Identification of a novel complex AβPP:Fe65:PP1 that regulates AβPP Thr668 phosphorylation levels

Journal of Alzheimer's Disease

Volumn 35, Issue 4, 2013, Pages 761-775

  Rebelo, Sandra ^a   Domingues, Sara C ^a   Santos, Mariana ^a   Fardilha, Margarida ^a   Esteves, Sara L C ^a   Vieira, Sandra Isabel ^a   Vintém, Ana Paula B ^a   Wu, Wenjuan ^a   Da Cruz E Silva, Edgar F ^a   Da Cruz E Silva, Odete A B ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

PP1 binding protein; Primary cultures; protein phosphatases; protein phosphorylation; subcellular localization; yeast tri hybrid

Indexed keywords

AMYLOID PRECURSOR PROTEIN; AMYLOID PRECURSOR PROTEIN THR 688; BINDING PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN FE65; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; HIPPOCAMPUS; IMMUNOPRECIPITATION; IN VIVO STUDY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT;

EID: 84878877274     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-130095     Document Type: Article

References (64)

1. Jin LW, Saitoh T (1995) Changes in protein kinases in brain aging and Alzheimer's disease. Implications for drug therapy. Drugs Aging 6, 136-149.
2. Gong CX, Singh TJ, Grundke-Iqbal I, Iqbal K (1993) Phosphoprotein phosphatase activities in Alzheimer disease brain. J Neurochem 61, 921-927.
3. Matsushima H, Shimohama S, Chachin M, Taniguchi T, Kimura J (1996) Ca2+-dependent and Ca2+-independent protein kinaseCchanges in the brain of patients with Alzheimer's disease. J Neurochem 67, 317-323.
4. Bennecib M, Gong CX, Grundke-Iqbal I, Iqbal K (2000) Role of protein phosphatase-2A and-1 in the regulation of GSK-3, cdk5 and cdc2 and the phosphorylation of tau in rat forebrain. FEBS Lett 485, 87-93.
5. Hata R, Masumura M, Akatsu H, Li F, Fujita H, Nagai Y, Yamamoto T, Okada H, Kosaka K, Sakanaka M, Sawada T (2001) Up-regulation of calcineurin Abeta mRNA in the Alzheimer's disease brain: Assessment by cDNA microarray. Biochem Biophys Res Commun 284, 310-316.
6. Vijayan S, El-Akkad E, Grundke-Iqbal I, Iqbal K (2001) A pool of beta-tubulin is hyperphosphorylated at serine residues in Alzheimer disease brain. FEBS Lett 509, 375-381.
7. Nitsch RM, Slack BE, Wurtman RJ, Growdon JH (1992) Release of Alzheimer amyloid precursor derivatives stimulated by activation of muscarinic acetylcholine receptors. Science 258, 304-307.
8. Selkoe DJ (1993) Physiological production of the betaamyloid protein and the mechanism of Alzheimer's disease. Trends Neurosci 16, 403-409.
9. Gong CX, Grundke-Iqbal I, Damuni Z, Iqbal K (1994) Dephosphorylation of microtubule-associated protein tau by protein phosphatase-1 and-2C and its implication in Alzheimer disease. FEBS Lett 341, 94-98.
10. Gong CX, Singh TJ, Grundke-Iqbal I, Iqbal K (1994) Alzheimer's disease abnormally phosphorylated tau is dephosphorylated by protein phosphatase-2B (calcineurin). J Neurochem 62, 803-806.
11. Gong CX, Shaikh S,Wang JZ, Zaidi T, Grundke-Iqbal I, Iqbal K(1995) Phosphatase activity toward abnormally phosphorylated tau: Decrease in Alzheimer disease brain. J Neurochem 65, 732-738.
12. Shima H, Hatano Y, Chun YS, Sugimura T, Zhang Z, Lee EY, Nagao M (1993) Identification of PP1 catalytic subunit isotypes PP1 gamma 1, PP1 delta and PP1 alpha in various rat tissues. Biochem Biophys Res Commun 192, 1289-1296.
13. da Cruze Silva EF, Fox CA, Ouimet CC, Gustafson E, Watson SJ, Greengard P (1995) Differential expression of protein phosphatase 1 isoforms in mammalian brain. J Neurosci 15, 3375-3389.
14. Vieira SI, Rebelo S, Esselmann H, Wiltfang J, Lah J, Lane R, Small SA, Gandy S, da Cruz ESEF, da Cruz ESOA (2010) Retrieval of the Alzheimer's amyloid precursor protein from the endosome to the TGN is S655 phosphorylation statedependent and retromer-mediated. Mol Neurodegener 5, 40.
15. Rebelo S, Vieira SI, Esselmann H,Wiltfang J, da Cruze Silva EF, da Cruze Silva OA (2007) Tyrosine 687 phosphorylated Alzheimer's amyloid precursor protein is retained intracellularly and exhibits a decreased turnover rate. Neurodegener Dis 4, 78-87.
16. Rebelo S, Vieira SI, Esselmann H, Wiltfang J, da Cruze Silva EF, da Cruze Silva OA (2007) Tyr687 dependent APP endocytosis and Abeta production. J Mol Neurosci 32, 1-8.
17. Vieira SI, Rebelo S, Domingues SC, da Cruze Silva EF, da Cruze Silva OA (2009) S655 phosphorylation enhances APP secretory traffic. Mol Cell Biochem 328, 145-154.
18. Walter J, Fluhrer R, Hartung B,Willem M, Kaether C, Capell A, Lammich S, Multhaup G, Haass C (2001) Phosphorylation regulates intracellular trafficking of beta-secretase. J Biol Chem 276, 14634-14641.
19. Fiore F, Zambrano N, Minopoli G, Donini V, Duilio A, Russo T (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.
20. Borg JP, Ooi J, Levy E, Margolis B (1996) The phosphotyrosine interaction domains of X11 and FE65 bind to distinct sites on the YENPTY motif of amyloid precursor protein. Mol Cell Biol 16, 6229-6241.
21. 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.
22. 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.
23. Sabo SL, Ikin AF, Buxbaum JD, Greengard P (2003) The amyloid precursor protein and its regulatory protein, FE65, in growth cones and synapses in vitro and in vivo. J Neurosci 23, 5407-5415.
24. 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.
25. Scheinfeld MH, Ghersi E, Laky K, Fowlkes BJ, D'Adamio L (2002) Processing of beta-amyloid precursor-like protein-1 and-2 by gamma-secretase regulates transcription. J Biol Chem 277, 44195-44201.
26. da Cruze Silva O, Vieira SI, Rebelo S, da Cruze Silva EF (2004) A model system to study intracellular trafficking and processing of the Alzheimer's amyloid precursor protein. Neurodegener Dis 1, 196-204.
27. da Cruze Silva OA, Iverfeldt K, Oltersdorf T, Sinha S, Lieberburg I, Ramabhadran TV, Suzuki T, Sisodia SS, Gandy S, Greengard P (1993) Regulated cleavage of Alzheimer betaamyloid precursor protein in the absence of the cytoplasmic tail. Neuroscience 57, 873-877.
28. Rebelo S, Vieira SI, Esselmann H,Wiltfang J, da Cruz ESEF, da Cruz ESOA (2007) Try687 dependent APP endocytosis and Abeta production. J Mol Neurosci 32, 1-8.
29. Fardilha M,Wu W, Sa R, Fidalgo S, Sousa C, Mota C, da Cruze Silva OA, da Cruze Silva EF (2004) Alternatively spliced protein variants as potential therapeutic targets for male infertility and contraception. Ann N Y Acad Sci 1030, 468-478.
30. Rebelo S, Henriques AG, da Cruze Silva EF, da Cruze Silva OA (2004) Effect of cell density on intracellular levels of the Alzheimer's amyloid precursor protein. J Neurosci Res 76, 406-414.
31. Henriques AG, Vieira SI, Rebelo S, Domingues SC, da Cruze Silva EF, da Cruze Silva OA(2007) Isoform specific amyloidbeta protein precursor metabolism. J Alzheimers Dis 11, 85-95.
32. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35, 567-576.
33. Watanabe T, da Cruze Silva EF, Huang HB, Starkova N,Kwon YG, Horiuchi A, Greengard P, Nairn AC (2003) Preparation and characterization of recombinant protein phosphatase 1. Methods Enzymol 366, 321-338.
34. Gouras GK, Tsai J, Naslund J,Vincent B, Edgar M, Checler F, Greenfield JP, HaroutunianV, Buxbaum JD, Xu H, Greengard P, Relkin NR (2000) Intraneuronal Ab 42 accumulation in human brain. Am J Pathol 156, 15-20.
35. Fardilha M, Esteves SL, Korrodi-Gregorio L, da Cruze Silva OA, da Cruze Silva FF (2010) The physiological relevance of protein phosphatase 1 and its interacting proteins to health and disease. Curr Med Chem 17, 3996-4017.
36. da Cruze Silva E, Fardilha M, da Cruze Silva O (2005) Characterization of the human testis protein phosphatase 1 interactome and its relevance to sperm motility. Biol Reprod SI, 251-252.
37. da Cruze Silva EF, da Cruze Silva OA, Zaia CT, Greengard P (1995) Inhibition of protein phosphatase 1 stimulates secretion of Alzheimer amyloid precursor protein. Mol Med 1, 535-541.
38. DeKosky ST, Scheff SW(1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: Correlation with cognitive severity. Ann Neurol 27, 457-464.
39. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann Neurol 30, 572-580.
40. Mulkey RM, Endo S, Shenolikar S, Malenka RC (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369, 486-488.
41. Genoux D, Haditsch U, Knobloch M, Michalon A, Storm D, Mansuy IM (2002) Protein phosphatase 1 is a molecular constraint on learning and memory. Nature 418, 970-975.
42. Waddell S (2003) Protein phosphatase 1 and memory: Practice makes PP1 imperfect? Trends Neurosci 26, 117-119.
43. Ouimet CC, da Cruze Silva EF, Greengard P (1995) The alpha and gamma 1 isoforms of protein phosphatase 1 are highly and specifically concentrated in dendritic spines. Proc Natl Acad Sci U S A 92, 3396-3400.
44. da Cruze Silva OA, Fardilha M, Henriques AG, Rebelo S, Vieira S, da Cruze Silva EF (2004) Signal transduction therapeutics: Relevance for Alzheimer's disease. J Mol Neurosci 23, 123-142.
45. Ando K, Oishi M, Takeda S, Iijima K, Isohara T, Nairn AC, Kirino Y, Greengard P, Suzuki T (1999) Role of phosphorylation of Alzheimer's amyloid precursor protein during neuronal differentiation. J Neurosci 19, 4421-4427.
46. 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.
47. Iijima K, Ando K, Takeda S, Satoh Y, Seki T, Itohara S, Greengard P, Kirino Y, Nairn AC, Suzuki T (2000) Neuron-specific phosphorylation of Alzheimer's betaamyloid precursor protein by cyclin-dependent kinase 5. J Neurochem 75, 1085-1091.
48. Mueller HT, Borg JP, Margolis B, Turner RS (2000) Modulation of amyloid precursor protein metabolism by X11alpha /Mint-1. A deletion analysis of protein-protein interaction domains. J Biol Chem 275, 39302-39306.
49. Roncarati R, Sestan N, Scheinfeld MH, Berechid BE, Lopez PA, Meucci O, McGlade JC, Rakic P, D'Adamio L (2002) The gamma-secretase-generated intracellular domain of betaamyloid precursor protein binds Numb and inhibits Notch signaling. Proc Natl Acad Sci U S A 99, 7102-7107.
50. Gong CX, Grundke-Iqbal I, Iqbal K (1994) Dephosphorylation of Alzheimer's disease abnormally phosphorylated tau by protein phosphatase-2A. Neuroscience 61, 765-772.
51. 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.
52. Suzuki T, Oishi M, Marshak DR, Czernik AJ, Nairn AC, Greengard P (1994) Cell cycle-dependent regulation of the phosphorylation and metabolism of the Alzheimer amyloid precursor protein. EMBO J 13, 1114-1122.
53. Aplin AE, Gibb GM, Jacobsen JS, Gallo JM, Anderton BH (1996) In vitro phosphorylation of the cytoplasmic domain of the amyloid precursor protein by glycogen synthase kinase-3beta. J Neurochem 67, 699-707.
54. Oishi M, Nairn AC, Czernik AJ, Lim GS, Isohara T, Gandy SE, Greengard P, Suzuki T (1997) The cytoplasmic domain of Alzheimer's amyloid precursor protein is phosphorylated at Thr654, Ser655, and Thr668 in adult rat brain and cultured cells. Mol Med 3, 111-123.
55. 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.
56. Standen CL, Brownlees J, Grierson AJ, Kesavapany S, Lau KF, McLoughlin DM, Miller CC (2001) Phosphorylation of thr(668) in the cytoplasmic domain of the Alzheimer's disease amyloid precursor protein by stress-activated protein kinase 1b (Jun N-terminal kinase-3). J Neurochem 76, 316-320.
57. 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.
58. Feyt C, Pierrot N, Tasiaux B,Van Hees J, Kienlen-Campard P, Courtoy PJ, Octave JN (2007) Phosphorylation of APP695 at Thr668 decreases gamma-cleavage and extracellular Abeta. Biochem Biophys Res Commun 357, 1004-1010.
59. 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.
60. Baek SH, Ohgi KA, Rose DW, Koo EH, Glass CK, Rosenfeld MG (2002) Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 110, 55-67.
61. von Rotz RC, Kohli BM, Bosset J, Meier M, Suzuki T, Nitsch RM,KonietzkoU(2004) The APP intracellular domain forms nuclear multiprotein complexes and regulates the transcription of its own precursor. J Cell Sci 117, 4435-4448.
62. Kim HS, Kim EM, Lee JP, Park CH, Kim S, Seo JH, Chang KA, Yu E, Jeong SJ, Chong YH, Suh YH (2003) C-terminal fragments of amyloid precursor protein exert neurotoxicity by inducing glycogen synthase kinase-3beta expression. FASEB J 17, 1951-1953.
63. Bennett D (2005) Transcriptional control by chromosomeassociated protein phosphatase-1. Biochem Soc Trans 33, 1444-1446.
64. Moorhead GB, Trinkle-Mulcahy L, Ulke-Lemee A (2007) Emerging roles of nuclear protein phosphatases. Nat Rev Mol Cell Biol 8, 234-244.