Linking Aβ and Tau in Late-Onset Alzheimer's Disease: A Dual Pathway Hypothesis

Neuron

Volumn 60, Issue 4, 2008, Pages 534-542

  Small, Scott A ^a   Duff, Karen ^a  

^a Columbia University College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN ANTIBODY; AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E; APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; GLYCOGEN SYNTHASE KINASE 3; HOMOTAURINE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; PLACEBO; TARENFLURBIL; TAU PROTEIN;

ALZHEIMER DISEASE; BINDING AFFINITY; CLINICAL FEATURE; CLINICAL TRIAL; DRUG EFFICACY; ENZYME ACTIVITY; EXPERIMENTAL MODEL; HUMAN; IMMUNIZATION; MENINGOENCEPHALITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; ANIMAL; BIOLOGICAL MODEL; BRAIN; GENETIC PREDISPOSITION; GENETICS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; SENILE PLAQUE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; APOLIPOPROTEIN E4; BRAIN; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MODELS, NEUROLOGICAL; PHOSPHORYLATION; SENILE PLAQUES; TAU PROTEINS;

EID: 56349119351     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2008.11.007     Document Type: Review

References (110)

1. Aisen P.S. Tarenflurbil: a shot on goal. Lancet Neurol. 7 (2008) 468-469
2. Aisen P.S., Gauthier S., Vellas B., Briand R., Saumier D., Laurin J., and Garceau D. Alzhemed: a potential treatment for Alzheimer's disease. Curr. Alzheimer Res. 4 (2007) 473-478
3. Andersen O.M., Reiche J., Schmidt V., Gotthardt M., Spoelgen R., Behlke J., von Arnim C.A., Breiderhoff T., Jansen P., Wu X., et al. Neuronal sorting protein-related receptor sorLA/LR11 regulates processing of the amyloid precursor protein. Proc. Natl. Acad. Sci. USA 102 (2005) 13461-13466
4. Asuni A.A., Hooper C., Reynolds C.H., Lovestone S., Anderton B.H., and Killick R. GSK3alpha exhibits beta-catenin and tau directed kinase activities that are modulated by Wnt. Eur. J. Neurosci. 24 (2006) 3387-3392
5. Bales K.R., Dodart J.C., DeMattos R.B., Holtzman D.M., and Paul S.M. Apolipoprotein E, amyloid, and Alzheimer disease. Mol. Interv. 2 (2002) 363-375 339
6. Beisiegel U., Weber W., Ihrke G., Herz J., and Stanley K.K. The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature 341 (1989) 162-164
7. Belenkaya T.Y., Wu Y., Tang X., Zhou B., Cheng L., Sharma Y.V., Yan D., Selva E.M., and Lin X. The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev. Cell 14 (2008) 120-131
8. Bertram L., Mullin K., Parkinson M., Hsiao M., Moscarillo T.J., Wagner S.L., Becker K.D., Velicelebi G., Blacker D., and Tanzi R.E. Is alpha-T catenin (VR22) an Alzheimer's disease risk gene?. J. Med. Genet. 44 (2007) e63
9. Bi X., Yong A.P., Zhou J., Ribak C.E., and Lynch G. Rapid induction of intraneuronal neurofibrillary tangles in apolipoprotein E-deficient mice. Proc. Natl. Acad. Sci. USA 98 (2001) 8832-8837
10. Braak H., and Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82 (1991) 239-259
11. Braak H., Alafuzoff I., Arzberger T., Kretzschmar H., and Del Tredici K. Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 112 (2006) 389-404
12. Brecht W.J., Harris F.M., Chang S., Tesseur I., Yu G.Q., Xu Q., Dee Fish J., Wyss-Coray T., Buttini M., Mucke L., et al. Neuron-specific apolipoprotein e4 proteolysis is associated with increased tau phosphorylation in brains of transgenic mice. J. Neurosci. 24 (2004) 2527-2534
13. Buxbaum J.D., Thinakaran G., Koliatsos V., O'Callahan J., Slunt H.H., Price D.L., and Sisodia S.S. Alzheimer amyloid protein precursor in the rat hippocampus: transport and processing through the perforant path. J. Neurosci. 18 (1998) 9629-9637
14. Caruso A., Motolese M., Iacovelli L., Caraci F., Copani A., Nicoletti F., Terstappen G.C., Gaviraghi G., and Caricasole A. Inhibition of the canonical Wnt signaling pathway by apolipoprotein E4 in PC12 cells. J. Neurochem. 98 (2006) 364-371
15. Cedazo-Minguez A., Popescu B.O., Blanco-Millan J.M., Akterin S., Pei J.J., Winblad B., and Cowburn R.F. Apolipoprotein E and beta-amyloid (1-42) regulation of glycogen synthase kinase-3beta. J. Neurochem. 87 (2003) 1152-1164
16. Chacon M.A., Varela-Nallar L., and Inestrosa N.C. Frizzled-1 is involved in the neuroprotective effect of Wnt3a against Abeta oligomers. J. Cell. Physiol. 217 (2008) 215-227
17. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., and Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261 (1993) 921-923
18. Coudreuse D.Y., Roel G., Betist M.C., Destree O., and Korswagen H.C. Wnt gradient formation requires retromer function in Wnt-producing cells. Science 312 (2006) 921-924
19. De Ferrari G.V., and Moon R.T. The ups and downs of Wnt signaling in prevalent neurological disorders. Oncogene 25 (2006) 7545-7553
20. De Ferrari G.V., Papassotiropoulos A., Biechele T., Wavrant De-Vrieze F., Avila M.E., Major M.B., Myers A., Saez K., Henriquez J.P., Zhao A., et al. Common genetic variation within the low-density lipoprotein receptor-related protein 6 and late-onset Alzheimer's disease. Proc. Natl. Acad. Sci. USA 104 (2007) 9434-9439
21. DeMattos R.B., Cirrito J.R., Parsadanian M., May P.C., O'Dell M.A., Taylor J.W., Harmony J.A., Aronow B.J., Bales K.R., Paul S.M., and Holtzman D.M. ApoE and clusterin cooperatively suppress Abeta levels and deposition: evidence that ApoE regulates extracellular Abeta metabolism in vivo. Neuron 41 (2004) 193-202
22. Dodart J.C., Marr R.A., Koistinaho M., Gregersen B.M., Malkani S., Verma I.M., and Paul S.M. Gene delivery of human apolipoprotein E alters brain Abeta burden in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. USA 102 (2005) 1211-1216
23. Duff K. Transgenic mouse models of Alzheimer's disease: phenotype and mechanisms of pathogenesis. Biochem. Soc. Symp. 67 (2001) 195-202
24. Eaton S. Retromer retrieves wntless. Dev. Cell 14 (2008) 4-6
25. Engel T., Hernandez F., Avila J., and Lucas J.J. Full reversal of Alzheimer's disease-like phenotype in a mouse model with conditional overexpression of glycogen synthase kinase-3. J. Neurosci. 26 (2006) 5083-5090
26. Fagan A.M., Watson M., Parsadanian M., Bales K.R., Paul S.M., and Holtzman D.M. Human and murine ApoE markedly alters A beta metabolism before and after plaque formation in a mouse model of Alzheimer's disease. Neurobiol. Dis. 9 (2002) 305-318
27. Franch-Marro X., Wendler F., Guidato S., Griffith J., Baena-Lopez A., Itasaki N., Maurice M.M., and Vincent J.P. Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat. Cell Biol. 10 (2008) 170-177
28. Galasko D., Chang L., Motter R., Clark C.M., Kaye J., Knopman D., Thomas R., Kholodenko D., Schenk D., Lieberburg I., et al. High cerebrospinal fluid tau and low amyloid beta42 levels in the clinical diagnosis of Alzheimer disease and relation to apolipoprotein E genotype. Arch. Neurol. 55 (1998) 937-945
29. Genis L., Chen Y., Shohami E., and Michaelson D.M. Tau hyperphosphorylation in apolipoprotein E-deficient and control mice after closed head injury. J. Neurosci. Res. 60 (2000) 559-564
30. George A., Leahy H., Zhou J., and Morin P.J. The vacuolar-ATPase inhibitor bafilomycin and mutant VPS35 inhibit canonical Wnt signaling. Neurobiol. Dis. 26 (2007) 125-133
31. Geschwind D.H. Tau phosphorylation, tangles, and neurodegeneration: the chicken or the egg?. Neuron 40 (2003) 457-460
32. Ghebremedhin E., Schultz C., Braak E., and Braak H. High frequency of apolipoprotein E epsilon4 allele in young individuals with very mild Alzheimer's disease-related neurofibrillary changes. Exp. Neurol. 153 (1998) 152-155
33. Gibb G.M., Pearce J., Betts J.C., Lovestone S., Hoffmann M.M., Maerz W., Blackstock W.P., and Anderton B.H. Differential effects of apolipoprotein E isoforms on phosphorylation at specific sites on tau by glycogen synthase kinase-3 beta identified by nano-electrospray mass spectrometry. FEBS Lett. 485 (2000) 99-103
34. Glenner G.G., and Wong C.W. Alzheimer's disease and Down's syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem. Biophys. Res. Commun. 122 (1984) 1131-1135
35. Glodzik-Sobanska L., Pirraglia E., Brys M., de Santi S., Mosconi L., Rich K.E., Switalski R., Louis L.S., Sadowski M.J., Martiniuk F., et al. The effects of normal aging and ApoE genotype on the levels of CSF biomarkers for Alzheimer's disease. Neurobiol. Aging (2007) 10.1016/j.neurobiolaging.2007.08.019 in press. Published online October 7, 2007
36. 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
37. Golombowski S., Muller-Spahn F., Romig H., Mendla K., and Hock C. Dependence of cerebrospinal fluid Tau protein levels on apolipoprotein E4 allele frequency in patients with Alzheimer's disease. Neurosci. Lett. 225 (1997) 213-215
38. Grundke-Iqbal I., Iqbal K., Quinlan M., Tung Y.C., Zaidi M.S., and Wisniewski H.M. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J. Biol. Chem. 261 (1986) 6084-6089
39. Haft C.R., de la Luz Sierra M., Bafford R., Lesniak M.A., Barr V.A., and Taylor S.I. Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Mol. Biol. Cell 11 (2000) 4105-4116
40. Hardy J., and Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297 (2002) 353-356
41. Harris F.M., Brecht W.J., Xu Q., Tesseur I., Kekonius L., Wyss-Coray T., Fish J.D., Masliah E., Hopkins P.C., Scearce-Levie K., et al. Carboxyl-terminal-truncated apolipoprotein E4 causes Alzheimer's disease-like neurodegeneration and behavioral deficits in transgenic mice. Proc. Natl. Acad. Sci. USA 100 (2003) 10966-10971
42. Harris F.M., Brecht W.J., Xu Q., Mahley R.W., and Huang Y. Increased tau phosphorylation in apolipoprotein E4 transgenic mice is associated with activation of extracellular signal-regulated kinase: modulation by zinc. J. Biol. Chem. 279 (2004) 44795-44801
43. Hausmann G., Banziger C., and Basler K. Helping Wingless take flight: how WNT proteins are secreted. Nat. Rev. Mol. Cell Biol. 8 (2007) 331-336
44. Hernandez F., Borrell J., Guaza C., Avila J., and Lucas J.J. Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J. Neurochem. 83 (2002) 1529-1533
45. Herz J., and Bock H.H. Lipoprotein receptors in the nervous system. Annu. Rev. Biochem. 71 (2002) 405-434
46. Hoe H.S., Freeman J., and Rebeck G.W. Apolipoprotein E decreases tau kinases and phospho-tau levels in primary neurons. Mol. Neurodegener. 1 (2006) 18
47. Holmes C., Boche D., Wilkinson D., Yadegarfar G., Hopkins V., Bayer A., Jones R.W., Bullock R., Love S., Neal J.W., et al. Long-term effects of Abeta42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 372 (2008) 216-223
48. Hong M., Chen D.C., Klein P.S., and Lee V.M. Lithium reduces tau phosphorylation by inhibition of glycogen synthase kinase-3. J. Biol. Chem. 272 (1997) 25326-25332
49. Houlden H., Rizzu P., Stevens M., de Knijff P., van Duijn C.M., van Swieten J.C., Heutink P., Perez-Tur J., Thomas V., Baker M., et al. Apolipoprotein E genotype does not affect the age of onset of dementia in families with defined tau mutations. Neurosci. Lett. 260 (1999) 193-195
50. Huang D.Y., Weisgraber K.H., Goedert M., Saunders A.M., Roses A.D., and Strittmatter W.J. ApoE3 binding to tau tandem repeat I is abolished by tau serine262 phosphorylation. Neurosci. Lett. 192 (1995) 209-212
51. Huang Y., Liu X.Q., Wyss-Coray T., Brecht W.J., Sanan D.A., and Mahley R.W. Apolipoprotein E fragments present in Alzheimer's disease brains induce neurofibrillary tangle-like intracellular inclusions in neurons. Proc. Natl. Acad. Sci. USA 98 (2001) 8838-8843
52. Hutton M., Lendon C.L., Rizzu P., Baker M., Froelich S., Houlden H., Pickering-Brown S., Chakraverty S., Isaacs A., Grover A., et al. Association of missense and 5[prime]-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393 (1998) 702-705
53. Irizarry M.C., Cheung B.S., Rebeck G.W., Paul S.M., Bales K.R., and Hyman B.T. Apolipoprotein E affects the amount, form, and anatomical distribution of amyloid beta-peptide deposition in homozygous APP(V717F) transgenic mice. Acta Neuropathol. 100 (2000) 451-458
54. Irizarry M.C., Rebeck G.W., Cheung B., Bales K., Paul S.M., Holzman D., and Hyman B.T. Modulation of A beta deposition in APP transgenic mice by an apolipoprotein E null background. Ann. N Y Acad. Sci. 920 (2000) 171-178
55. Jack Jr. C.R., Dickson D.W., Parisi J.E., Xu Y.C., Cha R.H., O'Brien P.C., Edland S.D., Smith G.E., Boeve B.F., Tangalos E.G., et al. Antemortem MRI findings correlate with hippocampal neuropathology in typical aging and dementia. Neurology 58 (2002) 750-757
56. Jackson G.R., Wiedau-Pazos M., Sang T.K., Wagle N., Brown C.A., Massachi S., and Geschwind D.H. Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 34 (2002) 509-519
57. Kang D.E., Soriano S., Xia X., Eberhart C.G., De Strooper B., Zheng H., and Koo E.H. Presenilin couples the paired phosphorylation of beta-catenin independent of axin: implications for beta-catenin activation in tumorigenesis. Cell 110 (2002) 751-762
58. Kim D.H., Inagaki Y., Suzuki T., Ioka R.X., Yoshioka S.Z., Magoori K., Kang M.J., Cho Y., Nakano A.Z., Liu Q., et al. A new low density lipoprotein receptor related protein, LRP5, is expressed in hepatocytes and adrenal cortex, and recognizes apolipoprotein E. J. Biochem. 124 (1998) 1072-1076
59. Knopman D.S., Parisi J.E., Salviati A., Floriach-Robert M., Boeve B.F., Ivnik R.J., Smith G.E., Dickson D.W., Johnson K.A., Petersen L.E., et al. Neuropathology of cognitively normal elderly. J. Neuropathol. Exp. Neurol. 62 (2003) 1087-1095
60. Koo E.H., and Kopan R. Potential role of presenilin-regulated signaling pathways in sporadic neurodegeneration. Nat. Med. 10 Suppl (2004) S26-S33
61. Lazarov O., Lee M., Peterson D.A., and Sisodia S.S. Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J. Neurosci. 22 (2002) 9785-9793
62. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445 (2007) 168-176
63. 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., et al. Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science 269 (1995) 973-977
64. Liang W.S., Dunckley T., Beach T.G., Grover A., Mastroeni D., Walker D.G., Caselli R.J., Kukull W.A., McKeel D., Morris J.C., et al. Gene expression profiles in anatomically and functionally distinct regions of the normal aged human brain. Physiol. Genomics 28 (2007) 311-322
65. Lovestone S., Hartley C.L., Pearce J., and Anderton B.H. Phosphorylation of tau by glycogen synthase kinase-3 beta in intact mammalian cells: the effects on the organization and stability of microtubules. Neuroscience 73 (1996) 1145-1157
66. Lucas J.J., Hernandez F., Gomez-Ramos P., Moran M.A., Hen R., and Avila J. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J. 20 (2001) 27-39
67. Magdesian M.H., Carvalho M.M., Mendes F.A., Saraiva L.M., Juliano M.A., Juliano L., Garcia-Abreu J., and Ferreira S.T. Amyloid-beta binds to the extracellular cysteine-rich domain of Frizzled and inhibits Wnt/beta-catenin signaling. J. Biol. Chem. 283 (2008) 9359-9368
68. Magoori K., Kang M.J., Ito M.R., Kakuuchi H., Ioka R.X., Kamataki A., Kim D.H., Asaba H., Iwasaki S., Takei Y.A., et al. Severe hypercholesterolemia, impaired fat tolerance, and advanced atherosclerosis in mice lacking both low density lipoprotein receptor-related protein 5 and apolipoprotein E. J. Biol. Chem. 278 (2003) 11331-11336
69. Mateo I., Infante J., Llorca J., Rodriguez E., Berciano J., and Combarros O. Association between glycogen synthase kinase-3beta genetic polymorphism and late-onset Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 21 (2006) 228-232
70. Mercado-Gomez O., Hernandez-Fonseca K., Villavicencio-Queijeiro A., Massieu L., Chimal-Monroy J., and Arias C. Inhibition of Wnt and PI3K signaling modulates GSK-3beta activity and induces morphological changes in cortical neurons: role of tau phosphorylation. Neurochem. Res. 33 (2008) 1599-1609
71. Mi K., Dolan P.J., and Johnson G.V. The low density lipoprotein receptor-related protein 6 interacts with glycogen synthase kinase 3 and attenuates activity. J. Biol. Chem. 281 (2006) 4787-4794
72. Muhammad A., Flores I., Zhang H., Yu R., Staniszewski A., Planel E., Herman M., Ho L., Kreber R., Honig L.S., et al. Retromer deficiency observed in Alzheimer's disease causes hippocampal dysfunction, neurodegeneration, and Abeta accumulation. Proc. Natl. Acad. Sci. USA 105 (2008) 7327-7332
73. Nielsen M.S., Gustafsen C., Madsen P., Nyengaard J.R., Hermey G., Bakke O., Mari M., Schu P., Pohlmann R., Dennes A., and Petersen C.M. Sorting by the cytoplasmic domain of the amyloid precursor protein binding receptor SorLA. Mol. Cell. Biol. 27 (2007) 6842-6851
74. Ohkubo N., Lee Y.D., Morishima A., Terashima T., Kikkawa S., Tohyama M., Sakanaka M., Tanaka J., Maeda N., Vitek M.P., and Mitsuda N. Apolipoprotein E and Reelin ligands modulate tau phosphorylation through an apolipoprotein E receptor/disabled-1/glycogen synthase kinase-3beta cascade. FASEB J. 17 (2003) 295-297
75. Pan C.L., Baum P.D., Gu M., Jorgensen E.M., Clark S.G., and Garriga G. C. elegans AP-2 and retromer control Wnt signaling by regulating mig-14/Wntless. Dev. Cell 14 (2008) 132-139
76. Pastor P., Roe C.M., Villegas A., Bedoya G., Chakraverty S., Garcia G., Tirado V., Norton J., Rios S., Martinez M., et al. Apolipoprotein Eepsilon4 modifies Alzheimer's disease onset in an E280A PS1 kindred. Ann. Neurol. 54 (2003) 163-169
77. Pei J.J., Braak E., Braak H., Grundke-Iqbal I., Iqbal K., Winblad B., and Cowburn R.F. Distribution of active glycogen synthase kinase 3beta (GSK-3beta) in brains staged for Alzheimer disease neurofibrillary changes. J. Neuropathol. Exp. Neurol. 58 (1999) 1010-1019
78. Phiel C.J., Wilson C.A., Lee V.M., and Klein P.S. GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 423 (2003) 435-439
79. Pickering-Brown S.M., Owen F., Isaacs A., Snowden J., Varma A., Neary D., Furlong R., Daniel S.E., Cairns N.J., and Mann D.M. Apolipoprotein E epsilon4 allele has no effect on age at onset or duration of disease in cases of frontotemporal dementia with pick- or microvacuolar-type histology. Exp. Neurol. 163 (2000) 452-456
80. Port F., Kuster M., Herr P., Furger E., Banziger C., Hausmann G., and Basler K. Wingless secretion promotes and requires retromer-dependent cycling of Wntless. Nat. Cell Biol. 10 (2008) 178-185
81. Prasad B.C., and Clark S.G. Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development 133 (2006) 1757-1766
82. Reilly J.F., Games D., Rydel R.E., Freedman S., Schenk D., Young W.G., Morrison J.H., and Bloom F.E. Amyloid deposition in the hippocampus and entorhinal cortex: quantitative analysis of a transgenic mouse model. Proc. Natl. Acad. Sci. USA 100 (2003) 4837-4842
83. Rogaev E.I., Sherrington R., Rogaeva E.A., Levesque G., Ikeda M., Liang Y., Chi H., Lin C., Holman K., Tsuda T., et al. Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature 376 (1995) 775-778
84. Rogaeva E., Meng Y., Lee J.H., Gu Y., Kawarai T., Zou F., Katayama T., Baldwin C.T., Cheng R., Hasegawa H., et al. The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nat. Genet. 39 (2007) 168-177
85. Sager K.L., Wuu J., Leurgans S.E., Rees H.D., Gearing M., Mufson E.J., Levey A.I., and Lah J.J. Neuronal LR11/sorLA expression is reduced in mild cognitive impairment. Ann. Neurol. 62 (2007) 640-647
86. Saunders A.M., Strittmatter W.J., Schmechel D., George-Hyslop P.H., Pericak-Vance M.A., Joo S.H., Rosi B.L., Gusella J.F., Crapper-MacLachlan D.R., Alberts M.J., et al. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology 43 (1993) 1467-1472
87. Scali C., Caraci F., Gianfriddo M., Diodato E., Roncarati R., Pollio G., Gaviraghi G., Copani A., Nicoletti F., Terstappen G.C., and Caricasole A. Inhibition of Wnt signaling, modulation of Tau phosphorylation and induction of neuronal cell death by DKK1. Neurobiol. Dis. 24 (2006) 254-265
88. Schaffer B.A., Bertram L., Miller B.L., Mullin K., Weintraub S., Johnson N., Bigio E.H., Mesulam M., Wiedau-Pazos M., Jackson G.R., et al. Association of GSK3B with Alzheimer disease and frontotemporal dementia. Arch. Neurol. 65 (2008) 1368-1374
89. Scherzer C.R., Offe K., Gearing M., Rees H.D., Fang G., Heilman C.J., Schaller C., Bujo H., Levey A.I., and Lah J.J. Loss of apolipoprotein E receptor LR11 in Alzheimer disease. Arch. Neurol. 61 (2004) 1200-1205
90. Seaman M.N. Recycle your receptors with retromer. Trends Cell Biol. 15 (2005) 68-75
91. Sherrington R., Rogaev E.I., Liang Y., Rogaeva E.A., Levesque G., Ikeda M., Chi H., Lin C., Li G., Holman K., et al. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375 (1995) 754-760
92. Shiurba R.A., Ishiguro K., Takahashi M., Sato K., Spooner E.T., Mercken M., Yoshida R., Wheelock T.R., Yanagawa H., Imahori K., and Nixon R.A. Immunocytochemistry of tau phosphoserine 413 and tau protein kinase I in Alzheimer pathology. Brain Res. 737 (1996) 119-132
93. Small S.A., and Gandy S. Sorting through the cell biology of Alzheimer's disease: intracellular pathways to pathogenesis. Neuron 52 (2006) 15-31
94. Small S.A., Kent K., Pierce A., Leung C., Kang M.S., Okada H., Honig L., Vonsattel J.P., and Kim T.W. Model-guided microarray implicates the retromer complex in Alzheimer's disease. Ann. Neurol. 58 (2005) 909-919
95. Spoelgen R., von Arnim C.A., Thomas A.V., Peltan I.D., Koker M., Deng A., Irizarry M.C., Andersen O.M., Willnow T.E., and Hyman B.T. Interaction of the cytosolic domains of sorLA/LR11 with the amyloid precursor protein (APP) and beta-secretase beta-site APP-cleaving enzyme. J. Neurosci. 26 (2006) 418-428
96. St George-Hyslop P.H., and Morris J.C. Will anti-amyloid therapies work for Alzheimer's disease?. Lancet 372 (2008) 180-182
97. Strittmatter W.J., and Roses A.D. Apolipoprotein E and Alzheimer disease. Proc. Natl. Acad. Sci. USA 92 (1995) 4725-4727
98. Su Y., Ryder J., Li B., Wu X., Fox N., Solenberg P., Brune K., Paul S., Zhou Y., Liu F., and Ni B. Lithium, a common drug for bipolar disorder treatment, regulates amyloid-beta precursor protein processing. Biochemistry 43 (2004) 6899-6908
99. Sunderland T., Mirza N., Putnam K.T., Linker G., Bhupali D., Durham R., Soares H., Kimmel L., Friedman D., Bergeson J., et al. Cerebrospinal fluid beta-amyloid1-42 and tau in control subjects at risk for Alzheimer's disease: the effect of APOE epsilon4 allele. Biol. Psychiatry 56 (2004) 670-676
100. Tanzi R.E., and Bertram L. Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 120 (2005) 545-555
101. Tesseur I., Van Dorpe J., Bruynseels K., Bronfman F., Sciot R., Van Lommel A., and Van Leuven F. Prominent axonopathy and disruption of axonal transport in transgenic mice expressing human apolipoprotein E4 in neurons of brain and spinal cord. Am. J. Pathol. 157 (2000) 1495-1510
102. Tesseur I., Van Dorpe J., Spittaels K., Van den Haute C., Moechars D., and Van Leuven F. Expression of human apolipoprotein E4 in neurons causes hyperphosphorylation of protein tau in the brains of transgenic mice. Am. J. Pathol. 156 (2000) 951-964
103. Tiraboschi P., Hansen L.A., Masliah E., Alford M., Thal L.J., and Corey-Bloom J. Impact of APOE genotype on neuropathologic and neurochemical markers of Alzheimer disease. Neurology 62 (2004) 1977-1983
104. Van Broeckhoven C., Backhovens H., Cruts M., Martin J.J., Crook R., Houlden H., and Hardy J. APOE genotype does not modulate age of onset in families with chromosome 14 encoded Alzheimer's disease. Neurosci. Lett. 169 (1994) 179-180
105. Whitwell J.L., Przybelski S.A., Weigand S.D., Knopman D.S., Boeve B.F., Petersen R.C., and Jack Jr. C.R. 3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer's disease. Brain 130 (2007) 1777-1786
106. Wisniewski T., and Konietzko U. Amyloid-beta immunisation for Alzheimer's disease. Lancet Neurol. 7 (2008) 805-811
107. Woodgett J.R. Judging a protein by more than its name: GSK-3. Sci. STKE 2001 (2001) RE12
108. Yang P.T., Lorenowicz M.J., Silhankova M., Coudreuse D.Y., Betist M.C., and Korswagen H.C. Wnt signaling requires retromer-dependent recycling of MIG-14/Wntless in Wnt-producing cells. Dev. Cell 14 (2008) 140-147
109. Ye S., Huang Y., Mullendorff K., Dong L., Giedt G., Meng E.C., Cohen F.E., Kuntz I.D., Weisgraber K.H., and Mahley R.W. Apolipoprotein (apo) E4 enhances amyloid beta peptide production in cultured neuronal cells: apoE structure as a potential therapeutic target. Proc. Natl. Acad. Sci. USA 102 (2005) 18700-18705
110. Zilberberg A., Yaniv A., and Gazit A. The low density lipoprotein receptor-1, LRP1, interacts with the human frizzled-1 (HFz1) and down-regulates the canonical Wnt signaling pathway. J. Biol. Chem. 279 (2004) 17535-17542