Alzheimer's disease-related loss of pin1 function influences the intracellular localization and the processing of AβPP

Journal of Alzheimer's Disease

Volumn 30, Issue 2, 2012, Pages 277-297

  Pastorino, Lucia ^a   Ma, Suk Ling ^a   Balastik, Martin ^a   Huang, Pengyu ^a   Pandya, Darshan ^a   Nicholson, Linda ^b   Lu, Kun Ping ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Department of Molecular Biology and Genetics   (United States)

Author keywords

Conformation; internalization; phosphorylation; prolyl isomerase

Indexed keywords

AMYLOID PRECURSOR PROTEIN; PEPTIDYLPROLYL ISOMERASE PIN1;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL LINE; CELL MEMBRANE; CONTROLLED STUDY; FEMALE; GENE SILENCING; GENETIC TRANSFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

EID: 84861486615     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-111259     Document Type: Article

References (103)

1. Glenner GG, Wong CW (1984) Alzheimer's disease and Down's syndrome: Sharing of a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun 122, 1131-1135. (Pubitemid 14027629)
2. Goedert M, Spillantini MG, Cairns NJ, Crowther RA (1992) Tau proteins of Alzheimer paired helical filaments: Abnormal phosphorylation of all six brain isoforms. Neuron 8, 159-168.
3. Glenner GG, Wong CW, Quaranta V, Eanes ED (1984) The amyloid deposits in Alzheimer's disease: Their nature and pathogenesis. Appl Pathol 2, 357-369. (Pubitemid 16028900)
4. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356. (Pubitemid 34790756)
5. Thinakaran G, Koo EH (2008) Amyloid precursor protein trafficking, processing, and function. J Biol Chem 283, 29615-29619.
6. Parvathy S, Hussain I, Karran EH, Turner AJ, Hooper NM (1999) Cleavage of Alzheimer's amyloid precursor protein by alpha-secretase occurs at the surface of neuronal cells. Biochemistry 38, 9728-9734.
7. Young-Pearse TL, Chen AC, Chang R, Marquez C, Selkoe DJ (2008) Secreted APP regulates the function of full-length APP in neurite outgrowth through interaction with integrin beta1. Neural Dev 3, 15.
8. Hussain I, Powell D, Howlett DR, Tew DG, Meek TD, Chapman C, Gloger IS, Murphy KE, Southan CD, Ryan DM, Smith TS, Simmons DL, Walsh FS, Dingwall C, Christie G (1999) Identification of a novel aspartic protease (Asp 2) as beta-secretase. Mol Cell Neurosci 14, 419-427. (Pubitemid 30026585)
9. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, Teplow DB, Ross S, Amarante P, Loeloff R, Luo Y, Fisher S, Fuller J, Edenson S, Lile J, Jarosinski MA, Biere AL, Curran E, Burgess T, Louis JC, Collins F, Tre-anor J, Rogers G, Citron M (1999) Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmem-brane aspartic protease BACE. Science 286, 735-741.
10. De Strooper B, Vassar R, Golde T (2010) The secretases: Enzymes with therapeutic potential in Alzheimer disease. Nat Rev Neurol 6, 99-107.
11. Sabo SL, Lanier LM, Ikin AF, Khorkova O, Sahasrabudhe S, Greengard P, Buxbaum JD (1999) Regulation of beta-amyloid secretion by FE65, an amyloid protein precursor-binding protein. J Biol Chem 274, 7952-7957.
12. Ando K, Iijima KI, Elliott JI, Kirino Y, Suzuki T (2001) Phosphorylation-dependent regulation of the interaction of amyloid precursor protein with Fe65 affects the production of beta-amyloid. J Biol Chem 276, 40353-40361.
13. Hutton M, Lewis J, Dickson D, Yen SH, McGowan E (2001) Analysis of tauopathies with transgenic mice. Trends Mol Med 7, 467-470. (Pubitemid 32964162)
14. Lu PJ, Zhou XZ, Shen M, Lu KP (1999) Function of WW domains as phosphoserine-or phosphothreonine-binding modules. Science 283, 1325-1328.
15. Mandelkow EM, Mandelkow E (1998) Tau in Alzheimer's disease. Trends Cell Biol 8, 425-427. (Pubitemid 28529713)
16. Luna-Munoz J, Chavez-Macias L, Garcia-Sierra F, Mena R (2007) Earliest stages of tau conformational changes are related to the appearance of a sequence of specific phospho-dependent tau epitopes in Alzheimer's disease. J Alzheimers Dis 12, 365-375.
17. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 33, 95-130.
18. Mandelkow EM, Drewes G, Biernat J, Gustke N, Van Lint J, Vandenheede JR, Mandelkow E (1992) Glyco-gen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett 314, 315-321. (Pubitemid 23005680)
19. Vincent IJ, Davies P (1992) A protein kinase associated with paired helicalfilamentsinAlzheimer disease. Proc Natl Acad Sci USA 89, 2878-2882.
20. Noble W, Olm V, Takata K, Casey E, Mary O, Meyerson J, Gaynor K, LaFrancois J, Wang L, Kondo T, Davies P, Burns M, Veeranna, Nixon R, Dickson D, Matsuoka Y, Ahlija-nian M, Lau LF, Duff K (2003) Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 38, 555-565. (Pubitemid 36645031)
21. Cruz JC, Tsai LH (2004) Cdk5 deregulation in the patho-genesis of Alzheimer's disease. Trends Mol Med 10, 452-458. (Pubitemid 39209212)
22. Lee MS, Kao SC, Lemere CA, Xia W, Tseng HC, Zhou Y, Neve R, Ahlijanian MK, Tsai LH (2003) APP processing is regulated by cytoplasmic phosphorylation. J Cell Biol 163, 83-95. (Pubitemid 37271436)
23. Cruz JC, Kim D, Moy LY, Dobbin MM, Sun X, Bronson RT, Tsai LH (2006) p25/cyclin-dependent kinase 5 induces production and intraneuronal accumulation of amyloid beta in vivo. J Neurosci 26, 10536-10541. (Pubitemid 44564604)
24. Pastorino L, Lu KP (2006) Pathogenic mechanisms in Alzheimer's disease. Eur J Pharmacol 545, 29-38. (Pubitemid 44215878)
25. Phiel CJ, Wilson CA, Lee VM, Klein PS (2003) GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 423, 435-439. (Pubitemid 36626994)
26. Lu KP, Zhou XZ (2007) The prolyl isomerase PIN1: A pivotal new twistinphosphorylation signalling and disease. Nat Rev Mol Cell Biol 8, 904-916. (Pubitemid 47622559)
27. Liou YC, Sun A, Ryo A, Zhou XZ, Yu ZX, Huang HK, Uchida T, Bronson R, Bing G, Li X, Hunter T, Lu KP (2003) Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature 424, 556-561. (Pubitemid 36975777)
28. Pastorino L, Sun A, Lu PJ, Zhou XZ, Balastik M, Finn G, Wulf G, Lim J, Li SH, Li X, Xia W, Nicholson LK, Lu KP (2006) The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production. Nature 440, 528-534.
29. Lim J, Balastik M, Lee TH, Nakamura K, Liou YC, Sun A, Finn G, Pastorino L, Lee VM, Lu KP (2008) Pin1 has opposite effects on wild-type and P301L tau stability and tauopathy. J Clin Invest 118, 1877-1889. (Pubitemid 351632390)
30. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP (1999) The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature399, 784-788. (Pubitemid 29293174)
31. Zhou XZ, Kops O, Werner A, Lu PJ, Shen M, Stoller G, Küllertz G, Stark M, Fischer G, Lu KP (2000) Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol Cell 6, 873-883.
32. Liou Y-C, Sun A, Ryo A, Zhou XZ, Yu Z-X, Huang H-K, Bronson R, Bing G, Li X, Hunter T, Lu KP (2003) Roleofthe prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature 424, 556-561. (Pubitemid 36975777)
33. Sultana R, Boyd-Kimball D, Poon HF, Cai J, Pierce WM, Klein JB, Markesbery WR, Zhou XZ, Lu KP, Butterfield DA (2006) Oxidative modification and down-regulation of Pin1 in Alzheimer's disease hippocampus: A redox proteomics analysis. Neurobiol Aging 27, 918-925.
34. Butterfield DA, Poon HF, St Clair D, Keller JN, Pierce WM, Klein JB, Markesbery WR (2006) Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: Insights into the development of Alzheimer's disease. Neurobiol Dis 22, 223-232.
35. Wijsman EM, Daw EW, Yu CE, Payami H, Steinbart EJ, Nochlin D, Conlon EM, Bird TD, Schellenberg GD (2004) Evidence for a novel late-onset Alzheimer disease locus on chromosome 19p13. 2. Am J Hum Genet 75, 398-409. (Pubitemid 39095816)
36. Segat L, Pontillo A, Annoni G, Trabattoni D, Vergani C, Clerici M, Arosio B, Crovella S (2007) Pin1 promoter polymorphisms are associated with Alzheimer's disease. Neurobiol Aging 28, 69-74. (Pubitemid 44802916)
37. Arosio B, Segat L, Milanese M, Galimberti L, Calabresi C, Zanetti M, Trabattoni D, Annoni G, Crovella S, Vergani C (2007) PIN-1 promoter polymorphisms in mild cognitive impairment and susceptibility to Alzheimer's disease: A preliminary report. Aging Clin Exp Res 19, 406-409. (Pubitemid 350285300)
38. Ma SL, Tang NLS, Tam CWC, Lui VWC, Lam LCW, Chiu HFK, Driver JA, Pastorino L, Lu KP (2012) A functional polymorphism in Pin1 that prevents its suppression by AP4 is associated with delayed onset of Alzheimer's disease. Neurobiol Aging 33, 804-813.
39. Ramelot TA, Gentile LN, Nicholson LK (2000) Transient structure of the amyloid precursor protein cytoplasmic tail indicates preordering of structure for binding to cytosolic factors. Biochemistry 39, 2714-2725. (Pubitemid 30148926)
40. Ramelot TA, Nicholson LK (2001) Phosphorylation-induced structural changes in the amyloid precursor protein cytoplasmic tail detected by NMR. J Mol Biol 307, 871-884. (Pubitemid 33027665)
41. Akiyama H, Shin RW, Uchida C, Kitamoto T, Uchida T (2005) Pin1 promotes production of Alzheimer's amyloid beta from beta-cleaved amyloid precursor protein. Biochem Biophys Res Commun 336, 521-529. (Pubitemid 41267260)
42. Tamayev R, Zhou D, D'Adamio L (2009) The interactome of the amyloid beta precursor protein family members is shaped by phosphorylation of their intracellular domains. Mol Neurodegener 4, 28.
43. Sano Y, Nakaya T, Pedrini S, Takeda S, Iijima-Ando K, Iijima K, Mathews PM, Itohara S, Gandy S, Suzuki T (2006) Physiological mouse brain Abeta levels are not related to the phosphorylation state of threonine-668 of Alzheimer's APP. PLoS One 1, e51.
44. Liou YC, Ryo A, Huang HK, Lu PJ, Bronson R, Fujimori F, Uchida T, Hunter T, Lu KP (2002) Loss of Pin1 function in the mouse causes phenotypes resembling cyclin D1-null phenotypes. Proc Natl Acad Sci USA 99, 1335-1340. (Pubitemid 34136494)
45. Barbagallo AP, Wang Z, Zheng H, D'Adamio L (2011) The intracellular threonine of amyloid precursor protein that is essential for docking of pin1 is dispensable for developmental function. PLoS One 6, e18006.
46. Pastorino L, Ikin AF, Lamprianou S, Vacaresse N, Revelli JP, Platt K, Paganetti P, Mathews PM, Harroch S, Buxbaum JD (2004) BACE (beta-secretase) modulates the processing of APLP2 in vivo. Mol Cell Neurosci 25, 642-649. (Pubitemid 38481473)
47. Sabo SL, Ikin AF, Buxbaum JD, Greengard P (2001) The Alzheimer amyloid precursor protein (APP) and FE65, an APP-binding protein, regulate cell movement. J Cell Biol 153, 1403-1414. (Pubitemid 34286125)
48. Ikezu T, Trapp BD, Song KS, Schlegel A, Lisanti MP, Okamoto T (1998) Caveolae, plasma membrane microdomains for alpha-secretase-mediated processing of the amyloid precursor protein. J Biol Chem 273, 10485-10495. (Pubitemid 28227659)
49. Lesne S, Ali C, Gabriel C, Croci N, MacKenzie ET, Glabe CG, Plotkine M, Marchand-Verrecchia C, Vivien D, Buisson A (2005) NMDA receptor activation inhibits alpha-secretase and promotes neuronal amyloid-beta production. J Neurosci 25, 9367-9377. (Pubitemid 41464749)
50. Seubert P, Oltersdorf T, Lee MG, Barbour R, Blomquist C, Davis DL, Bryant K, Fritz LC, Galasko D, Thal LJ, et al. (1993) Secretion of beta-amyloid precursor protein cleaved at the amino terminus of the beta-amyloid peptide. Nature 361, 260-263. (Pubitemid 23034476)
51. Yamazaki T, Koo EH, Selkoe DJ (1996) Trafficking of cell-surface amyloid beta-protein precursor. II. Endocytosis, recycling and lysosomal targeting detectedbyimmunolocal-ization. J Cell Sci 109 (Pt 5), 999-1008. (Pubitemid 126477168)
52. Daniels GM, Amara SG (1998) Selective labeling of neuro-transmitter transporters atthe cell surface. Methods Enzymol 296, 307-318. (Pubitemid 28455029)
53. Huh KH, Wenthold RJ (1999) Turnover analysis of glu-tamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J Biol Chem 274, 151-157. (Pubitemid 29035042)
54. Pastorino L, Ikin AF, Nairn AC, Pursnani A, Buxbaum JD (2002) The carboxyl-terminus of BACE contains a sorting signal that regulates BACE trafficking but not the formation of total A (beta). Mol Cell Neurosci 19, 175-185. (Pubitemid 34211898)
55. Lichtenthaler SF (2011) Alpha-secretase in Alzheimer's disease: Molecular identity, regulation and therapeutic potential. J Neurochem 116, 10-21.
56. Buxbaum JD, Liu KN, Luo Y, Slack JL, Stocking KL, Peschon JJ, Johnson RS, Castner BJ, Cerretti DP, Black RA (1998) Evidence that tumor necrosis factor alpha converting enzyme is involved in regulated alpha-secretase cleavage of the Alzheimer amyloid protein precursor. J Biol Chem 273, 27765-27767. (Pubitemid 28496060)
57. Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, Wolfson MF, Castner BJ, Stocking KL, Reddy P, Srinivasan S, Nelson N, Boiani N, Schooley KA, Gerhart M, Davis R, Fitzner JN, Johnson RS, Paxton RJ, March CJ, Cerretti DP (1997) A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385, 729-733. (Pubitemid 27098094)
58. McCulloch DR, Akl P, Samaratunga H, Herington AC, Odorico DM (2004) Expression of the disintegrin metallo-protease, ADAM-10, in prostate cancer and its regulation by dihydrotestosterone, insulin-like growth factor I, and epidermal growth factor in the prostate cancer cell model LNCaP. Clin Cancer Res 10, 314-323. (Pubitemid 38114194)
59. Dallas DJ, Genever PG, Patton AJ, Millichip MI, McKie N, Skerry TM (1999) Localization of ADAM10 and Notch receptors in bone. Bone 25, 9-15. (Pubitemid 29322055)
60. Schlondorff J, Becherer JD, Blobel CP (2000) Intracellular maturation and localization of the tumour necrosis factor alpha convertase (TACE). Biochem J 347 (Pt 1), 131-138. (Pubitemid 30199050)
61. Nakano A, Koinuma D, Miyazawa K, Uchida T, Saitoh M, Kawabata M, Hanai J, Akiyama H, Abe M, Miyazono K, Matsumoto T, Imamura T (2009) Pin1 down-regulates transforming growth factor-beta (TGF-beta) signaling by inducing degradation of Smad proteins. J Biol Chem 284, 6109-6115.
62. Ma SL, Pastorino L, Zhou XZ, Lu KP (2011) Propyl iso-merase Pin1 promotes APP protein turnover by inhibiting GSK3beta kinase activity: A novel mechanism for Pin1 to protect against Alzheimer's disease. J Biol Chem, 287, 6969-6973.
63. Walter J, Fluhrer R, Hartung B, Willem M, Kaether C, Capell A, Lammich S, Multhaup G, Haass C (2001) Phosphoryla-tion regulates intracellular trafficking of beta-secretase. J Biol Chem 276, 14634-14641.
64. Zou L, Wang Z, Shen L, Bao GB, Wang T, Kang JH, Pei G (2007) Receptor tyrosine kinases positively regulate BACE activity and Amyloid-beta production through enhancing BACE internalization. Cell Res 17, 389-401. (Pubitemid 46763090)
65. Yu L, Mohamed AJ, Vargas L, Berglof A, Finn G, Lu KP, Smith CI (2006) Regulation of Bruton tyrosine kinase by the peptidylprolyl isomerase Pin1. J Biol Chem 281, 18201-18207. (Pubitemid 44035620)
66. Lam PB, Burga LN, Wu BP, Hofstatter EW, Lu KP, Wulf GM (2008) Prolyl isomerase Pin1 is highly expressed in Her2-positive breast cancer and regulates erbB2 protein stability. Mol Cancer 7, 91.
67. Khanal P, Namgoong GM, Kang BS, Woo ER, Choi HS (2010) The prolyl isomerase Pin1 enhances HER-2 expression and cellular transformation via its interaction with mitogen-activated protein kinase/extracellular signal-regulated kinase kinase 1. Mol Cancer Ther 9, 606-616.
68. Lu PJ, Zhou XZ, Liou YC, Noel JP, Lu KP (2002) Critical role of WW domain phosphorylation in regulating phosphoserine binding activity and Pin1 function. J Biol Chem 277, 2381-2384. (Pubitemid 34953258)
69. Carey RM, Balcz BA, Lopez-Coviella I, Slack BE (2005) Inhibition of dynamin-dependent endocytosis increases shedding of the amyloid precursor protein ectodomain and reduces generation of amyloid beta protein. BMC Cell Biol 6, 30.
70. Lorenzen A, Samosh J, Vandewark K, Anborgh PH, Seah C, Magalhaes AC, Cregan SP, Ferguson SS, Pasternak SH (2010) Rapid and direct transport of cell surface APP to the lysosome defines anovel selective pathway. Mol Brain3, 11.
71. Vingtdeux V, Hamdane M, Loyens A, Gele P, Drobeck H, Begard S, Galas MC, Delacourte A, Beauvillain JC, Buee L, Sergeant N (2007) Alkalizing drugs induce accumulation of amyloid precursor protein by-products in luminal vesicles of multivesicular bodies. J Biol Chem 282, 18197-18205. (Pubitemid 47100204)
72. Koo EH, Squazzo SL (1994) Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J Biol Chem 269, 17386-17389. (Pubitemid 24218009)
73. Sabo S (2002) Cytosolic protein-protein interactions that regulate the amyloid precursor protein. Drug Devel Res 56, 228-241. (Pubitemid 35014945)
74. Minopoli G, de Candia P, Bonetti A, Faraonio R, Zambrano N, Russo T (2001) The beta-amyloid precursor protein functions as a cytosolic anchoring site that prevents Fe65 nuclear translocation. J Biol Chem 276, 6545-6550. (Pubitemid 37373518)
75. Zambrano N, Buxbaum JD, Minopoli G, Fiore F, De Candia P, De Renzis S, Faraonio R, Sabo S, Cheetham J, Sudol M, Russo T (1997) Interaction of the phosphotyrosine interac-tion/phosphotyrosine binding-related domains of Fe65 with wild-type and mutant Alzheimer's beta-amyloid precursor proteins. J Biol Chem 272, 6399-6405. (Pubitemid 27118118)
76. Borg JP, Ooi J, Levy E, Margolis B (1996) The phosphoty-rosine interaction domains of X11 and FE65 bind to distinct sites on the YENPTY motif of amyloid precursor protein. Mol Cell Biol 16, 6229-6241. (Pubitemid 26360983)
77. King GD, Scott Turner R (2004) Adaptor protein interactions: Modulators of amyloid precursor protein metabolism and Alzheimer's disease risk? Exp Neurol 185, 208-219. (Pubitemid 38084847)
78. Zhou D, Zambrano N, Russo T, D'Adamio L (2009) Phosphorylation of a tyrosine in the amyloid-beta protein precursor intracellular domain inhibits Fe65 binding and signaling. J Alzheimers Dis 16, 301-307.
79. Radzimanowski J, Simon B, Sattler M, Beyreuther K, Sinning I, Wild K (2008) Structureofthe intracellular domain of the amyloid precursor protein in complex with Fe65-PTB2. EMBO Rep 9, 1134-1140.
80. Maltese WA, Wilson S, Tan Y, Suomensaari S, Sinha S, Barbour R, McConlogue L (2001) Retention of the Alzheimer's amyloid precursor fragment C99 in the endoplasmic retic-ulum prevents formation of amyloid beta-peptide. J Biol Chem 276, 20267-20279.
81. Wiley JC, Smith EA, Hudson MP, Ladiges WC, Bothwell M (2007) Fe65 stimulates proteolytic liberation of the beta-amyloid precursor protein intracellular domain. J Biol Chem 282, 33313-33325. (Pubitemid 350159549)
82. Cao X, Sudhof TC (2001) A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293, 115-120. (Pubitemid 32625507)
83. Cao X, Sudhof TC (2004) Dissection of amyloid-beta precursor protein-dependent transcriptional transactivation. J Biol Chem 279, 24601-24611. (Pubitemid 38725327)
84. Leissring MA, Murphy MP, Mead TR, Akbari Y, Sugar-man MC, Jannatipour M, Anliker B, Muller U, Saftig P, De Strooper B, Wolfe MS, Golde TE, LaFerla FM (2002) A physiologic signaling role for the gamma-secretase-derived intracellular fragment of APP. Proc Natl Acad Sci USA 99, 4697-4702. (Pubitemid 34286047)
85. vonRotz RC, Kohli BM, Bosset J, Meier M, Suzuki T, Nitsch RM, Konietzko U (2004) The APP intracellular domain forms nuclear multiprotein complexes and regulates the transcription of its own precursor. J Cell Sci 117, 4435-4448. (Pubitemid 39360070)
86. Pardossi-Piquard R, Petit A, Kawarai T, Sunyach C, Alves da Costa C, Vincent B, Ring S, D'Adamio L, Shen J, Muller U, St George Hyslop P, Checler F (2005) Presenilin-dependent transcriptional control of the Abeta-degrading enzyme neprilysin by intracellular domains of betaAPP and APLP. Neuron 46, 541-554. (Pubitemid 40797380)
87. Kimberly WT, Zheng JB, Town T, Flavell RA, Selkoe DJ (2005) Physiological regulation of the beta-amyloid precursor protein signaling domain by c-Jun N-terminal kinase JNK3 during neuronal differentiation. J Neurosci 25, 5533-5543. (Pubitemid 40800645)
88. Ghosal K, Vogt DL, Liang M, Shen Y, Lamb BT, Pimplikar SW (2009) Alzheimer's disease-like pathological features in transgenic mice expressing the APP intracellular domain. Proc Natl Acad Sci USA 106, 18367-18372.
89. Giliberto L, Zhou D, Weldon R, Tamagno E, De Luca P, Tabaton M, D'Adamio L (2008) Evidence that the Amyloid beta Precursor Protein-intracellular domain lowers the stress threshold of neurons and has a "regulated" transcriptional role. Mol Neurodegener 3, 12.
90. Walsh DM, Fadeeva JV, LaVoie MJ, Paliga K, Eggert S, Kimberly WT, Wasco W, Selkoe DJ (2003) 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, 6664-6673. (Pubitemid 36666107)
91. Chang KA, Kim HS, Ha TY, Ha JW, Shin KY, Jeong YH, Lee JP, Park CH, Kim S, Baik TK, Suh YH (2006) Phos-phorylation of amyloid precursor protein (APP) at Thr668 regulates the nuclear translocation of the APP intracellular domain and induces neurodegeneration. Mol Cell Biol 26, 4327-4338. (Pubitemid 43788031)
92. Walsh DM, Tseng BP, Rydel RE, Podlisny MB, Selkoe DJ (2000) The oligomerization of amyloid beta-protein begins intracellularly in cells derived from human brain. Biochemistry 39, 10831-10839.
93. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shep-ardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14, 837-842.
94. Walsh DM, Selkoe DJ (2007) A beta oligomers-a decade of discovery. J Neurochem 101, 1172-1184.
95. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M (2009) APP bindsDR6totrigger axon pruning and neuron death via distinct caspases. Nature 457, 981-989.
96. Jiang Y, Mullaney KA, Peterhoff CM, Che S, Schmidt SD, Boyer-Boiteau A, Ginsberg SD, Cataldo AM, Mathews PM, Nixon RA Alzheimer's-related endosome dysfunction in Down syndromeis Abeta-independent but requires APP and is reversed by BACE-1 inhibition. Proc Natl Acad Sci USA 107, 1630-1635.
97. Harada A, Oguchi K, Okabe S, Kuno J, Terada S, Ohshima T, Sato-Yoshitake R, Takei Y, Noda T, Hirokawa N (1994) Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369, 488-491. (Pubitemid 24210568)
98. Dawson HN, Ferreira A, Eyster MV, Ghoshal N, Binder LI, Vitek MP (2001) Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J Cell Sci 114, 1179-1187. (Pubitemid 32288531)
99. Gomez de Barreda E, Perez M, Gomez Ramos P, de Cristobal J, Martin-Maestro P, Moran A, Dawson HN, Vitek MP, Lucas JJ, Hernandez F, Avila J (2010) Tau-knockout mice show reduced GSK3-induced hippocampal degeneration and learning deficits. Neurobiol Dis 37, 622-629.
100. Nakaya T, Suzuki T (2006) Role of APP phosphorylation in FE65-dependent gene transactivation mediated by AICD. Genes Cells 11, 633-645. (Pubitemid 43744814)
101. Muresan Z, Muresan V (2005) c-Jun NH2-terminal kinase-interacting protein-3 facilitates phosphorylation and controls localization of amyloid-beta precursor protein. J Neurosci 25, 3741-3751. (Pubitemid 40570407)
102. Muresan Z, Muresan V (2007) The amyloid-beta precursor protein is phosphorylated via distinct pathways during differentiation, mitosis, stress, and degeneration. Mol Biol Cell 18, 3835-3844. (Pubitemid 47519477)
103. Lee TH, Tun-Kyi A, Shi R, Lim J, Soohoo C, Finn G, Bal-astik M, Pastorino L, Wulf G, Zhou XZ, Lu KP (2009) Essential role of Pin1 in the regulation of TRF1 stability and telomere maintenance. Nat Cell Biol 11, 97-105.