8102.
152. Strittmatter, W.J., Saunders, A.M., Goedert, M., Weisgraber, K.H., Dong, L.-M., Jakes, R., Huang, D.Y., Pericak-Vance, M., Schmechel, D., and Roses, A.D. (1994). Isoform-specific interactions of apolipoprotein E with microtubule-associated protein tau: Implications for Alzheimer's disease. Proc. Natl. Acad. Sci. USA 91, 11183-11186.
153. Su, J.H., Anderson, A.J., Cummings, B.J., and Cotman, C.W. (1994). Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 5, 2529-2533.
154. Subbarao, K.V., Richardson, J.S., and Ang, L.C. (1990). Autopsy samples of Alzheimer's cortex show increased peroxidation in vitro. J. Neurochem. 55, 342-345.
155. 717) mutants. Science 264, 1336-1340.
156. Tanzi, R.E., McClatchey, A.I., Lamperti, E.D., Villa-Komaroff, L.T., Gusella, J.F., and Neve, R.L. (1988). Protease inhibitor domain encoded by an amyloid protein precursor mRNA associated with Alzheimer's disease. Nature 331, 528-530.
157. Terry, R.D., Masliah, E., Salmon, D.P., Butters, N., DeTeresa, R., Hill, R., Hansen, L.A., and Katzman, R. (1991). Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572-580.
158. Thinakaran, G., Kitt, C.A., Roskams, J.I., Slunt, H.H., Masliah, E., von Koch, C., Ginsberg, S.D., Ronnett, G.V., Reed, R.R., Price, D.L., and Sisodia, S.S. (1995). Distribution of an APP homolog, APLP2, in the mouse olfactory system: a potential role for APLP2 in axogenesis. J. Neurosci. 15, 6314-6326.
159. Tuszynski, M.H., Sang, H., Yoshida, K., and Gage, F.H. (1991). Recombinant human nerve growth factor infusions prevent cholinergic neuronal degeneration in the adult primate brain. Ann. Neurol. 30, 625-636.
160. Urbányi, Z., Lakics, V., and Erd@, S.L. (1994). Serum amyloid P component-induced cell death in primary cultures of rat cerebral cortex. Eur. J. Pharm. 270, 375-378.
161. Van Nostrand, W.E., Wagner, S.L., Shankle, W.R., Farrow, J.S., Dick, M., Rozemuller, J.M., Kuiper, M.A., Wolters, E.C., Zimmerman, J., Cotman, C. W., and Cunningham, D.D. (1992). Decreased levels of soluble amyloid β-protein precursor in cerebrospinal fluid of live Alzheimer disease patients. Proc. Natl. Acad. Sci. USA 89, 2551-2555.
162. Vitek, M.P., Bhattacharya, K., Glendening, J.M., Stopa, E., Vlassara, H., Bucala, R., Manogue, K., and Cerami, A. (1994). Advanced glycation end products contribute to amyloidosis in Alzheimer disease. Proc. Natl. Acad. Sci. USA 91, 4766-4770.
163. 2+-binding protein ALG-2 and Alzheimer's disease gene ALG-3. Science 271, 521-525.
164. Wasco, W., Bupp, K., Magendantz, M., Gusella, J.F., Tanzi, R.E., and Solomon, F. (1992). Identification of a mouse brain cDNA that encodes a protein related to the Alzheimer disease-associated amyloid β protein precursor. Proc. Natl. Acad. Sci. USA 89, 10758-10762.
165. Wasco, W., Gurubhagavatula, S., d. Paradis, M., Romano, D.M., Sisodia, S.S., Hyman, B.T., Neve, R.L., and Tanzi, R.E. (1993). Isolation and characterization of APLP2 encoding a homologue of the Alzheimer's associated amyloid β protein precursor. Nature Genet. 5, 95-100.
166. Wasco, W., Pettingel, W.P., Jondro, P.D., Schmidt, S.D., Gurubhagavatula, S., Rodes, L., diBlasi, T., Romano, D.M., Guenette, S. Y., Kovacs, D.M., Growdon, J.H., Tanzi, R.E. (1995). Familial Alzheimer's chromosome 14 mutations. Nature Med. 1, 848.
167. Weidemann, A., König, G., Bunke, D., Fischer, P., Salbaum, J.M., Masters, C.L., and Beyreuther, K. (1989). Identification, biogenesis, and localization of precursors of Alzheimer's disease A4 amyloid protein. Cell 57, 115-126.
168. Whitehouse, P.J., Price, D.L., Struble, R.G., Clark, A.W., Coyle, A.W., and Delon, M.R. (1982). Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215, 1237-1239.
169. Whitson, J.S., and Appel, S.H. (1995). Neurotoxicity of Aβ amyloid protein in vitro is not altered by calcium channel blockade. Neurobiol. Aging 16, 5-10.
170. Wisniewski, T., and Frangione, B. (1992). Apolipoprotein E: A pathological chaperone protein in patients with cerebral and systemic amyloid. Neurosci. Lett. 135, 235-238.
171. Wisniewski, T., Ghiso, J., and Frangione, B. (1991). Peptides homologous to the amyloid protein of Alzheimer's disease containing a glutamine for glutamic acid substitution have accelerated amyloid fibril formation. Biochem. Biophys. Res. Commun. 179, 1247-1254.
172. Wisniewski, T., Castaño, E.M., Golabek, A., Vogel, T., and Frangione, B. (1994). Acceleration of Alzheimer's fibril formation by apolipoprotein E in vitro. Am. J. Pathol. 145, 1030-1034.
173. Yamazaki, T., Yamaguchi, H., Nakazato, Y., Ishiguro, K., Kawarabayashi, T., and Hirai, S. (1992). Ultrastructural characterization of cerebellar diffuse plaques in Alzheimer's disease. J. Neuropath. Exp. Neurol. 51, 281-286.
174. Yamazaki, T., Selkoe, D.J., and Koo, E.H. (1995). Trafficking of cell surface β-amyloid precursor protein: retrograde and transcytotic transport in cultured neurons. J. Cell Biol. 129, 431-442.
175. Yankner, B.A., Dawes, L.R., Fisher, S., Villa-Komaroff, L., Oster-Granite, M.L., and Neve, R.L. (1989). Neurotoxicity of a fragment of the amyloid precursor associated with Alzheimer's disease. Science 245, 417-429.
176. Yankner, B.A., Duffy, L.K., and Kirschner, D.A. (1990a). Neurotrophic and neurotoxic effects of amyloid β protein: reversal by tachykinin neuropeptides. Science 250, 279-282.
177. Yankner, B.A., Caceres, A., and Duffy, L.K. (1990b). Nerve growth factor potentiates the neurotoxicity of β amyloid. Proc. Natl. Acad. Sci. USA 87, 9020-9023.
178. Zhang, C., Lambert, M.P., Bunch, C., Barber, K., Wade, W.S., Krafft, G. A., and Klein, W.L. (1994). Focal adhesion kinase expressed by nerve cell lines shows increased tyrosine phosphorylation in response to Alzheimer's Aβ peptide. J. Biol. Chem. 269, 25247-25250.
179. Zheng, H., Jiang, M., Trumbauer, M.E., Sirinathsinghji, D.J. S., Hopkins, R., Smith, D.W., Heavens, R.P., Dawson, G.R., Boyce, S., Conner, M.W., Stevens, K.A., Slunt, H.H., Sisodia, S.S., Chen, H.Y., and Van der Ploeg, L.H. T. (1995). β-Amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81, 525-531.