Fe65 Ser228 is phosphorylated by ATM/ATR and inhibits Fe65-APP-mediated gene transcription

Biochemical Journal

Volumn 465, Issue , 2015, Pages 413-421

  Jowsey, Paul A ^a   Blain, Peter G ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Alzheimer's disease; Amyloid precursor protein; DNA damage; Fe65; Protein phosphorylation transcriptional regulation

Indexed keywords

ALANINE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; ATM PROTEIN; ATR PROTEIN; CELL DNA; CHECKPOINT KINASE RAD3; PROTEIN FE65; SERINE; APBB1 PROTEIN, HUMAN; ATM PROTEIN, HUMAN; ATR PROTEIN, HUMAN; NERVE PROTEIN; NUCLEAR PROTEIN;

ALZHEIMER DISEASE; ARTICLE; ATAXIA TELANGIECTASIA; CELLULAR DISTRIBUTION; DNA DAMAGE; DNA STRAND BREAKAGE; ENZYME ACTIVATION; GENE MUTATION; GENETIC TRANSCRIPTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TRANSCRIPTION INITIATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

MUS;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; HEK293 CELLS; HUMANS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; SERINE; TRANSCRIPTION, GENETIC;

EID: 84921651771     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140656     Document Type: Article

References (36)

1. McLoughlin, D. M. and Miller, C. C. (2008) The FE65 proteins and Alzheimer's disease. J. Neurosci. Res. 86, 744-754 CrossRef PubMed
2. Borg, J. P., Ooi, J., Levy, E. and 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 PubMed
3. McLoughlin, D. M. and Miller, C. C. (1996) The intracellular cytoplasmic domain of the Alzheimer's disease amyloid precursor protein interacts with phosphotyrosine-binding domain proteins in the yeast two-hybrid system. FEBS Lett. 397, 197-200 CrossRef PubMed
4. De Strooper, B. and Annaert, W. (2000) Proteolytic processing and cell biological functions of the amyloid precursor protein. J. Cell Sci. 113, 1857-1870 PubMed
5. Benilova, I., Karran, E. and De Strooper, B. (2012) The toxic Ainnodatabeta oligomer and Alzheimer's disease: an emperor in need of clothes. Nat. Neurosci. 15, 349-357 CrossRef PubMed
6. Kimberly, W. T., Zheng, J. B., Guenette, S. Y. and Selkoe, D. J. (2001) The intracellular domain of the innodatabeta -amyloid precursor protein is stabilized by Fe65 and translocates to the nucleus in a notch-like manner. J. Biol. Chem. 276, 40288-40292 CrossRef PubMed
7. Kinoshita, A., Whelan, C. M., Smith, C. J., Berezovska, O. and Hyman, B. T. (2002) Direct visualization of the ã secretase-generated carboxyl-terminal domain of the amyloid precursor protein: association with Fe65 and translocation to the nucleus. J. Neurochem. 82, 839-847 CrossRef PubMed
8. 668 regulates the nuclear translocation of the APP intracellular domain and induces neurodegeneration. Mol. Cell. Biol. 26, 4327-4338 CrossRef PubMed
9. Kim, H. S., Kim, E. M., Lee, J. P., Park, C. H., Kim, S., Seo, J. H., Chang, K. A., Yu, E., Jeong, S. J., Chong, Y. H. and Suh, Y. H. (2003) C-terminal fragments of amyloid precursor protein exert neurotoxicity by inducing glycogen synthase kinase-3β expression. FASEB J. 17, 1951-1953 PubMed
10. Telese, F., Bruni, P., Donizetti, A., Gianni, D., D'Ambrosio, C., Scaloni, A., Zambrano, N., Rosenfeld, M. G. and Russo, T. (2005) Transcription regulation by the adaptor protein Fe65 and the nucleosome assembly factor SET. EMBO Rep. 6, 77-82 CrossRef PubMed
11. von Rotz, R. C., Kohli, B. M., Bosset, J., Meier, M., Suzuki, T., Nitsch, R. M. and 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 CrossRef PubMed
12. Cao, X. and Südhof, T. C. (2001) A transcriptionally active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293, 115-120 CrossRef PubMed
13. Ando, K., Iijima, K. I., Elliott, J. I., Kirino, Y. and Suzuki, T. (2001) Phosphorylation-dependent regulation of the interaction of amyloid precursor protein with Fe65 affects the production of β-amyloid. J. Biol. Chem. 276, 40353-40361 CrossRef PubMed
14. 682 in the intracellular domain of APP regulates amyloidogenic APP processing in vivo. PLoS ONE 5, e15503 CrossRef PubMed
15. Sabo, S. L., Lanier, L. M., Ikin, A. F., Khorkova, O., Sahasrabudhe, S., Greengard, P. and Buxbaum, J. D. (1999) Regulation of β-amyloid secretion by FE65, an amyloid protein precursor-binding protein. J. Biol. Chem. 274, 7952-7957 CrossRef PubMed
16. Xie, Z., Dong, Y., Maeda, U., Xia, W. and Tanzi, R. E. (2007) RNA interference silencing of the adaptor molecules ShcC and Fe65 differentially affect amyloid precursor protein processing and Aβ generation. J. Biol. Chem. 282, 4318-4325 CrossRef PubMed
17. Minopoli, G., de Candia, P., Bonetti, A., Faraonio, R., Zambrano, N. and Russo, T. (2001) The β-amyloid precursor protein functions as a cytosolic anchoring site that prevents Fe65 nuclear translocation. J. Biol. Chem. 276, 6545-6550 CrossRef PubMed
18. Perkinton, M. S., Standen, C. L., Lau, K. F., Kesavapany, S., Byers, H. L., Ward, M., McLoughlin, D. M. and Miller, C. C. (2004) The c-Abl tyrosine kinase phosphorylates the Fe65 adaptor protein to stimulate Fe65/amyloid precursor protein nuclear signaling. J. Biol. Chem. 279, 22084-22091 CrossRef PubMed
19. Sumioka, A., Nagaishi, S., Yoshida, T., Lin, A., Miura, M. and Suzuki, T. (2005) Role of 14-3-3γ in FE65-dependent gene transactivation mediated by the amyloid β-protein precursor cytoplasmic fragment. J. Biol. Chem. 280, 42364-42374 CrossRef PubMed
20. Lau, K. F., Chan, W. M., Perkinton, M. S., Tudor, E. L., Chang, R. C., Chan, H. Y., McLoughlin, D. M. and Miller, C. C. (2008) Dexras1 interacts with FE65 to regulate FE65-amyloid precursor protein-dependent transcription. J. Biol. Chem. 283, 34728-34737 CrossRef PubMed
21. Minopoli, G., Stante, M., Napolitano, F., Telese, F., Aloia, L., De Felice, M., Di Lauro, R., Pacelli, R., Brunetti, A., Zambrano, N. and Russo, T. (2007) Essential roles for Fe65, Alzheimer amyloid precursor-binding protein, in the cellular response to DNA damage. J. Biol. Chem. 282, 831-835 CrossRef PubMed
22. Saeki, K., Nose, Y., Hirao, N., Takasawa, R. and Tanuma, S. (2011) Amyloid precursor protein binding protein Fe65 is cleaved by caspases during DNA damage-induced apoptosis. Biol. Pharm. Bull. 34, 290-294 CrossRef PubMed
23. Stante, M., Minopoli, G., Passaro, F., Raia, M., Vecchio, L. D. and Russo, T. (2009) Fe65 is required for Tip60-directed histone H4 acetylation at DNA strand breaks. Proc. Natl. Acad. Sci. U.S.A. 106, 5093-5098 CrossRef PubMed
24. Abraham, R. T. (2004) PI 3-kinase related kinases: 'big' players in stress-induced signaling pathways. DNA Repair 3, 883-887 CrossRef PubMed
25. Hurley, P. J. and Bunz, F. (2007) ATM and ATR: components of an integrated circuit. Cell Cycle 6, 414-417 CrossRef PubMed
26. Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, 3rd, E. R., Hurov, K. E., Luo, J., Bakalarski, C. E., Zhao, Z., Solimini, N., Lerenthal, Y. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 CrossRef PubMed
27. Traven, A. and Heierhorst, J. (2005) SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damage-response proteins. BioEssays 27, 397-407 CrossRef PubMed
28. Cuesta, A., Zambrano, A., Lopez, E. and Pascual, A. (2009) Thyroid hormones reverse the UV-induced repression of APP in neuroblastoma cells. FEBS Lett. 583, 2401-2406 CrossRef PubMed
29. Almenar-Queralt, A., Falzone, T. L., Shen, Z., Lillo, C., Killian, R. L., Arreola, A. S., Niederst, E. D., Ng, K. S., Kim, S. N., Briggs, S. P. et al. (2014) UV irradiation accelerates amyloid precursor protein (APP) processing and disrupts APP axonal transport. J. Neurosci. 34, 3320-3339 CrossRef PubMed
30. Cuesta, A., Zambrano, A., Royo, M. and Pascual, A. (2009) The tumour suppressor p53 regulates the expression of amyloid precursor protein (APP). Biochem. J. 418, 643-650 CrossRef PubMed
31. Shiloh, Y. and Ziv, Y. (2013) The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol. 14, 197-210 CrossRef
32. Bencokova, Z., Kaufmann, M. R., Pires, I. M., Lecane, P. S., Giaccia, A. J. and Hammond, E. M. (2009) ATM activation and signaling under hypoxic conditions. Mol. Cell. Biol. 29, 526-537 CrossRef PubMed
33. Guo, Z., Kozlov, S., Lavin, M. F., Person, M. D. and Paull, T. T. (2010) ATM activation by oxidative stress. Science 330, 517-521 CrossRef PubMed
34. Yang, D. Q. and Kastan, M. B. (2000) Participation of ATM in insulin signalling through phosphorylation of eIF-4E-binding protein 1. Nat. Cell Biol. 2, 893-898 CrossRef PubMed
35. Ermekova, K. S., Zambrano, N., Linn, H., Minopoli, G., Gertler, F., Russo, T. and Sudol, M. (1997) The WW domain of neural protein FE65 interacts with proline-rich motifs in Mena, the mammalian homolog of Drosophila enabled. J. Biol. Chem. 272, 32869-32877 CrossRef PubMed
36. Zambrano, N., Bruni, P., Minopoli, G., Mosca, R., Molino, D., Russo, C., Schettini, G., Sudol, M. and Russo, T. (2001) The innodatabeta -amyloid precursor protein APP is tyrosine-phosphorylated in cells expressing a constitutively active form of the Abl protoncogene. J. Biol. Chem. 276, 19787-19792 CrossRef PubMed