Structure and functions of the human amyloid precursor protein: The whole is more than the sum of its parts

Progress in Neurobiology

Volumn 82, Issue 1, 2007, Pages 11-32

  Gralle, Matthias ^a   Ferreira, Sérgio T ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Adhesion protein; Alzheimer's disease; Amyloid precursor protein; Dimerization; Functions; Structural determination

Indexed keywords

AMYLOID PRECURSOR PROTEIN;

ALZHEIMER DISEASE; BRAIN FUNCTION; DIMERIZATION; HUMAN; MORPHOGENESIS; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVOUS SYSTEM; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; SYNAPTOGENESIS; X RAY CRYSTALLOGRAPHY;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; HUMANS; PROTEIN STRUCTURE, TERTIARY;

EID: 34248172449     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2007.02.001     Document Type: Review

References (223)

1. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., and Walter P. Cell communication. Molecular Biology of the Cell (2002), Garland Science, New York pp. 831-907
2. Allinquant B., Moya K.L., Bouillot C., and Prochiantz A. Amyloid precursor protein in cortical neurons-coexistence of 2 pools differentially distributed in axons and dendrites and association with cytoskeleton. J. Neurosci. 14 (1994) 6842-6854
3. Allinquant B., Hantraye P., Mailleux P., Moya K., Bouillot C., and Prochiantz A. Down-regulation of amyloid precursor protein inhibits neurite outgrowth in vitro. J. Cell Biol. 128 (1995) 919-927
4. Anandatheerthavarada H.K., Biswas G., Robin M.A., and Avadhani N.G. Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells. J. Cell Biol. 161 (2003) 41-54
5. Ando K., Oishi M., Takeda S., Iijima K., Isohara T., Nairn A.C., Kirino Y., Greengard P., and Suzuki T. Role of phosphorylation of Alzheimer's amyloid precursor protein during neuronal differentiation. J. Neurosci. 19 (1999) 4421-4427
6. Arai R., Wriggers W., Nishikawa Y., Nagamune T., and Fujisawa T. Conformations of variably linked chimeric proteins evaluated by synchrotron X-ray small-angle scattering. Proteins 57 (2004) 829-838
7. Araki W., Kitaguchi N., Tokushima Y., Ishii K., Aratake H., Shimohama S., Nakamura S., and Kimura J. Trophic effect of beta-amyloid precursor protein on cerebral cortical neurons in culture. Biochem. Biophys. Res. Comm. 181 (1991) 265-271
8. Arama E., Agapite J., and Steller H. Caspase activity and a specific cytochrome c are required for sperm differentiation in Drosophila. Dev. Cell 4 (2003) 687-697
9. Arendt T., Schindler C., Bruckner M.K., Eschrich K., Bigl V., Zedlick D., and Marcova L. Plastic neuronal remodeling is impaired in patients with Alzheimer's disease carrying apolipoprotein epsilon 4 allele. J. Neurosci. 17 (1997) 516-529
10. Arendt T., Bruckner M.K., Gertz H.J., and Marcova L. Cortical distribution of neurofibrillary tangles in Alzheimer's disease matches the pattern of neurons that retain their capacity of plastic remodelling in the adult brain. Neuroscience 83 (1998) 991-1002
11. Barnham K.J., McKinstry W.J., Multhaup G., Galatis D., Morton C.J., Curtain C.C., Williamson N.A., White A.R., Hinds M.G., Norton R.S., Beyreuther K., Masters C.L., Parker M.W., and Cappai R. Structure of the Alzheimer's disease amyloid precursor protein copper binding domain-a regulator of neuronal copper homeostasis. J. Biol. Chem. 278 (2003) 17401-17407
12. Beher D., Hesse L., Masters C.L., and Multhaup G. Regulation of amyloid protein precursor (APP) binding to collagen and mapping of the binding sites on APP and collagen type I. J. Biol. Chem. 271 (1996) 1613-1620
13. Berezovska O., Ramdya P., Skoch J., Wolfe M.S., Bacskai B.J., and Hyman B.T. Amyloid precursor protein associates with a nicastrin-dependent docking site on the presenilin 1-gamma-secretase complex in cells demonstrated by fluorescence lifetime imaging. J. Neurosci. 23 (2003) 4560-4566
14. Blangy A., Vidal F., Cuzin F., Yang Y.H., Boulukos K.E., and Rassoulzadegan M. CDEBP, s site-specific DNA-binding protein of the 'APP-like' family, is required during the early development of the mouse. J. Cell Sci. 108 (1995) 675-683
15. Blasko I., Beer R., Bigl M., Apelt J., Franz G., Rudzki D., Ransmayr G., Kampfl A., and Schliebs R. Experimental traumatic brain injury in rats stimulates the expression, production and activity of Alzheimer's disease beta-secretase (BACE-1). J. Neural Transm. 111 (2004) 523-536
16. Borg J.P., Ooi J., Levy E., and Margolis B. The phosphotyrosine interaction domains of X11 and FE65 bind to distinct sites on the YENPTY motif of amyloid precursor protein. Mol. Cell. Biol. 16 (1996) 6229-6241
17. Botelho M.G., Gralle M., Oliveira C.L.P., Torriani I., and Ferreira S.T. Folding and stability of the extracellular domain of the human amyloid precursor protein. J. Biol. Chem. 278 (2003) 34259-34267
18. Breen K.C., Bruce M., and Anderton B.H. Beta-amyloid precursor protein mediates neuronal cell-cell and cell-surface adhesion. J. Neurosci. Res. 28 (1991) 90-100
19. Brouillet E., Trembleau A., Galanaud D., Volovitch M., Bouillot C., Valenza C., Prochiantz A., and Allinquant B. The amyloid precursor protein interacts with G(o) heterotrimeric protein within a cell compartment specialized in signal transduction. J. Neurosci. 19 (1999) 1717-1727
20. Bush A.I., Multhaup G., Moir R.D., Williamson T.G., Small D.H., Rumble B., Pollwein P., Beyreuther K., and Masters C.L. A novel zinc(II) binding site modulates the function of the beta-A4 amyloid protein precursor of Alzheimer's disease. J. Biol. Chem. 268 (1993) 16109-16112
21. Caillé I., Allinquant B., Dupont E., Bouillot C., Langer A., Müller U., and Prochiantz A. Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development 131 (2004) 2173-2181
22. Campbell D.S., and Holt C.E. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 37 (2003) 939-952
23. Cao X., and Südhof T.C. A transcriptionally active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293 (2001) 115-120
24. Cao X., and Südhof T.C. Dissection of amyloid-beta precursor protein-dependent transcriptional transactivation. J. Biol. Chem. 279 (2004) 24601-24611
25. Cappai, R., Cheng, F., Ciccotosto, G.D., Needham, B.E., Masters, C.L., Multhaup, G., Fransson, L.A., Mani, K., 2005. The amyloid precursor protein (APP) of Alzheimer disease and its paralog, APLP2, modulate the Cu/Zn-nitric oxide-catalyzed degradation of glypican-1 heparan sulfate in vivo. J. Biol. Chem. 280(14), 13913-13920.
26. Capsoni S., Giannotta S., and Cattaneo A. Beta-amyloid plaques in a model for sporadic Alzheimer's disease based on transgenic anti-nerve growth factor antibodies. Mol. Cell. Neurosci. 21 (2002) 15-28
27. Chen C.D., Oh S.Y., Hinman J.D., and Abraham C.R. Visualization of APP dimerization and APP-Notch2 heterodimerization in living cells using bimolecular fluorescence complementation. J. Neurochem. 97 (2006) 30-43
28. Chen F., Hasegawa H., Schmitt-Ulms G., Kawarai T., Bohm C., Katayama T., Gu Y., Sanjo N., Glista M., Rogaeva E., Wakutani Y., Pardossi-Piquard R., Ruan X., Tandon A., Checler F., Marambaud P., Hansen K., Westaway D., St George-Hyslop P., and Fraser P. TMP21 is a presenilin complex component that modulates gamma-secretase but not epsilon-secretase activity. Nature 440 (2006) 1208-1212
29. Chow N.W., Korenberg J.R., Chen X.N., and Neve R.L. APP-BP1, a novel protein that binds to the carboxyl-terminal region of the amyloid precursor protein. J. Biol. Chem. 271 (1996) 11339-11346
30. Citron M., Oltersdorf T., Haass C., McConlogue L., Hung A.Y., Seubert P., Vigopelfrey C., Lieberburg I., and Selkoe D.J. Mutation of the beta-amyloid precursor protein in familial Alzheimer's disease increases beta-protein production. Nature 360 (1992) 672-674
31. Citron M., Teplow D.B., and Selkoe D.J. Generation of amyloid beta protein from its precursor is sequence specific. Neuron 14 (1995) 661-670
32. Ciuculescu E.D., Mekmouche Y., and Faller P. Metal-binding properties of the peptide APP(170-188): a model of the Zn-II-binding site of amyloid precursor protein (APP). Chemistry 11 (2005) 903-909
33. Clarris H.J., Key B., Beyreuther K., Masters C.L., and Small D.H. Expression of the amyloid protein precursor of Alzheimer's disease in the developing rat olfactory system. Dev. Brain Res. 88 (1995) 87-95
34. 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 P.M., Schmader K.E., Small G.W., Roses A.D., Haines J.L., and Pericak-Vance M.A. Protective effect of apolipoprotein E type 2 allele for late-onset Alzheimer disease. Nat. Genet. 7 (1994) 180-184
35. Daigle I., and Li C. apl-1, a Caenorhabditis elegans gene encoding a protein related to the human beta-amyloid protein precursor. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 12045-12049
36. Dawson G.R., Seabrook G., Zheng H., Smith D.W., Graham S., O'Dowd G., Bowery B.J., Boyce S., Trumbauer M.E., Chen H.Y., Van der Ploeg L.H., and Sirinathsinghji D.J. Age-related cognitive deficits, impaired long-term potentiation and reduction in synaptic marker density in mice lacking the beta-amyloid precursor protein. Neuroscience 90 (1999) 1-13
37. de La Fournière-Besseuille L., Grange D., and Buchet R. Purification and spectroscopic characterization of beta-amyloid precursor protein from porcine brains. Eur. J. Biochem. 250 (1997) 705-711
38. De Strooper B., and Annaert W. Proteolytic processing and cell biological functions of the amyloid precursor protein. J. Cell Sci. 113 (2000) 1857-1870
39. De Strooper B., Annaert W., Cupers B., Saftig P., Craessaerts K., Mumm J.S., Schroeter E.H., Schrijvers V., Wolfe M.S., Ray W.J., Goate A., and Kopan R. A presenilin 1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398 (1999) 518-522
40. DePristo M.A., de Bakker P.I., and Blundell T.L. Heterogeneity and inaccuracy in protein structures solved by X-ray crystallography. Structure 12 (2004) 831-838
41. Devi L., Prabhu B.M., Galati D.F., Avadhani N.G., and Anandatheerthavarada H.K. Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J. Neurosci. 26 (2006) 9057-9068
42. Dityatev A., Dityateva G., Sytnyk V., Delling M., Toni N., Nikonenko I., Muller D., and Schachner M. Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J. Neurosci. 24 (2004) 9372-9382
43. Dulubova I., Ho A., Huryeva I., Südhof T.C., and Rizo J. Three-dimensional structure of an independently folded extracellular domain of human amyloid-beta precursor protein. Biochemistry 43 (2004) 9583-9588
44. Dunaevsky A., Tashiro A., Majewska A., Mason C., and Yuste R. Developmental regulation of spine motility in the mammalian central nervous system. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 13438-13443
45. Edbauer D., Winkler E., Regula J.T., Pesold B., Steiner H., and Haass C. Reconstitution of gamma-secretase activity. Nat. Cell Biol. 5 (2003) 486-488
46. Edelman G.M., and Cunningham B.A. Place-dependent cell adhesion, process retraction, and spatial signaling in neural morphogenesis. Cold Spring Harb. Symp. Quant. Biol. 55 (1990) 303-318
47. Eggert S., Paliga K., Soba P., Evin G., Masters C.L., Weidemann A., and Beyreuther K. The proteolytic processing of the amyloid precursor protein gene family members APLP-1 and APLP-2 involves alpha-, beta-, gamma-, and epsilon-like cleavages. Modulation of APLP-1 processing by N-glycosylation. J. Biol. Chem. 279 (2004) 18146-18156
48. Ehehalt R., Keller P., Haass C., Thiele C., and Simons K. Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J. Cell Biol. 160 (2003) 113-123
49. Engert F., and Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399 (1999) 66-70
50. Esler W.P., Kimberly W.T., Ostaszewski B.L., Diehl T.S., Moore C.L., Tsai J.Y., Rahmati T., Xia W.M., Selkoe D.J., and Wolfe M.S. Transition-state analogue inhibitors of gamma-secretase bind directly to presenilin-1. Nat. Cell Biol. 2 (2000) 428-434
51. Fedorov A.N., and Baldwin T.O. Process of biosynthetic protein folding determines the rapid formation of native structure. J. Mol. Biol. 294 (1999) 579-586
52. Ferreira S.T. Fluorescence studies of the conformational dynamics of parvalbumin in solution lifetime and rotational motions of the single tryptophan residue. Biochemistry 28 (1989) 10066-10072
53. Ferreira S.T., Stella L., and Gratton E. Conformational dynamics of bovine Cu, Zn superoxide dismutase revealed by time-resolved fluorescence spectroscopy of the single tyrosine residue. Biophys. J. 66 (1994) 1185-1196
54. Furukawa K., Barger S.W., Blalock E.M., and Mattson M.P. Activation of K+ channels and suppression of neuronal activity by secreted beta-amyloid precursor protein. Nature 379 (1996) 74-78
55. Furukawa K., Sopher B.L., Rydel R.E., Begley J.G., Pham D.G., Martin G.M., Fox M., and Mattson M.P. Increased activity-regulating and neuroprotective efficacy of alpha-secretase-derived secreted amyloid precursor protein conferred by a C-terminal heparin-binding domain. J. Neurochem. 67 (1996) 1882-1896
56. Galvan V., Gorostiza O.F., Banwait S., Ataie M., Logvinova A.V., Sitaraman S., Carlson E., Sagi S.A., Chevallier N., Jin K., Greenberg D.A., and Bredesen D.E. Reversal of Alzheimer's-like pathology and behavior in human APP transgenic mice by mutation of Asp664. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 7130-7135
57. Gebbink M.F., Zondag G.C., Koningstein G.M., Feiken E., Wubbolts R.W., and Moolenaar W.H. Cell surface expression of receptor protein tyrosine phosphatase RPTP mu is regulated by cell-cell contact. J. Cell Biol. 131 (1995) 251-260
58. Glenner G.G., and Wong C.W. Alzheimer's disease-initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Comm. 120 (1984) 885-890
59. Goate A., Chartier-Harlin M.C., Mullan M., Brown J., Crawford F., Fidani L., Giuffra L., Haynes A., Irving N., James L., et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349 (1991) 704-706
60. Goda Y. Cadherins communicate structural plasticity of presynaptic and postsynaptic terminals. Neuron 35 (2002) 1-3
61. Goldsbury C., Mocanu M.M., Thies E., Kaether C., Haass C., Keller P., Biernat J., Mandelkow E., and Mandelkow E.M. Inhibition of APP trafficking by tau protein does not increase the generation of amyloid-beta peptides. Traffic 7 (2006) 873-888
62. Gong Y.S., Chang L., Viola K.L., Lacor P.N., Lambert M.P., Finch C.E., Krafft G.A., and Klein W.L. Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 10417-10422
63. Goo J.H., and Park W.J. Elucidation of the interactions between C99, presenilin, and nicastrin by the split-ubiquitin assay. DNA Cell Biol. 23 (2004) 59-65
64. Gralle M., Botelho M.M., de Oliveira C.L.P., Torriani I., and Ferreira S.T. Solution studies and structural model of the extracellular domain of the human amyloid precursor protein. Biophys. J. 83 (2002) 3513-3524
65. Gralle M., Oliveira C.L.P., Guerreiro L.H., McKinstry W.J., Galatis D., Masters C.L., Cappai R., Parker M.W., Ramos H.I., Torriani I., and Ferreira S.T. Solution conformation and heparin-induced dimerization of the full-length extracellular domain of the human amyloid precursor protein. J. Mol. Biol. 357 (2006) 493-508
66. Hashimoto Y., Niikura T., Chiba T., Tsukamoto E., Kadowaki H., Nishitoh H., Yamagishi Y., Ishizaka M., Yamada M., Nawa M., Terashita K., Aiso S., Ichijo H., and Nishimoto I. The cytoplasmic domain of Alzheimer's amyloid-beta protein precursor causes sustained apoptosis signal-regulating kinase 1/c-Jun NH2-terminal kinase-mediated neurotoxic signal via dimerization. J. Pharmacol. Exp. Ther. 306 (2003) 889-902
67. Hass M.R., and Yankner B.A. A gamma-secretase-independent mechanism of signal transduction by the amyloid precursor protein. J. Biol. Chem. 280 (2005) 36895-36904
68. Heber S., Herms J., Gajic V., Hainfellner J., Aguzzi A., Rulicke T., Kretzschmar H., von Koch C., Sisodia S., Tremml P., Lipp H.P., Wolfer D.P., and Müller U. Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J. Neurosci. 20 (2000) 7951-7963
69. Hebert S.S., Serneels L., Tolia A., Craessaerts K., Derks C., Filippov M.A., Müller U., and De Strooper B. Regulated intramembrane proteolysis of amyloid precursor protein and regulation of expression of putative target genes. EMBO Rep. 7 (2006) 739-745
70. Hedstrom L., Szilagyi L., and Rutter W.J. Converting trypsin to chymotrypsin-the role of surface loops. Science 255 (1992) 1249-1253
71. Heidemann S.R. Cytoplasmic mechanisms of axonal and dendritic growth in neurons. Int. Rev. Cytol. 165 (1996) 235-296
72. Hérard, A.S., Besret, L., Dubois, A., Dauguet, J., Delzescaux, T., Hantraye, P., Bonvento, G., Moya, K.L., 2006. siRNA targeted against amyloid precursor protein impairs synaptic activity in vivo. Neurobiol. Aging 27(12), 1740-1750.
73. Herms J., Anliker B., Heber S., Ring S., Fuhrmann M., Kretzschmar H., Sisodia S., and Müller U. Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members. EMBO J. 23 (2004) 4106-4115
74. Herrick-Davis K., Grinde E., Harrigan T.J., and Mazurkiewicz J.E. Inhibition of serotonin 5-hydroxytryptamine2C receptor function through heterodimerization. Receptor dimers bind two molecules of ligand and one G-protein. J. Biol. Chem. 280 (2005) 40144-40151
75. Hesse L., Beher D., Masters C.L., and Multhaup G. The beta-A4 amyloid precursor protein binding to copper. FEBS Lett. 349 (1994) 109-116
76. Ho A., and Südhof T.C. Binding of F-spondin to amyloid-beta precursor protein: a candidate amyloid-beta precursor protein ligand that modulates amyloid-beta precursor protein cleavage. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 2548-2553
77. Huber G., Bailly Y., Martin J.R., Mariani J., and Brugg B. Synaptic beta-amyloid precursor proteins increase with learning capacity in rats. Neuroscience 80 (1997) 313-320
78. Hynes T.R., Randal M., Kennedy L.A., Eigenbrot C., and Kossiakoff A.A. X-ray crystal structure of the protease inhibitor domain of Alzheimer's amyloid beta-protein precursor. Biochemistry 29 (1990) 10018-10022
79. Ikezu T., Okamoto T., Komatsuzaki K., Matsui T., Martyn J.A.J., and Nishimoto I. Negative transactivation of cAMP response element by familial Alzheimer's mutants of APP. EMBO J. 15 (1996) 2468-2475
80. Isacson O., Seo H., Lin L., Albeck D., and Granholm A.-C. Alzheimer's disease and Down's syndrome: roles of APP, trophic factors and ACh. Trends Neurosci. 25 (2002) 79-84
81. Jansens A., van Duijn E., and Braakman I. Coordinated nonvectorial folding in a newly synthesized multidomain protein. Science 298 (2002) 2401-2403
82. Jellinger K.A. Head injury and dementia. Curr. Opin. Neurol. 17 (2004) 719-723
83. Jick H., Zornberg G.L., Jick S.S., Seshadri S., and Drachman D.A. Statins and the risk of dementia. Lancet 356 (2000) 1627-1631
84. Jin L.W., Ninomiya H., Roch J.M., Schubert D., Masliah E., Otero D.A.C., and Saitoh T. Peptides containing the RERMS sequence of amyloid beta/A4 protein precursor bind cell surface and promote neurite extension. J. Neurosci. 14 (1994) 5461-5470
85. Kakio A., Nishimoto S., Yanagisawa K., Kozutsumi Y., and Matsuzaki K. Cholesterol-dependent formation of GM1 ganglioside-bound amyloid beta-protein, an endogenous seed for Alzheimer amyloid. J. Biol. Chem. 276 (2001) 24985-24990
86. Kamal A., Stokin G.B., Yang Z.H., Xia C.H., and Goldstein L.S.B. Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28 (2000) 449-459
87. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., and Malinow R. APP processing and synaptic function. Neuron 37 (2003) 925-937
88. Kang J., and Müller-Hill B. Differential splicing of Alzheimer's disease amyloid A4 precursor RNA in rat tissues-preA4(695) messenger RNA is predominantly produced in rat and human brain. Biochem. Biophys. Res. Comm. 166 (1990) 1192-1200
89. Kang J., Lemaire H.G., Unterbeck A., Salbaum J.M., Masters C.L., Grzeschik K.H., Multhaup G., Beyreuther K., and Müller-Hill B. The precursor of Alzheimer's disease amyloid-A4 protein resembles a cell surface receptor. Nature 325 (1987) 733-736
90. Kennedy N.J., Kataoka T., Tschopp J., and Budd R.C. Caspase activation is required for T cell proliferation. J. Exp. Med. 190 (1999) 1891-1895
91. Kibbey M.C., Jucker M., Weeks B.S., Neve R.L., Van Nostrand W.E., and Kleinman H.K. Beta-amyloid precursor protein binds to the neurite-promoting IKVAV site of laminin. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 10150-10153
92. Kimberly W.T., LaVoie M.J., Ostaszewski B.L., Ye W., Wolfe M.S., and Selkoe D.J. Gamma secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 6382-6387
93. Kimberly W.T., Zheng J.B., Town T., Flavell R.A., and Selkoe D.J. Physiological regulation of the beta-amyloid precursor protein signaling domain by c-Jun N-terminal kinase JNK3 during neuronal differentiation. J. Neurosci. 25 (2005) 5533-5543
94. Kirfel G., Borm B., Rigort A., and Herzog V. The secretory beta-amyloid precursor protein is a motogen for human epidermal keratinocytes. Eur. J. Cell Biol. 81 (2002) 664-676
95. Kitaguchi N., Takahashi Y., Tokushima Y., Shiojiri S., and Ito H. Novel precursor of Alzheimer's disease amyloid protein shows protease inhibitory activity. Nature 331 (1988) 530-532
96. Klein W.L., Lacor P.N., De Felice F.G., and Ferreira S.T. Molecules that disrupt memory circuits in Alzheimer's disease: the attack on synapses by Abeta oligomers (ADDLs). In: Bontempi B., Silva A., and Christen Y. (Eds). Memories: Molecules and Circuits (2006), Springer, Paris
97. Kojro E., Gimpl G., Lammich S., Marz W., and Fahrenholz F. Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the alpha-secretase ADAM 10. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 5815-5820
98. Kong G.K., Adams J.J., Harris H.H., Boas J.F., Curtain C.C., Galatis D., Masters C.L., Barnham K.J., McKinstry W.J., Cappai R., and Parker M.W. Structural studies of the Alzheimer's amyloid precursor protein copper-binding domain reveal how it binds copper ions. J. Mol. Biol. 367 (2007) 148-161
99. Koo E.H., and Squazzo S.L. Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J. Biol. Chem. 269 (1994) 17386-17389
100. Koo E.H., Sisodia S.S., Archer D.R., Martin L.J., Weidemann A., Beyreuther K., Fischer P., Masters C.L., and Price D.L. Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 1561-1565
101. Kounnas M.Z., Moir R.D., Rebeck G.W., Bush A.I., Argraves W.S., Tanzi R.E., Hyman B.T., and Strickland D.K. LDL receptor-related protein, a multifunctional ApoE receptor, binds secreted beta amyloid precursor protein and mediates its degradation. Cell 82 (1995) 331-340
102. Kroenke C.D., Ziemnicka-Kotula D., Xu J., Kotula L., and Palmer III A.G. Solution conformations of a peptide containing the cytoplasmic domain sequence of the beta amyloid precursor protein. Biochemistry 36 (1997) 8145-8152
103. Kuida K., Zheng T.S., Na S.Q., Kuan C.Y., Yang D., Karasuyama H., Rakic P., and Flavell R.A. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384 (1996) 368-372
104. Lacor P.N., Buniel M.C., Chang L., Fernandez S.J., Gong Y.S., Viola K.L., Lambert M.P., Velasco P.T., Bigio E.H., Finch C.E., Krafft G.A., and Klein W.L. Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J. Neurosci. 24 (2004) 10191-10200
105. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., and Klein W.L. Diffusible, nonfibrillar ligands derived from A beta(1-42) are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 6448-6453
106. Lazarov O., Morfini G.A., Lee E.B., Farah M.H., Szodorai A., DeBoer S.R., Koliatsos V.E., Kins S., Lee V.M.-Y., Wong P.C., Price D.L., Brady S.T., and Sisodia S.S. Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: revisited. J. Neurosci. 25 (2005) 2386-2395
107. LeBlanc A.C., Kovacs D.M., Chen H.Y., Villare F., Tykocinski M., Autilio-Gambetti L., and Gambetti P. Role of amyloid precursor protein (APP): study with antisense transfection of human neuroblastoma cells. J. Neurosci. Res. 31 (1992) 635-645
108. Leyssen M., Ayaz D., Hebert S.S., Reeve S., De Strooper B., and Hassan B.A. Amyloid precursor protein promotes post-developmental neurite arborization in the Drosophila brain. EMBO J. 24 (2005) 2944-2955
109. Lien W.H., Klezovitch O., Fernandez T.E., Delrow J., and Vasioukhin V. alpha E-Catenin controls cerebral cortical size by regulating the hedgehog signaling pathway. Science 311 (2006) 1609-1612
110. Lindorff-Larsen K., Best R.B., DePristo M.A., Dobson C.M., and Vendruscolo M. Simultaneous determination of protein structure and dynamics. Nature 433 (2005) 128-132
111. Loewer A., Soba P., Beyreuther K., Paro R., and Merdes G. Cell-type-specific processing of the amyloid precursor protein by Presenilin during Drosophila development. EMBO Rep. 5 (2004) 405-411
112. Löffler J., and Huber G. Beta-amyloid precursor protein isoforms in various rat brain regions and during brain development. J. Neurochem. 59 (1992) 1316-1324
113. Lorenzo A., Yuan M.L., Zhang Z.H., Paganetti P.A., Sturchler-Pierrat C., Staufenbiel M., Mautino J., Sol Vigo F., Sommer B., and Yankner B.A. Amyloid beta interacts with the amyloid precursor protein: a potential toxic mechanism in Alzheimer's disease. Nat. Neurosci. 3 (2000) 460-464
114. Lue L.F., Kuo Y.M., Roher A.E., Brachova L., Shen Y., Sue L., Beach T., Kurth J.H., Rydel R.E., and Rogers J. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155 (1999) 853-862
115. Lu D.C., Shaked G.M., Masliah E., Bredesen D.E., and Koo E.H. Amyloid beta protein toxicity mediated by the formation of amyloid-beta protein precursor complexes. Ann. Neurol. 54 (2003) 781-789
116. Lu C., Wang Y., Furukawa K., Fu W., Ouyang X., and Mattson M.P. Evidence that caspase-1 is a negative regulator of AMPA receptor-mediated long-term potentiation at hippocampal synapses. J. Neurochem. 97 (2006) 1104-1110
117. Lyckman A.W., Confaloni A.M., Thinakaran G., Sisodia S.S., and Moya K.L. Post-translational processing and turnover kinetics of presynaptically targeted amyloid precursor superfamily proteins in the central nervous system. J. Biol. Chem. 273 (1998) 11100-11106
118. Majocha R.E., Agrawal S., Tang J.Y., Humke E.W., and Marotta C.A. Modulation of the PC12 cell response to nerve growth factor by antisense oligonucleotide to amyloid precursor protein. Cell Mol. Neurobiol. 14 (1994) 425-437
119. Marquez-Sterling N.R., Lo A.C.Y., Sisodia S.S., and Koo E.H. Trafficking of cell-surface beta-amyloid precursor protein: evidence that a sorting intermediate participates in synaptic vesicle recycling. J. Neurosci. 17 (1997) 140-151
120. Masters C.L., Simms G., Weinman N.A., Multhaup G., McDonald B.L., and Beyreuther K. Amyloid plaque core protein in Alzheimer's disease and Down Syndrome. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 4245-4249
121. Matsuda S., Yasukawa T., Homma Y., Ito Y., Niikura T., Hiraki T., Hirai S., Ohno S., Kita Y., Kawasumi M., Kouyama K., Yamamoto T., Kyriakis J.M., and Nishimoto I. c-Jun N-terminal kinase (JNK)-interacting protein-1b/islet-brain-1 scaffolds Alzheimer's amyloid precursor protein with JNK. J. Neurosci. 21 (2001) 6597-6607
122. Mattson M.P., Cheng B., Culwell A.R., Esch F.S., Lieberburg I., and Rydel R.E. Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of the beta-amyloid precursor protein. Neuron 10 (1993) 243-254
123. Mauch D.H., Nagler K., Schumacher S., Goritz C., Müller E.C., Otto A., and Pfrieger F.W. CNS synaptogenesis promoted by glia-derived cholesterol. Science 294 (2001) 1354-1357
124. McLean C.A., Cherny R.A., Fraser F.W., Fuller S.J., Smith M.J., Beyreuther K., Bush A.I., and Masters C.L. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 46 (1999) 860-866
125. McMahon H.T., and Gallop J.L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438 (2005) 590-596
126. Meziane H., Dodart J.C., Mathis C., Little S., Clemens J., Paul S.M., and Ungerer A. Memory-enhancing effects of secreted forms of the beta-amyloid precursor protein in normal and amnestic mice. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 12683-12688
127. Milward E.A., Papadopoulos R., Fuller S.J., Moir R.D., Small D., Beyreuther K., and Masters C.L. The amyloid protein precursor of Alzheimer's disease is a mediator of the effects of nerve growth factor on neurite outgrowth. Neuron 9 (1992) 129-137
128. Mok S.S., Sberna G., Heffernan D., Cappai R., Galatis D., Clarris H.J., Sawyer W.H., Beyreuther K., Masters C.L., and Small D.H. Expression and analysis of heparin-binding regions of the amyloid precursor protein of Alzheimer's disease. FEBS Lett. 415 (1997) 303-307
129. Morimoto T., Ohsawa I., Takamura C., Ishiguro M., Nakamura Y., and Kohsaka S. Novel domain-specific actions of amyloid precursor protein on developing synapses. J. Neurosci. 18 (1998) 9386-9393
130. Moss L. What Genes Can't Do (2003), MIT Press, Cambridge, MA
131. Moya K.L., Benowitz L.I., Schneider G.E., and Allinquant B. The amyloid precursor protein is developmentally regulated and correlated with synaptogenesis. Dev. Biol. 161 (1994) 597-603
132. Multhaup G., Bush A.I., Pollwein P., and Masters C.L. Interaction between the zinc(II) and the heparin binding site of the Alzheimer's disease beta-A4 amyloid precursor protein (APP). FEBS Lett. 355 (1994) 151-154
133. Multhaup G., Ruppert T., Schlicksupp A., Hesse L., Bill E., Pipkorn R., Masters C.L., and Beyreuther K. Copper-binding amyloid precursor protein undergoes a site-specific fragmentation in the reduction of hydrogen peroxide. Biochemistry 37 (1998) 7224-7230
134. Narindrasorasak S., Lowery D.E., Altman R.A., Gonzalez-de Whitt P.A., Greenberg B.D., and Kisilevsky R. Characterization of high-affinity binding between laminin and Alzheimer's disease amyloid precursor proteins. Lab. Invest. 67 (1992) 643-652
135. Nelson C.M., Jean R.P., Tan J.L., Liu W.F., Sniadescki N.J., Spector A.A., and Chen C.S. Emergent patterns of growth controlled by multicellular form and mechanics. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 11594-11599
136. Nishimoto I., Okamoto T., Matsuura Y., Takahashi S., Murayama Y., and Ogata E. Alzheimer amyloid protein precursor complexes with brain GTP-binding protein G(o). Nature 362 (1993) 75-79
137. Ohsawa I., Takamura C., and Kohsaka S. The amino-terminal region of amyloid precursor protein is responsible for neurite outgrowth in rat neocortical explant culture. Biochem. Biophys. Res. Commun. 236 (1997) 59-65
138. Ohsawa I., Takamura C., and Kohsaka S. Fibulin-1 binds the amino-terminal head of beta-amyloid precursor protein and modulates its physiological function. J. Neurochem. 76 (2001) 1411-1420
139. Okamoto T., Takeda S., Murayama Y., Ogata E., and Nishimoto I. Ligand-dependent G protein coupling function of amyloid transmembrane precursor. J. Biol. Chem. 270 (1995) 4205-4208
140. Ouimet C.C., Baerwald K.D., Gandy S.E., and Greengard P. Immunocytochemical localization of amyloid precursor protein in rat brain. J. Comp. Neurol. 348 (1994) 244-260
141. Pahlsson P., and Spitalnik S.L. The role of glycosylation in synthesis and secretion of beta-amyloid precursor protein by Chinese hamster ovary cells. Arch. Biochem. Biophys. 331 (1996) 177-186
142. Pangalos M.N., Efthimiopoulos S., Shioi J., and Robakis N.K. The chondroitin sulfate attachment site of appican is formed by splicing out exon 15 of the amyloid precursor gene. J. Biol. Chem. 270 (1995) 10388-10391
143. Pardossi-Piquard R., Petit A., Kawarai T., Sunyach C., Alves da Costa C., Vincent B., Ring S., D'Adamio L., Shen J., Müller U., Hyslop P.S., and Checler F. Presenilin-dependent transcriptional control of the Abeta-degrading enzyme neprilysin by intracellular domains of betaAPP and APLP. Neuron 46 (2005) 541-554
144. Pastorino L., Sun A., Lu P.J., Zhou X.Z., Balastik M., Finn G., Wulf G., Lim J., Li S.H., Li X.J., Xia W.M., Nicholson L.K., and Lu K.P. The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production. Nature 440 (2006) 528-534
145. Patel T.B. Single transmembrane spanning heterotrimeric G protein-coupled receptors and their signaling cascades. Pharmacol. Rev. 56 (2004) 371-385
146. Perez R.G., Zheng H., Van der Ploeg L.H., and Koo E.H. The beta-amyloid precursor protein of Alzheimer's disease enhances neuron viability and modulates neuronal polarity. J. Neurosci. 17 (1997) 9407-9414
147. Pietrzik C.U., Hoffmann J., Stober K., Chen C.Y., Bauer C., Otero D.A.C., Roch J.M., and Herzog V. From differentiation to proliferation: the secretory amyloid precursor protein as a local mediator of growth in thyroid epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 1770-1775
148. Pike C.J., Walencewicz A.J., Glabe C.G., and Cotman C.W. In vitro aging of beta-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res. 563 (1991) 311-314
149. Ponte P., Gonzalez-de Whitt P., Schilling J., Miller J., Hsu D., Greenberg B., Davis K., Wallace W., Lieberburg I., Fuller F., and Cordell B. A new A4-amyloid messenger RNA contains a domain homologous to serine proteinase inhibitors. Nature 331 (1988) 525-527
150. Postina R., Schroeder A., Dewachter I., Bohl J., Schmitt U., Kojro E., Prinzen C., Endres K., Hiemke C., Blessing M., Flamez P., Dequenne A., Godaux E., van Leuven F., and Fahrenholz F. A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model. J. Clin. Invest. 113 (2004) 1456-1464
151. Priller C., Bauer T., Mitteregger G., Krebs B., Kretzschmar H.A., and Herms J. Synapse formation and function is modulated by the amyloid precursor protein. J. Neurosci. 26 (2006) 7212-7221
152. Qahwash I., He W., Tomasselli A., Kletzien R.F., and Yan R. Processing amyloid precursor protein at the beta-site requires proper orientation to be accessed by BACE1. J. Biol. Chem. 279 (2004) 39010-39016
153. Qiu W.Q., Ferreira A., Miller C., Koo E.H., and Selkoe D.J. Cell-surface beta-amyloid precursor protein stimulates neurite outgrowth of hippocampal neurons in an isoform-dependent manner. J. Neurosci. 15 (1995) 2157-2167
154. Quast T., Wehner S., Kirfel G., Jaeger K., De Luca M., and Herzog V. sAPP as a regulator of dendrite motility and melanin release in epidermal melanocytes and melanoma cells. FASEB J. 17 (2003) 1739-1741
155. Ramelot T.A., Gentile L.N., and Nicholson L.K. Transient structure of the amyloid precursor protein cytoplasmic tail indicates preordering of structure for binding to cytosolic factors. Biochemistry 39 (2000) 2714-2725
156. Rassoulzadegan M., Yang Y.H., and Cuzin F. APLP2, a member of the Alzheimer precursor protein family, is required for correct genomic segregation in dividing mouse cells. EMBO J. 17 (1998) 4647-4656
157. Reichmann D., Rahat O., Albeck S., Meged R., Dym O., and Schreiber G. The modular architecture of protein-protein binding interfaces. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 57-62
158. Richards S.J., Hodgman C., and Sharpe M. Reported sequence homology between Alzheimer amyloid(770) and the MRC OX-2 antigen does not predict function. Brain Res. Bull. 38 (1995) 305-306
159. Roberts G.W., Gentleman S.M., Lynch A., and Graham D.I. Beta-A4 amyloid protein deposition in brain after head trauma. Lancet 338 (1991) 1422-1423
160. Rossjohn J., Cappai R., Feil S.C., Henry A., McKinstry W.J., Galatis D., Hesse L., Multhaup G., Beyreuther K., Masters C.L., and Parker M.W. Crystal structure of the N-terminal, growth factor-like domain of Alzheimer amyloid precursor protein. Nat. Struct. Biol. 6 (1999) 327-331
161. Russo C., Salis S., Dolcini V., Venezia V., Song X.H., Teller J.K., and Schettini G. Identification of amino-terminally and phosphotyrosine-modified carboxy-terminal fragments of the amyloid precursor protein in Alzheimer's disease and Down's syndrome brain. Neurobiol. Dis. 8 (2001) 173-180
162. Russo C., Dolcini V., Salis S., Venezia V., Zambrano N., Russo T., and Schettini G. Signal transduction through tyrosine-phosphorylated C-terminal fragments of amyloid precursor protein via an enhanced interaction with Shc/Grb2 adaptor proteins in reactive astrocytes of Alzheimer's disease brain. J. Biol. Chem. 277 (2002) 35282-35288
163. Sabo S.L., Ikin A.F., Buxbaum J.D., and Greengard P. The Alzheimer amyloid precursor protein (APP) and FE65, an APP-binding protein, regulate cell movement. J. Cell Biol. 153 (2001) 1403-1414
164. Sabo S.L., Ikin A.F., Buxbaum J.D., and Greengard P. The amyloid precursor protein and its regulatory protein, FE65, in growth cones and synapses in vitro and in vivo. J. Neurosci. 23 (2003) 5407-5415
165. Saitoh T., Sundsmo M., Roch J.M., Kimura N., Cole G., Schubert D., Oltersdorf T., and Schenk D.B. Secreted form of amyloid beta protein precursor is involved in the growth regulation of fibroblasts. Cell 58 (1989) 615-622
166. Sakurai Y. How do cell assemblies encode information in the brain?. Neurosci. Biobehav. Rev. 23 (1999) 785-796
167. Salbaum J.M., and Ruddle F.H. Embryonic expression pattern of amyloid protein precursor suggests a role in differentiation of specific subsets of neurons. J. Exp. Zool. 269 (1994) 116-127
168. Sandbrink R., Masters C.L., and Beyreuther K. Similar alternative splicing of a non-homologous domain in betaA4-amyloid protein precursor-like proteins. J. Biol. Chem. 269 (1994) 14227-14234
169. Schaefer A.W., Kamei Y., Kamiguchi H., Wong E.V., Rapoport I., Kirchhausen T., Beach C.M., Landreth G., Lemmon S.K., and Lemmon V. L1 endocytosis is controlled by a phosphorylation-dephosphorylation cycle stimulated by outside-in signaling by L1. J. Cell Biol. 157 (2002) 1223-1232
170. Scheuermann S., Hambsch B., Hesse L., Stumm J., Schmidt C., Beher D., Bayer T.A., Beyreuther K., and Multhaup G. Homodimerization of amyloid precursor protein and its implication in the amyloidogenic pathway of Alzheimer's disease. J. Biol. Chem. 276 (2001) 33923-33929
171. Schubert D., Lacorbiere M., Saitoh T., and Cole G. Characterization of an amyloid beta precursor protein that binds heparin and contains tyrosine sulfate. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 2066-2069
172. Selkoe D.J. Clearing the brain's amyloid cobwebs. Neuron 32 (2001) 177-180
173. Sester M., Feuerbach D., Frank R., Preckel T., Gutermann A., and Burgert H.G. The amyloid precursor-like protein 2 associates with the major histocompatibility complex class I molecule K-d. J. Biol. Chem. 275 (2000) 3645-3654
174. Sisodia S.S., Koo E.H., Hoffman P.N., Perry G., and Price D.L. Identification and transport of full-length amyloid precursor proteins in rat peripheral nervous system. J. Neurosci. 13 (1993) 3136-3142
175. Small D.H., Nurcombe V., Reed G., Clarris H., Moir R., Beyreuther K., and Masters C.L. A heparin-binding domain in the amyloid protein precursor of Alzheimer's disease is involved in the regulation of neurite outgrowth. J. Neurosci. 14 (1994) 2117-2127
176. Smith-Swintosky V.L., Pettigrew L.C., Craddock S.D., Culwell A.R., Rydel R.E., and Mattson M.P. Secreted forms of beta-amyloid precursor protein protect against ischemic brain injury. J. Neurochem. 63 (1994) 781-784
177. Soba P., Eggert S., Wagner K., Zentgraf H., Siehl K., Kreger S., Lower A., Langer A., Merdes G., Paro R., Masters C.L., Muller U., Kins S., and Beyreuther K. Homo- and heterodimerization of APP family members promotes intercellular adhesion. EMBO J. 24 (2005) 3624-3634
178. Sondag C.M., and Combs C.K. Amyloid precursor protein cross-linking stimulates beta amyloid production and pro-inflammatory cytokine release in monocytic lineage cells. J. Neurochem. 97 (2006) 449-461
179. Sprecher C.A., Grant F.J., Grimm G., O'Hara P.J., Norris F., Norris K., and Foster D.C. Molecular cloning of the cDNA for a human amyloid precursor protein homolog: evidence for a multigene family. Biochemistry 32 (1993) 4481-4486
180. Storey E., Katz M., Brickman Y., Beyreuther K., and Masters C.L. Amyloid precursor protein of Alzheimer's disease: evidence for a stable, full-length, trans-membrane pool in primary neuronal cultures. Eur. J. Neurosci. 11 (1999) 1779-1788
181. Strittmatter W.J., Saunders A.M., Schmechel D., Pericak-Vance M., Enghild J., Salvesen G.S., and Roses A.D. Apolipoprotein E-high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 1977-1981
182. 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. Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 8098-8102
183. Struhl G., and Adachi A. Requirements for presenilin-dependent cleavage of notch and other transmembrane proteins. Mol. Cell 6 (2000) 625-636
184. Suzuki N., Cheung T.T., Cai X.D., Odaka A., Otvos L., Eckman C., Golde T.E., and Younkin S.G. An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta-APP(717)) mutants. Science 264 (1994) 1336-1340
185. Svergun D.I., Petoukhov M.V., and Koch M.H.J. Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80 (2001) 2946-2953
186. 0 alpha in an identified population of migratory neurons. Dev. Biol. 288 (2005) 160-178
187. Szepanski S., Veit M., Pleschka S., Klenk H.D., Schmidt M.F.G., and Herrler G. Posttranslational folding of the influenza C virus glycoprotein HEF-defective processing in cells expressing the cloned gene. J. Gen. Virol. 75 (1994) 1023-1030
188. Tanzi R.E., McClatchey A.I., Lamperti E.D., Villakomaroff L., Gusella J.F., and Neve R.L. Protease inhibitor domain encoded by an amyloid protein precursor messenger RNA associated with Alzheimer's disease. Nature 331 (1988) 528-530
189. Toledo-Rodriguez M., Blumenfeld B., Wu C.Z., Luo J.Y., Attali B., Goodman P., and Markram H. Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex. Cereb. Cortex 14 (2004) 1310-1327
190. Tolia A., Chavez-Gutierrez L., and De Strooper B. Contribution of presenilin transmembrane domains 6 and 7 to a water-containing cavity in the gamma-secretase complex. J. Biol. Chem. 281 (2006) 27633-27642
191. Tominaga-Yoshino K., Uetsuki T., Yoshikawa K., and Ogura A. Neurotoxic and neuroprotective effects of glutamate are enhanced by introduction of amyloid precursor protein cDNA. Brain Res. 918 (2001) 121-130
192. Trapp B.D., and Hauer P.E. Amyloid precursor protein is enriched in radial glia-implications for neuronal development. J. Neurosci. Res. 37 (1994) 538-550
193. Turner P.R., O'Connor K., Tate W.P., and Abraham W.C. Roles of amyloid precursor protein and its fragments in regulating neural activity, plasticity and memory. Prog. Neurobiol. 70 (2003) 1-32
194. Van Nostrand W.E. Zinc(II) selectively enhances the inhibition of coagulation factor XIa by protease nexin-2/amyloid beta-protein precursor. Thromb. Res. 78 (1995) 43-53
195. Van Nostrand W.E., Schmaier A.H., Farrow J.S., and Cunningham D.D. Protease nexin-II (amyloid beta-protein precursor): a platelet alpha-granule protein. Science 248 (1990) 745-748
196. Van Nostrand W.E., Melchor J.P., Keane D.M., Saporito-Irwin S.M., Romanov G., Davis J., and Xu F. Localization of a fibrillar amyloid beta-protein binding domain on its precursor. J. Biol. Chem. 277 (2002) 36392-36398
197. Vassar R. Beta-secretase (BACE) as a drug target for Alzheimer's disease. Adv. Drug Deliv. Rev. 54 (2002) 1589-1602
198. Wagner S.L., Siegel R.S., Vedvick T.S., Raschke W.C., and Van Nostrand W.E. High-level expression, purification, and characterization of the Kunitz-type protease inhibitor domain of protease nexin-2/amyloid beta protein precursor. Biochem. Biophys. Res. Commun. 186 (1992) 1138-1145
199. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., and Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416 (2002) 535-539
200. Walsh D.M., Fadeeva J.V., LaVoie M.J., Paliga K., Eggert S., Kimberly W.T., Wasco W., and Selkoe D.J. Gamma-secretase cleavage and binding to FE65 regulate the nuclear translocation of the intracellular C-terminal domain (ICD) of the APP family of proteins. Biochemistry 42 (2003) 6664-6673
201. Wang Y., and Ha Y. The X-ray structure of an antiparallel dimer of the human amyloid precursor protein E2 domain. Mol. Cell 15 (2004) 343-353
202. Wang H.W., Pasternak J.F., Kuo H., Ristic H., Lambert M.P., Chromy B., Viola K.L., Klein W.L., Stine W.B., Krafft G.A., and Trommer B.L. Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res. 924 (2002) 133-140
203. Wang P., Yang G., Mosier D.R., Chang P., Zaidi T., Gong Y.D., Zhao N.M., Dominguez B., Lee K.F., Gan W.B., and Zheng H. Defective neuromuscular synapses in mice lacking amyloid precursor protein (APP) and APP-like protein 2. J. Neurosci. 25 (2005) 1219-1225
204. Wasco W., Bupp K., Magendantz M., Gusella J.F., Tanzi R.E., and Solomon F. Identification of a mouse brain cDNA that encodes a protein related to the Alzheimer disease-associated amyloid-beta protein precursor. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 10758-10762
205. Wasco W., Gurubhagavatula S., Dparadis M., Romano D.M., Sisodia S.S., Hyman B.T., Neve R.L., and Tanzi R.E. Isolation and characterization of APLP2 encoding a homolog of the Alzheimer's associated amyloid beta-protein precursor. Nat. Genet. 5 (1993) 95-100
206. Washbourne P., Dityatev A., Scheiffele P., Biederer T., Weiner J.A., Christopherson K.S., and El-Husseini A. Cell adhesion molecules in synapse formation. J. Neurosci. 24 (2004) 9244-9249
207. Weber G. Protein Interactions (1992), Chapman & Hall, New York
208. Yankner B.A., Duffy L.K., and Kirschner D.A. Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. Science 250 (1990) 279-282
209. Williamson T.G., Mok S.S., Henry A., Cappai R., Lander A.D., Nurcombe V., Beyreuther K., Masters C.L., and Small D.H. Secreted glypican binds to the amyloid precursor protein of Alzheimer's disease (APP) and inhibits APP-induced neurite outgrowth. J. Biol. Chem. 271 (1996) 31215-31221
210. Wilson C.A., Doms R.W., Zheng H., and Lee V.M.-Y. Presenilins are not required for Abeta42 production in the early secretory pathway. Nat. Neurosci. 5 (2002) 849-855
211. Wolfe M.S., Xia W., Ostaszewski B.L., Diehl T.S., Kimberly W.T., and Selkoe D.J. Two transmembrane aspartates in presenilin 1 required for presenilin endoproteolysis and gamma secretase activity. Nature 398 (1999) 513-517
212. Wootton J.C., and Federhen S. Analysis of compositionally biased regions in sequence databases. Methods Enzymol. 266 (1996) 554-571
213. Wright P.E., and Dyson H.J. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293 (1999) 321-331
214. Yamatsuji T., Matsui T., Okamoto T., Komatsuzaki K., Takeda S., Fukumoto H., Iwatsubo T., Suzuki N., Asami-Odaka A., Ireland S., Kinane T.B., Giambarella U., and Nishimoto I. G protein-mediated neuronal DNA fragmentation induced by familial Alzheimer's disease-associated mutants of APP. Science 272 (1996) 1349-1352
215. Yamatsuji T., Okamoto T., Takeda S., Murayama Y., Tanaka N., and Nishimoto I. Expression of V642 APP mutant causes cellular apoptosis as Alzheimer trait-linked phenotype. EMBO J. 15 (1996) 498-509
216. Yamazaki T., Selkoe D.J., and Koo E.H. Trafficking of cell-surface beta-amyloid precursor protein-retrograde and transcytotic transport in cultured neurons. J. Cell Biol. 129 (1995) 431-442
217. Yang G., Gong Y.D., Gong K., Jiang W.L., Kwon E., Wang P., Zheng H., Zhang X.F., Gan W.B., and Zhao N.M. Reduced synaptic vesicle density and active zone size in mice lacking amyloid precursor protein (APP) and APP-like protein 2. Neurosci. Lett. 384 (2005) 66-71
218. Yoshikai S., Sasaki H., Doh-ura K., Furuya H., and Sakaki Y. Genomic organization of the human amyloid beta-protein precursor gene. Gene 87 (1990) 257-263
219. Yoshikai S., Sasaki H., Doh-ura K., Furuya H., and Sakaki Y. Genomic organization of the human-amyloid beta-protein precursor gene. Gene 102 (1991) 291-292
220. Zambrano N., Bruni P., Minopoli G., Mosca R., Molino D., Russo C., Schettini G., Sudol M., and Russo T. The beta-amyloid precursor protein APP is tyrosine-phosphorylated in cells expressing a constitutively active form of the Abl protooncogene. J. Biol. Chem. 276 (2001) 19787-19792
221. Zhang Y., Scandura J.M., Van Nostrand W.E., and Walsh P.N. The mechanism by which heparin promotes the inhibition of coagulation factor XIa by protease nexin-2. J. Biol. Chem. 272 (1997) 26139-26144
222. Zheng H., Jiang M., Trumbauer M.E., Sirinathsinghji D.J., 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. Beta-amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81 (1995) 525-531
223. Zhou S., Zhou H., Walian P.J., and Jap B.K. CD147 is a regulatory subunit of the gamma-secretase complex in Alzheimer's disease amyloid beta-peptide production. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 7499-7504