Tyr682 in the intracellular domain of APP regulates amyloidogenic APP processing in vivo

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Barbagallo, Alessia P M ^a   Weldon, Richard ^a   Tamayev, Robert ^a   Zhou, Dawang ^a   Giliberto, Luca ^c   Foreman, Oded ^b   D'Adamio, Luciano ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b JACKSON LABORATORY   (United States)

^c FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; TYROSINE; AMYLOID; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; IN VIVO STUDY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; ANIMAL; BINDING SITE; BRAIN; C57BL MOUSE; CELL CULTURE; GENE TARGETING; GENETICS; IMMUNOBLOTTING; METABOLISM; MUTATION; NERVE CELL; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPTOSOME;

MUS;

AMYLOID; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BINDING SITES; BRAIN; CELLS, CULTURED; GENE KNOCK-IN TECHNIQUES; IMMUNOBLOTTING; MICE; MICE, INBRED C57BL; MUTATION; NEURONS; PEPTIDE FRAGMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYNAPTOSOMES; TYROSINE;

EID: 78649496201     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015503     Document Type: Article

References (78)

1. Hardy JA, Higgins GA (1992) Alzheimer's disease: the amyloid cascade hypothesis. Science 256: 184-185.
2. Selkoe DJ (2000) The genetics and molecular pathology of Alzheimer's disease: roles of amyloid and the presenilins. Neurol Clin 18: 903-922.
3. Passer B, Pellegrini L, Russo C, Siegel RM, Lenardo MJ, et al. (2000) Generation of an apoptotic intracellular peptide by gamma-secretase cleavage of Alzheimer's amyloid beta protein precursor. J Alzheimers Dis 2: 289-301.
4. Cao X, Sudhof TC (2001) A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293: 115-120.
5. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, et al. (2005) Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307: 1282-1288.
6. Galvan V, Gorostiza OF, Banwait S, Ataie M, Logvinova AV, et al. (2006) 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: 7130-7135.
7. Zheng H, Jiang M, Trumbauer ME, Sirinathsinghji DJ, Hopkins R, et al. (1995) beta-Amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81: 525-531.
8. Ring S, Weyer SW, Kilian SB, Waldron E, Pietrzik CU, et al. (2007) The secreted beta-amyloid precursor protein ectodomain APPs alpha is sufficient to rescue the anatomical, behavioral, and electrophysiological abnormalities of APP-deficient mice. J Neurosci 27: 7817-7826.
9. Russo C, Salis S, Dolcini V, Venezia V, Song XH, et al. (2001) Amino-terminal modification and tyrosine phosphorylation of [corrected] carboxy-terminal fragments of the amyloid precursor protein in Alzheimer's disease and Down's syndrome brain. Neurobiol Dis 8: 173-180.
10. Austin SA, Combs CK (2008) Amyloid precursor protein mediates monocyte adhesion in AD tissue and apoE(2)/(2) mice. Neurobiol Aging.
11. Perez RG, Soriano S, Hayes JD, Ostaszewski B, Xia W, et al. (1999) Mutagenesis identifies new signals for beta-amyloid precursor protein endocytosis, turnover, and the generation of secreted fragments, including Abeta42. J Biol Chem 274: 18851-18856.
12. King GD, Cherian K, Turner RS (2004) X11alpha impairs gamma- but not beta-cleavage of amyloid precursor protein. J Neurochem 88: 971-982.
13. 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.
14. Tamayev R, Zhou D, D'Adamio L (2009) The interactome of the Amyloid betaeta Precursor Protein family members is shaped by phosphorylation of their intracellular domains. Mol Neurodegener 4: 28.
15. Giliberto L, Zhou D, Weldon R, Tamagno E, De Luca P, et al. (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.
16. Giliberto L, Borghi R, Piccini A, Mangerini R, Sorbi S, et al. (2009) Mutant presenilin 1 increases the expression and activity of BACE1. J Biol Chem 284: 9027-9038.
17. Schmidt SD, Nixon RA, Mathews PM (2005) ELISA method for measurement of amyloid-beta levels. Methods Mol Biol 299: 279-297.
18. Lanz TA, Schachter JB (2006) Demonstration of a common artifact in immunosorbent assays of brain extracts: development of a solid-phase extraction protocol to enable measurement of amyloid-beta from wild-type rodent brain. J Neurosci Methods 157: 71-81.
19. Minopoli G, Stante M, Napolitano F, Telese F, Aloia L, et al. (2007) Essential roles for Fe65, Alzheimer amyloid precursor-binding protein, in the cellular response to DNA damage. J Biol Chem 282: 831-835.
20. Sano Y, Nakaya T, Pedrini S, Takeda S, Iijima-Ando K, et al. (2006) Physiological mouse brain Abeta levels are not related to the phosphorylation state of threonine-668 of Alzheimer's APP. PLoS ONE 1: e51.
21. Huttunen HJ, Puglielli L, Ellis BC, MacKenzie Ingano LA, Kovacs DM (2009) Novel N-terminal cleavage of APP precludes Abeta generation in ACATdefective AC29 cells. J Mol Neurosci 37: 6-15.
22. Selkoe DJ, Yamazaki T, Citron M, Podlisny MB, Koo EH, et al. (1996) The role of APP processing and trafficking pathways in the formation of amyloid betaprotein. Ann N Y Acad Sci 777: 57-64.
23. Kaether C, Schmitt S, Willem M, Haass C (2006) Amyloid precursor protein and Notch intracellular domains are generated after transport of their precursors to the cell surface. Traffic 7: 408-415.
24. Ehehalt R, Keller P, Haass C, Thiele C, Simons K (2003) Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J Cell Biol 160: 113-123.
25. Reinhard C, Hebert SS, De Strooper B (2005) The amyloid-beta precursor protein: integrating structure with biological function. EMBO J 24: 3996-4006.
26. Zheng H, Koo EH (2006) The amyloid precursor protein: beyond amyloid. Mol Neurodegener 1: 5.
27. Turner PR, O'Connor K, Tate WP, Abraham WC (2003) Roles of amyloid precursor protein and its fragments in regulating neural activity, plasticity and memory. Prog Neurobiol 70: 1-32.
28. Mattson MP (1997) Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol Rev 77: 1081-1132.
29. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457: 981-989.
30. Puzzo D, Privitera L, Leznik E, Fa M, Staniszewski A, et al. (2008) Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus. J Neurosci 28: 14537-14545.
31. Hamid R, Kilger E, Willem M, Vassallo N, Kostka M, et al. (2007) Amyloid precursor protein intracellular domain modulates cellular calcium homeostasis and ATP content. J Neurochem 102: 1264-1275.
32. Madeira A, Pommet JM, Prochiantz A, Allinquant B (2005) SET protein (TAF1beta, I2PP2A) is involved in neuronal apoptosis induced by an amyloid precursor protein cytoplasmic subdomain. FASEB J 19: 1905-1907.
33. Cupers P, Orlans I, Craessaerts K, Annaert W, De Strooper B (2001) The amyloid precursor protein (APP)-cytoplasmic fragment generated by gammasecretase is rapidly degraded but distributes partially in a nuclear fraction of neurones in culture. J Neurochem 78: 1168-1178.
34. Pardossi-Piquard R, Petit A, Kawarai T, Sunyach C, Alves da Costa C, et al. (2005) Presenilin-dependent transcriptional control of the Abeta-degrading enzyme neprilysin by intracellular domains of betaAPP and APLP. Neuron 46: 541-554.
35. Liu Q, Zerbinatti CV, Zhang J, Hoe HS, Wang B, et al. (2007) Amyloid precursor protein regulates brain apolipoprotein E and cholesterol metabolism through lipoprotein receptor LRP1. Neuron 56: 66-78.
36. von Rotz RC, Kohli BM, Bosset J, Meier M, Suzuki T, et al. (2004) The APP intracellular domain forms nuclear multiprotein complexes and regulates the transcription of its own precursor. J Cell Sci 117: 4435-4448.
37. Kim HS, Kim EM, Lee JP, Park CH, Kim S, et al. (2003) C-terminal fragments of amyloid precursor protein exert neurotoxicity by inducing glycogen synthase kinase-3beta expression. FASEB J 17: 1951-1953.
38. Baek SH, Ohgi KA, Rose DW, Koo EH, Glass CK, et al. (2002) Exchange of NCoR corepressor and Tip60 coactivator complexes links gene expression by NFkappaB and beta-amyloid precursor protein. Cell 110: 55-67.
39. Checler F, Sunyach C, Pardossi-Piquard R, Sevalle J, Vincent B, et al. (2007) The gamma/epsilon-secretase-derived APP intracellular domain fragments regulate p53. Curr Alzheimer Res 4: 423-426.
40. Leissring MA, Murphy MP, Mead TR, Akbari Y, Sugarman MC, et al. (2002) A physiologic signaling role for the gamma -secretase-derived intracellular fragment of APP. Proc Natl Acad Sci U S A 99: 4697-4702.
41. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298: 789-791.
42. Buxbaum JD, Thinakaran G, Koliatsos V, O'Callahan J, Slunt HH, et al. (1998) Alzheimer amyloid protein precursor in the rat hippocampus: transport and processing through the perforant path. J Neurosci 18: 9629-9637.
43. Tienari PJ, De Strooper B, Ikonen E, Simons M, Weidemann A, et al. (1996) The beta-amyloid domain is essential for axonal sorting of amyloid precursor protein. EMBO J 15: 5218-5229.
44. Simons M, Ikonen E, Tienari PJ, Cid-Arregui A, Monning U, et al. (1995) Intracellular routing of human amyloid protein precursor: axonal delivery followed by transport to the dendrites. J Neurosci Res 41: 121-128.
45. Moya KL, Confaloni AM, Allinquant B (1994) In vivo neuronal synthesis and axonal transport of Kunitz protease inhibitor (KPI)-containing forms of the amyloid precursor protein. J Neurochem 63: 1971-1974.
46. Sisodia SS, Koo EH, Hoffman PN, Perry G, Price DL (1993) Identification and transport of full-length amyloid precursor proteins in rat peripheral nervous system. J Neurosci 13: 3136-3142.
47. Morin PJ, Abraham CR, Amaratunga A, Johnson RJ, Huber G, et al. (1993) Amyloid precursor protein is synthesized by retinal ganglion cells, rapidly transported to the optic nerve plasma membrane and nerve terminals, and metabolized. J Neurochem 61: 464-473.
48. Koo EH, Sisodia SS, Archer DR, Martin LJ, Weidemann A, et al. (1990) Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc Natl Acad Sci U S A 87: 1561-1565.
49. Kamal A, Stokin GB, Yang Z, Xia CH, Goldstein LS (2000) Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28: 449-459.
50. Lazarov O, Morfini GA, Lee EB, Farah MH, Szodorai A, et al. (2005) Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: revisited. J Neurosci 25: 2386-2395.
51. Matsuda S, Matsuda Y, D'Adamio L (2003) Amyloid beta protein precursor (AbetaPP), but not AbetaPP-like protein 2, is bridged to the kinesin light chain by the scaffold protein JNK-interacting protein 1. J Biol Chem 278: 38601-38606.
52. Inomata H, Nakamura Y, Hayakawa A, Takata H, Suzuki T, et al. (2003) A scaffold protein JIP-1b enhances amyloid precursor protein phosphorylation by JNK and its association with kinesin light chain 1. J Biol Chem 278: 22946-22955.
53. Muresan Z, Muresan V (2005) Coordinated transport of phosphorylated amyloid-beta precursor protein and c-Jun NH2-terminal kinase-interacting protein-1. J Cell Biol 171: 615-625.
54. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA, Goldstein LS (2001) Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 414: 643-648.
55. Praprotnik D, Smith MA, Richey PL, Vinters HV, Perry G (1996) Filament heterogeneity within the dystrophic neurites of senile plaques suggests blockage of fast axonal transport in Alzheimer's disease. Acta Neuropathol 91: 226-235.
56. Cash AD, Aliev G, Siedlak SL, Nunomura A, Fujioka H, et al. (2003) Microtubule reduction in Alzheimer's disease and aging is independent of tau filament formation. Am J Pathol 162: 1623-1627.
57. Kins S, Lauther N, Szodorai A, Beyreuther K (2006) Subcellular trafficking of the amyloid precursor protein gene family and its pathogenic role in Alzheimer's disease. Neurodegener Dis 3: 218-226.
58. Terry RD (1996) The pathogenesis of Alzheimer disease: an alternative to the amyloid hypothesis. J Neuropathol Exp Neurol 55: 1023-1025.
59. Stokin GB, Goldstein LS (2006) Axonal transport and Alzheimer's disease. Annu Rev Biochem 75: 607-627.
60. Stokin GB, Goldstein LS (2006) Linking molecular motors to Alzheimer's disease. J Physiol Paris 99: 193-200.
61. 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.
62. Pietrzik CU, Yoon IS, Jaeger S, Busse T, Weggen S, et al. (2004) FE65 constitutes the functional link between the low-density lipoprotein receptorrelated protein and the amyloid precursor protein. J Neurosci 24: 4259-4265.
63. Scheinfeld MH, Ghersi E, Davies P, D'Adamio L (2003) Amyloid beta protein precursor is phosphorylated by JNK-1 independent of, yet facilitated by, JNKinteracting protein (JIP)-1. J Biol Chem 278: 42058-42063.
64. Fiore F, Zambrano N, Minopoli G, Donini V, Duilio A, et al. (1995) The regions of the Fe65 protein homologous to the phosphotyrosine interaction/phosphotyrosine binding domain of Shc bind the intracellular domain of the Alzheimer's amyloid precursor protein. J Biol Chem 270: 30853-30856.
65. Kimura A, Horikoshi M (1998) Tip60 acetylates six lysines of a specific class in core histones in vitro. Genes Cells 3: 789-800.
66. Scheinfeld MH, Matsuda S, D'Adamio L (2003) JNK-interacting protein-1 promotes transcription of A beta protein precursor but not A beta precursor-like proteins, mechanistically different than Fe65. Proc Natl Acad Sci U S A 100: 1729-1734.
67. Balastik M, Lim J, Pastorino L, Lu KP (2007) Pin1 in Alzheimer's disease: multiple substrates, one regulatory mechanism? Biochim Biophys Acta 1772: 422-429.
68. Pastorino L, Sun A, Lu PJ, Zhou XZ, Balastik M, et al. (2006) The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production. Nature 440: 528-534.
69. Zhou D, Noviello C, D'Ambrosio C, Scaloni A, D'Adamio L (2004) Growth factor receptor-bound protein 2 interaction with the tyrosine-phosphorylated tail of amyloid beta precursor protein is mediated by its Src homology 2 domain. J Biol Chem 279: 25374-25380.
70. Russo C, Dolcini V, Salis S, Venezia V, Zambrano N, et al. (2002) 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: 35282-35288.
71. Tarr PE, Roncarati R, Pelicci G, Pelicci PG, D'Adamio L (2002) Tyrosine phosphorylation of the beta-amyloid precursor protein cytoplasmic tail promotes interaction with Shc. J Biol Chem 277: 16798-16804.
72. Ando K, Iijima KI, Elliott JI, Kirino Y, Suzuki T (2001) Phosphorylationdependent regulation of the interaction of amyloid precursor protein with Fe65 affects the production of beta-amyloid. J Biol Chem 276: 40353-40361.
73. Lee MS, Kao SC, Lemere CA, Xia W, Tseng HC, et al. (2003) APP processing is regulated by cytoplasmic phosphorylation. J Cell Biol 163: 83-95.
74. Cao X, Sudhof TC (2004) Dissection of amyloid-beta precursor proteindependent transcriptional transactivation. J Biol Chem 279: 24601-24611.
75. Russo T, Faraonio R, Minopoli G, De Candia P, De Renzis S, et al. (1998) Fe65 and the protein network centered around the cytosolic domain of the Alzheimer's beta-amyloid precursor protein. FEBS Lett 434: 1-7.
76. Trommsdorff M, Borg JP, Margolis B, Herz J (1998) Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J Biol Chem 273: 33556-33560.
77. Ulery PG, Beers J, Mikhailenko I, Tanzi RE, Rebeck GW, et al. (2000) Modulation of beta-amyloid precursor protein processing by the low density lipoprotein receptor-related protein (LRP). Evidence that LRP contributes to the pathogenesis of Alzheimer's disease. J Biol Chem 275: 7410-7415.
78. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.